Mechanisms and Deployment of Resistance in Trees To Insects

Mechanisms and Deployment of Resistance in Trees to Insects
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Mechanisms and
Deployment of
Resistance in Trees
to Insects
Edited by
Michael R. Wagner
School of Forestry,
Northern Arizona University, Flagstaff, AZ, U.S.A.
Karen M. Clancy
Rocky Mountain Research Station,
Flagstaff, AZ, U.S.A.
François Lieutier
Université d’Orléans, Orléans, France and
Institut National de la Recherche Agronomique, Orléans, France
and
Timothy D. Paine
Department of Entomology,
University of California, Riverside, CA, U.S.A.
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Table of Contents
Preface vii
Acknowledgement ix
Chapter 1 Resistance in trees to insects – An overview of mechanisms and

interactions .... 1
S. LARSON
Chapter 2 Mechanisms of resistance in conifers and bark beetle attack

strategies 31
F. LIEUTIER
Chapter 3 Mechanisms of resistance in trees to defoliators 79

K. CLANCY
Chapter 4 Mechanisms of resistance in conifers against shoot infesting

insects.The case of the white pine weevil Pissodes strobi (Peck)
(Coleoptera: Curculionidae) 105
R. I. ALFARO, J. H. BORDEN, J. N. KING, E. S. TOMLIN, R. L. MCINTOSH,
J. BOHLMANN
Chapter 5 Host tree resistance to wood-boring insects 131

T. D. PAINE
Chapter 6 Plant resistance against gall-forming insects: the role of

hypersensitivity ....... 137
T. G. CORNELISSEN, D. NEGREIROS, G.W. FERNANDES
Chapter 7 The resistance of hybrid willows to specialist and generalist

herbivores and pathogens: the potential role of secondary chemistry and
parent host plant status 153
J. HJÄLTÉN, P. HALLGREN
Chapter 8 Deploying pest resistance in genetically-limited forest

plantations: developing ecologically-based strategues for managing risk
169
D. J. ROBISON
vi
Chapter 9 Deployment of tree resistance to insects in short-rotation

Populus plantations 189
D. R. COYLE, J. D. MCMILLIN, R. B. HALL, E. HART
Chapter 10 Strategies for Deployment of Insect Resistant Ornamental

Plants 217
D. A. HERMS
Chapter 11 Possibilities to utilize tree resistance to insects in forest pest

management in central and western Europe 239
C.M. HEIDGER and F. LIEUTIER
Chapter 12 Deployment of tree resistance to pests in Asia 265

N. KAMATA.
Chapter 13 Using resistance in tropical forest plantations ... 287

J. D. NICHOLS, M. R. WAGNER, J. R. COBBINAH
Keyword Index 311

Species Index 325
Preface
This book is the result of an international symposium that was held in

Iguassu Falls, Brazil August 20-26, 2000 as part of the International Congress
of Entomology. The symposium was organized by the International Union of
Forest Research Organizations (IUFRO) Working Party S7.01.02, Tree
Resistance to Insects which is part of the IUFRO Subject Group S7.01 –
Physiology and Genetics of Tree-Phytophage Interactions. The organizers of
this symposium were the editors of this book and all are members of the
IUFRO Working Party. Contributors were invited members of the IUFRO
Working Party with particular knowledge in some aspect of deployment and
mechanisms of resistance. All papers presented in this book were peer
reviewed prior to their acceptance.
This book reviews the major worldwide literature on mechanisms and
deployment of resistance in trees to insects. General patterns in the
mechanisms of resistance for defoliators, shoot insects, wood borers, bark
beetles, and gall forming insects are presented. Strategies for deployment of
tree resistance in short-rotation biomass plantations, horticulture, and natural
forests are discussed. Regional patterns of deployment of resistance for
Europe, Asia, and Tropical Forests illustrate the extent to which foresters are
currently using environmentally appropriate genetic resistance as a pest
management tool. Overview chapters synthesize many of the broad patterns
and provide guidance for future research and implementation of genetic
resistance in trees to insects.
Michael R. Wagner
Karen M. Clancy
Francois Lieutier
Timothy D. Paine
vii
Acknowledgment
The authors gratefully acknowledge the generous support of Northern

Arizona University School of Forestry McIntire-Stennis Program; the USDA
Forest Service Research and Development, Rocky Mountain Research Station
and the University of California-Riverside University of California-Riverside
Department of Entomology for partial underwriting of the cost of printing and
distribution of this book. Special thanks to Yiqun Lin, Northern Arizona
University School of Forestry for editorial assistance and to Maia Dickerson at
the Rocky Mountain Research Station for assistance in checking the literature
citations. Finally our thanks to all members of the IUFRO Working Party
S7.01.02 Tree Resistance to Insects for the many years of free exchange of
ideas about tree resistance to insects that make this type of overview
publication possible.
Michael R. Wagner
Karen M. Clancy
Francois Lieutier
Timothy D. Paine
ix
CHAPTER 1
RESISTANCE IN TREES TO INSECTS – AN

OVERVIEW OF MECHANISMS AND
INTERACTIONS
STIG LARSSON
Department of Entomology, Swedish University of Agricultural Sciences, Box 7044,SE-750 07

Uppsala, Sweden
1. INTRODUCTION
The use of insect-resistant plant varieties is an important part of integrated pest
management in agriculture. Classic breeding for insect resistance includes extensive
screening of a large number of genotypes in a common environment, selection of the
most promising genotypes for testing in field trials, and then production of new
crosses based on data from field tests (Maxwell and Jennings 1980). Forest
management has, on the other hand, to handle long rotation times, in certain
ecosystems a hundred years or more. Obviously, under such circumstances it is not
easy to apply the traditional breeding techniques developed for agricultural crops.
Consequently, few tree genotypes exist that have been intentionally bred for
resistance against insects (Hanover 1980).
There is no doubt, however, that tree resistance plays an important role in the
ecology of forest insects. Variation in traits likely to confer resistance to insects has
been found within many natural plant populations, including trees (Marquis 1992).
In managed forests, damage caused by insects varies among stands, varieties
(provenances, clones), and individual trees, sometimes due to documented
differences in resistance (Leather 1996). An often discussed aspect of tree resistance
is the suggested abiotic induction of tree susceptibility that may trigger insect
outbreaks (Mattson and Haack 1987).
Although it has long been accepted that tree resistance needs to be considered in
insect pest management models (Stark 1965), it has been difficult to achieve this
goal because of the poor mechanistic understanding of the resistance. However, the
1
M.R. Wagner et al. (eds.), Mechanisms and Deployment of Resistance in Trees to Insects, 1–29.
© 2002 Kluwer Academic Publishers. Printed in the Netherlands.
2 S. LARSSON
last two decades have seen an impressive development of conceptual models on

mechanisms involved in the interaction between plant and insect. Initially,
plant/insect interactions were studied mainly from an ecological perspective. In
recent years, breakthroughs in molecular techniques have made it possible to address
questions at the cellular level.
A challenge for the future will be to combine the ecological and the molecular
paradigms in order to develop reliable models of tree resistance. Such models will
be important for ecologists who aim to explain the abundance and distribution of
insect populations, as well as for forest managers who aim to include resistant tree
genotypes into forest pest management strategies. In order for such models to be
successful, we need to acknowledge that questions asked at different levels of
organization, i.e., cell, individual, population, will inevitably yield different kinds of
answers. It will be essential to develop research tools that view resistance
mechanisms from this variety of organization levels (Rausher 2001).
2. CONCEPTS AND DEFINITIONS

The resistance concept has its roots in plant breeding research (e.g., Painter 1958;
Maxwell and Jennings 1980). During recent years ecologists have elaborated on the
breeding concepts but without consistency in terminology. This is not the place to
thoroughly discuss the conceptual basis of resistance and related terms, but it is
important to define a few key concepts. For the purpose of this chapter I follow,
with some modifications, the definitions proposed by Karban and Baldwin (1997),
and Strauss and Agrawal (1999). This view is different from the Painter (1958)
definition in that it separates resistance from tolerance (see Fig. 1). Painter’s
definition focuses on damage to the plant; any plant characters that minimize
damage will contribute to resistance, be they toxins, deterrents or compensatory
processes. Thus, he viewed compensation, or tolerance, as one component of
resistance, and others after him have adopted this view (e.g., Berenbaum and
Zangerl 1992a). Research during the last decade has emphasized the importance of
tolerance as a plant strategy to reduce negative effects of herbivory (Stowe et al.
2000; Haukioja and Koricheva 2001). It appears that resistance and tolerance may
be alternatives, and because they both carry costs they cannot simultaneously be
maximized in one and the same plant genotype (Fineblum and Rausher 1995). Thus,
there are good theoretical reasons to treat them as qualitatively different solutions
for reducing fitness costs in response to herbivory. Still, our understanding of
tolerance lags behind that of resistance, although tolerance may be much more
important than generally acknowledged (Hjältén et al. 1993).
Resistance as defined here is not primarily related to plant damage, as opposed to
Painter's (1958) definition, but instead focuses on the negative effect a resistant plant
has on the target herbivore. It is important to separate the concept of resistance into
its two parts, the plant component, the resistant trait, and the insect response
(behavioral or physiological) to this trait. I consider the interaction between the plant
trait and the insect response to constitute the mechanism of resistance (see Fig. 1).
Thus defined, a resistance mechanism cannot be described unless both the plant trait
MECHANISMS AND INTERACTIONS - AN OVERVIEW 3
and the target herbivore are identified. A resistance trait such as a toxic chemical,
trichomes, or thick bark can have evolved in response to a number of selection
pressures, including UV-radiation, frost, drought, microorganisms, mammals, plant
competition, as well as to herbivorous insects (Marquis 1992). Such a trait may, or
may not, negatively influence the insect herbivore under study. Nevertheless, it is
convenient to classify the character as a resistance trait as long as we know that it
negatively affects some insect(s), or on logical grounds can be supposed to do so. In
order to talk about a mechanism of resistance, however, we have to require that the
insect responds negatively when exposed to the resistance trait (Fig. 1).
4 S. LARSSON
The negative effect on the insect can be of two kinds. It can either result in an
avoidance behavior, oviposition or feeding, whereby the insect is deterred by the
plant trait (antixenosis). Alternatively, the resistance trait can interfere with the
physiology of the insect, once it has accepted to feed on the plant, leading to reduced
growth, fecundity, or survival (antibiosis).
"Non-host resistance" is a term used in plant pathology to describe the inability
of a pathogen to infect a plant “due to lack of something in the plant that the
pathogen needs or to the presence of substances incompatible with the pathogen”
(Agrios 1997; also cf. Heath 2000). It is interesting to note that this term is seldom
used in the insect literature although the avoidance behavior shown by an insect to a
plant that is not part of its host range is highly analogous to non-host resistance
against microorganisms. One important difference between microorganisms and
insects is that the latter have behaviors. Because insect behaviors related to feeding
and oviposition often are context dependent, it may be difficult to describe what is
non-host resistance to a particular insect species. A rich literature exists on the
plasticity of insect behavior when it comes to host acceptance. For example, age,
egg load, plant abundance, and previous experience are factors known to modify
acceptance of a plant for feeding and oviposition (Finch and Collier 2000; Papaj
2000; Hopkins and van Loon 2001).
It should be emphasized that the definitions used here do not necessarily imply
that a resistant plant will be damaged less than a more susceptible plant (although
that would most often be the case). For example, sub-lethal effects of a particular
resistance trait on insect growth can lead to compensatory feeding whereby more
plant tissue is consumed on a resistant plant than on a less resistant one (e.g.,
Winterer and Bergelson 2001).
The concept of defense has been suggested to account for plant characters that
in fact protect the plant (Karban & Baldwin 1997). This view is followed here, but
others have different perspectives on the concept of defense. In particular, it has
been proposed that the term defense implies something about evolutionary history,
i.e. that the trait in question has evolved because of selection from herbivores
(Rausher 1992).
Traditionally, resistance has been considered as genetically determined, probably
because of the strong influence from plant breeders in agriculture (e.g., Painter
1958). Ecologists have increasingly used resistance more broadly. Especially when
it comes to tree/insect interactions the term resistance is frequently referred to as a
phenotypic feature possibly shaped by biotic as well as abiotic factors (e.g.,
Christiansen et al. 1987; Hanks et al. 1991; Wagner and Zhang 1993).
3. RESISTANCE TRAITS
Plant characteristics known to influence insect preference and performance include
(1) primary metabolites, (2) secondary metabolites, (3) physical factors, and (4)
phenology. Current research increasingly emphasizes interactions among these
features (Schopf 1986; Duffey and Stout, 1996; Tomlin and Borden 1997; Kause et
al., 1999a; Nelson and Kursar 1999).
3.1 PRIMARY METABOLITES

Nitrogen is by far the most important nutrient for insect growth and survival
(Mattson 1980, Mattson and Scriber 1987). Many insects have evolved life history
traits to maximize nitrogen uptake from plant tissue low in nitrogen, in comparison
to their needs (Slansky 1993). It is worth pointing out that plant-feeding insects most
likely are sensitive to the composition of nitrogenous compounds, and thus total
nitrogen can be misleading when judging the suitability of a particular plant (Felton
1996; Sandström and Moran 1999).
Carbohydrates have largely been ignored in plant/insect studies probably based
on the assumption that energy does not limit growth of herbivorous insects. A
number of recent studies indicate, however, that single carbohydrate compounds are
essential ingredients in the food of arboreal caterpillars (Jensen 1988; Clancy et al.
1993; Suomela et al. 1995).
There is much variation in concentrations of primary metabolites within species
growing in different habitats, within species of different age, as well as among tissue
types within plant individuals (Clancy et al. 1995). Because there is so much
variation that is seemingly of ontogenetic and physiological origin primary
metabolites are rarely considered to be part of plant resistance, although this may be
erroneous (Berenbaum 1995).
3.2. SECONDARY METABOLITES

A multitude of studies have documented genetic variation in secondary metabolites,
such as terpenoids, phenolics, and alkaloids and the negative effects that these
compounds have on insect performance (Rosenthal and Berenbaum 1992). In
contrast to primary metabolites, there is a tremendous interspecific variation in the
composition and concentration of secondary metabolites (Harborne 1993). In
addition, there is also a considerable variation among genotypes within a species
(e.g., Orians et al 1996; Osier et al. 2000), among plant individuals of different age
(Fritz et al. 2001), among branches within the canopy (Carisey and Bauce 1997),
and among leaf ages within individual branches (Ikeda et al. 1977; Wait et al. 1998).
Many secondary metabolites are highly toxic to insects. In order to exploit plant
tissue containing secondary metabolites insects have evolved behavioral adaptations
to avoid the chemicals (Dussourd 1993), or efficient detoxification systems
(Brattsten 1992). Presumably, biochemical adaptations are costly (Berenbaum and
Zangerl 1992b) and have been considered to be the prime reason for the widespread
specificity in plant use among herbivorous insects. For example, 16 out of 72
needle-eating insect species on Scots pine Pinus sylvestris in Sweden feed only on
the genus Pinus (Björkman and Larsson 1991). However, other phenomena, e.g.,
escape from natural enemies, also are likely to contribute to the high degree of host
plant specialization in herbivorous insects (Bernays and Graham 1988; Stamp 2001).
6 S. LARSSON
Secondary metabolites can be constitutive, i.e. always present in the plant, or

induced by insect feeding (Karban and Baldwin 1997). Constitutive compounds are
often used as cues by insects when selecting host plant for feeding or oviposition
(Byers 1995, Roininen et al. 1999). Thus, for adapted insects, i.e. those that have
evolved the biochemical machinery that allows them to feed on otherwise toxic
plants, secondary metabolites generally do not act as resistance traits. On the
contrary, the secondary metabolites are essential for guiding the insect to the right
plant. It should be remembered, however, that constitutive secondary metabolites
protect the plant from the majority of non-adapted insects, obviously by means of
deterring them from encounters (Bernays and Chapman 1976). Even specialist
insects can be influenced negatively by high concentrations of secondary
compounds in their natural food plant (Larsson et al. 1986; Zangerl and Berenbaum
1993).
Increased concentrations of secondary metabolites observed as a result of
induction by an attacking insect have received much attention in recent years. Many
types of chemicals are found in higher concentrations following induction, including
phenolic compounds in mountain birch induced by the autumnal moth (Kaitaniemi
et al. 1998), tannins in oak after feeding damage by the gypsy moth (Rossiter et al.
1988), and terpenoids and phenolics after attack by bark beetles (Raffa 1991).
A great number of hypotheses have been developed to explain the distribution of
secondary metabolites among plant species and within plant individuals. In general,
two types of hypotheses prevail. On one hand are models that take an evolutionary
approach and aim to understand patterns of secondary metabolites among plant
species with different life histories and growing in different habitats, emphasizing
aspects such as optimality (McKey 1979), plant apparency (Feeny 1976), and
resource availability (Coley et al. 1985). Another set of models focuses on variation
in ecological time with predominantly ecophysiological explanations, pointing at
hierarchies in allocation of resources (Waring and Pitman 1985), the balance
between carbon and nutrient availability (Bryant et al. 1983), balance between
growth and differentiation (Loomis 1932, Lorio 1986), and sink/source regulation
(Honkanen and Haukioja 1998). Recently, attempts have been made to integrate the
evolutionary and ecological/physiological perspective (Herms and Mattson 1992;
Koricheva et al. 1998a; Jones and Hartley 1999). When testing these hypotheses,
and when suggesting improvements (Hamilton et al. 2001), it is important to take
into account the different time scales on which they operate (Coley and Barone
1996) and whether the focus is on constitutive or induced resistance (Lombardero et
al. 2000). It is also important to keep in mind that although all the models were
initially developed within a plant/herbivore framework, most of them make
predictions about plant traits, in particular traits assumed to have a defensive
function. Thus, most models cannot be tested by simply performing bioassays with
randomly chosen species of insects, a common practice in the past, because of
general problems related to seemingly idiosyncratic insect responses (e.g., Lindroth
et al. 1993; Hemming and Lindroth 1995; Ikonen et al. 2001).
3.3. PHYSICAL FACTORS

The toughness of plant structures is a serious hurdle for many herbivorous insects.
Toughness of leaves on woody plants varies among taxa (Coley 1983), within taxa
among habitats (Shure and Wilson 1993), and among age classes within a species
(Larsson and Ohmart 1988). Most likely, tough leaves hinder many non-adapted
insects from initiating feeding, although this source of resistance is difficult to
separate from chemical traits. Even adapted insects find it difficult to feed on the
tough leaves of certain plants. For example, neonate larvae of the leaf beetle
Paropsis atomaria can only establish feeding on the very tender young leaves of its
host Eucalyptus blakelyi; larvae will suffer very high mortality if these leaves for
some reason are not available, e.g., because of extended drought or defoliation by
another herbivore (Larsson and Ohmart 1988).
In many plants the surface of buds, leaves and young shoots is covered by hairs
that can be morphologically and functionally very diverse (Werker 2000). It is
generally assumed that hairs can act as a resistance trait against insects (Levin
1973). For example, experimental removal of the hairs from young willow leaves
make them more accessible for leaf beetle larvae (Rowell-Rahier and Pasteels 1982).
Leaves on certain plant species have trichomes with glands containing secondary
metabolites (Duffey 1986), thus a combination of a chemical and a physical trait.
Such glandular trichomes affect insect feeding and movement through the action of
the glandular exudate that may trap or deter the insect. Many examples of plants
with glandular trichomes providing resistance against insects exist in the agricultural
literature. Hairs are present on many woody plants, especially in young tissue (e.g.,
Denno et al. 1990), but their ecological importance has not been extensively
investigated (Zvereva et al. 1998).
3.4. PHENOLOGY
Many insects are specialized not only to a particular plant taxon but also to a
particular tissue type. This represents a considerable risk for the insect if the tissue is
available for only a short period in time, which is the case, for example, with the
budbreak of perennial plants in temperate regions. There is variation in timing of
budbreak at several spatial levels, i.e., among plant populations (Lawrence et al.
1997), among individuals within a population (Hunter 1992, Quiring 1994), among
branches within plant individuals (Carroll and Quiring 1994) and among buds within
a branch (Quiring 1993). Such variation may have consequences for the growth and
survival of associated herbivores, and the strength of the effect depends on insect
life history traits, e.g., degree of tissue specialization, dispersal capacity, and life
span. In particular, insects with short life spans and an extreme dependence on a
particular growth phase are vulnerable to such variation, e.g., galling cecidomyiids
that depend on undifferentiated tissue for successful gall initiation (Yukawa 2000).
In natural systems insect life history is synchronized with seasonal development
of the preferred plant tissue. This means that most insect individuals in most years
successfully can exploit the food resource. However, the resources - plant
8 S. LARSSON
individuals, branches, or buds - that for some reason are out of synchrony with the
main part of the resource population will be resistant. Exploiting asynchrony
between tree and insect pest could possibly be an important part of integrated pest
control (Hulme 1995). However, recent studies on effects on the population ecology
of lepidopterans have found little support for asynchrony playing an important role
(Hunter 1993; Watt and Woiwod 1999; but see Thomson et al. 1984). Insects with a
more intimate association with the host plant, such as galling insects, may be more
vulnerable to asynchrony (Isaev et al. 1988).
Plant phenology, in the sense of, for example, seasonal development of leaf
morphology or shoot length, is almost always accompanied by changes in chemistry.
Development and chemistry in growing oak leaves is a classic example; protein
concentrations decrease and tannin concentrations increase as leaves mature and get
tougher (Feeny 1970). Recent work by Salminen et al. (2001) demonstrates intricate
within-season dynamics in the composition and concentrations of tannins in birch
leaves, with consequenses for insect growth (Ossipov et al. 2001). Thus, in cases
where chemistry has been thoroughly investigated great changes in concentrations
with aging of the plant tissues have always been detected. Therefore, what is
generally labeled a "phenological" trait is probably most often of a chemical or
physical nature. The extremely dynamic conditions in growing tissue can also be a
serious methodological problem. Koricheva (1999) pointed out that many ecological
studies of secondary metabolites do not make appropriate distinctions between
concentration and content, a problem that is especially frequent when studying
rapidly growing tissue.
3.5. THE IMPORTANCE OF TRADE-OFFS IN DETERMINING LEVEL OF

RESISTANCE
It is central to theories about plant resistance that there is a cost associated with the
construction and maintenance of traits conferring resistance (McKey 1979; Simms
1992). If there is a cost, then there is the potential for trade-offs, meaning “a
negative association between two traits seen in the phenotypic expression” (Mole
1994). One trade-off that has been widely discussed is that between growth and
defense (Fagerström et al. 1987; Herms and Mattson 1992). Surprisingly often the
expected negative relationships between these two functions have been difficult to
document (Simms and Rausher 1989; Rousi et al. 1993; but cf. Bergelson and
Purrington 1996). Recently, Koricheva (2002) concluded from a meta-analysis that
the magnitude of the trade-off varies depending on whether it is measured at the
level of phenotype or genotype; the average magnitude of among-genotype
correlations was higher than that of among-phenotype correlations. It is also
important to remember that there are different kinds of costs. Most often trade-offs
refer to allocation costs, i.e., cost of production, transport, storage, and maintenance.
Two other costs may also be important to consider. Opportunity costs occur when
the plant loses in competition because it invests in resistance early in ontogeny
(Coley et al. 1985). Ecological costs can come about if a trait that confers resistance
to one insect species results in increased susceptibility to another, or negatively
influences natural enemies (van Dam and Hare 1998) or pollinators (Strauss et al.
1999).
A much less studied but potentially important trade-off is the one between
different kinds of resistance traits. Again, if there is a cost, then one would expect
trade-offs between different resistance traits. For example, leaf toughness and
trichome density is negatively correlated in Rubus bogotensis (Björkman and
Andersson 1990). The fact that different resistant traits respond differently to
environmental factors (e.g., Björkman et al. 1998) can also be the result of trade-offs
and competition for common resources (Haukioja et al. 1998).
Obviously, we need to know more about trade-offs between growth and
resistance, and among different resistant traits, if we are to understand the evolution
of resistance and to develop insect-resistant plant genotypes. It is generally accepted
that resistance has had to be compromised with other desirable traits in high-
yielding agricultural crops (Rosenthal and Dirzo 1997). Fewer efforts have been
made concerning resistance breeding in forestry (Hanover 1966), and thus we know
less about the importance of trade-offs in woody plants. But because the underlying
resource base for trade-offs is larger, it is possible that the magnitude of the effect is
smaller in trees than in cereal crops (cf. Mole 1994).
4. INSECT RESPONSES
As defined here, resistance mechanisms constitute the action of a plant trait on the
insect under study. I consider this perspective to be essential because whether or not
a particular plant characteristic is manifested as a resistance trait depends on the
response of the insect. Many insects adapted to feed on a plant species with, for
example, high concentrations of secondary metabolites will suffer small or no
negative effects on individual performance (e.g., Larsson et al. 1992); by definition
(Karban & Baldwin 1997), such a plant has low or no resistance to that insect.
What we call adapted insects have evolved life history traits that allow them to
cope with resistance traits such as low tissue nitrogen concentration, high
concentrations of secondary metabolites, adverse physical features such as tough
leaves, or short temporal windows in suitability. It is generally believed that
specialized insects are better equipped to handle potent resistance traits, although
there does not seem to be a straightforward correlation (Jaenike 1990). Most natural
plant populations exhibit polymorphism with respect to resistance traits so that
resistance is overexpressed in certain plant individuals (e.g., Osier et al. 2000). On
such plants even highly specialized insects can suffer reduction in growth and
survival (Fig. 2).
10 S. LARSSON
Much progress has been made in recent years with respect to understanding the
responses of insect individuals to variable plant resistance traits (e.g., Brewer et al.
1985; Ayres et al. 1997; Hwang & Lindroth 1997, Ossipov et al. 2001).
Unfortunately, for most plant/insect interactions we still only have qualitative
information, i.e., statistically significant effects have been documented for one or at
the most a few doses of the resistance trait. Although such information is essential in
order to develop hypotheses covering qualitative relationships, it is of limited value
when extrapolating to interactions at the population level; more accurate dose-
response functions will be necessary for successful development of such models (see
below).
The efficiency of a particular resistance trait can be influenced by other plant
traits. For example, the alkaloid negatively influences the performance
of Heliothis-larvae when incorporated into artificial larval diet (Campbell and Duffy
1979). However, in actual plant tissue the effect is ameliorated by rutin, another
secondary metabolite naturally occurring in tomato leaves (Duffy et al. 1986). Thus,
to what extent a resistance trait will affect the insect may depend on interactions
with other traits. Little is known about this type of complicated interactions, but it is
probable that they are common and important (Stamp and Yang 1996; Simpson and
Raubenheimer 2001). It is commonly believed that resistance is maintained through
mixtures of secondary compounds (Cates 1996), and it is possible that certain
compounds are more important than can be judged from mere measuring their
concentration if there is a synergistic interaction with a co-occurring toxicant
(Berenbaum 1985). To complicate the matter further, under field conditions
resistance mechanisms are often modified by environmental factors, abiotic as well
as biotic (see below).
The response to a particular resistance trait is not universal among insect
individuals within a species (e.g., Hanks and Denno 1994; Glynn and Larsson
2000). The fact that such variation exists should come as no surprise because
intraspecific variation in preference or performance is the basis for the evolution of
food plant specialization among insect taxa. However, the magnitude with which
insect individuals in natural systems vary with respect to their ability to overcome
resistance traits is largely unknown. Several examples of local adaptations are
documented for herbivorous insects (van Zandt and Mopper 1998), but little
straightforward evidence exists linking this to plant resistance traits. There are many
examples of so called biotypes that are able to overcome resistance in agricultural
system (Via 1990). Thus, when studying plant resistance mechanisms it is essential
to control for variation among the insect individuals used, especially in studies on
insect species with an endophagous feeding mode because these seem to commonly
show local adaptations (van Zandt and Mopper 1998).
There can be many reasons why all insect species do not respond to variation in
a resistance trait in the same way, as discussed above. Regardless of what causes this
variation, the diverse responses make it difficult to make statements about the
degree of plant resistance based on single observations of insect responses. A
somewhat pessimistic view argues that we are dealing with a myriad of
12 S. LARSSON
idiosyncracies and that it will be difficult, if possible at all, to formulate universal

theories (Lawton 2000). A more optimistic view would be that the diversity in
interactions can be explained once we better understand how resistance traits vary
among plants with different life histories (Coley 1988; Loehle 1988), and to what
extent insect life history determines the response to such variation (Mattson et al.
1988; Kause et al. 1999b). For the present, however, we need to be cautious when
using insect bioassays to test phytocentric hypotheses such as the carbon/nutrient
balance (Bryant et al. 1983) or the growth differentiation balance (Herms and
Mattson 1992) hypotheses.
5. INDUCED RESISTANCE
In the previous section I did not distinguish between constitutive and induced
resistance. In many cases, including the issues discussed above, it may not be so
important whether the resistance is of a constitutive or an induced nature. In fact, if
the plant always responds with an induced reaction to insect damage, which seems
to be the case in at least some systems (Edwards et al. 1986), then from an adapted
insect’s point of view the response can be seen as functionally constitutive. The
tremendous focus on induced plant responses in recent years, however, calls for a
special section on insect-induced resistance.
It has long been known that microorganisms induce responses in plants that
render them resistant to attack (e.g., Kuc 1982). At least in crop systems there can be
a very close interaction between the genomes of the two organisms, the resistance
gene in the plant and the virulence gene in the pathogen (e.g., Dangl and Jones
2001). The mechanisms behind plant/pathogen interactions have been identified in
great detail. Elicitors in the form of oligosaccharids or proteins delivered by the
pathogen trigger receptor molecules in the plant (Ebel and Mithöfer 1998). Various
types of biochemical cascades follow in the plant cell upon receptor recognition,
frequently, but not always, resulting in the hypersensitive response, a type of
programmed cell death (Heath 1998). Signal compounds, such as salicylic acid or
jasmonic acid, play important roles in the induction of the cascades (Bostock et al.
2001). Through the action of signal compounds resistance can be systemic, i.e.
tissues away from the site of infection may also become resistant to the invading
pathogen (Mauch-Mani and Metraux 1998).
The study of induced resistance to insects has a much shorter history and has
proceeded along somewhat different lines (Karban and Baldwin 1997). Some of the
insect-oriented research subscribed early on to the resistance paradigm prevailing in
plant pathology (Ryan 1983), but most research on insect-induced resistance took a
different approach with a focus on phenotypic responses in the plant often detected
by using insect individuals as bioassays (Tallamy and Raupp 1991).
It soon became clear that insects induce changes in perennial plants that can last
over long periods of time, and thus could act as a density dependent factor in insect
population dynamics (Benz 1974; Haukioja 1980). Haukioja and Neuvonen (1987)
introduced the terms rapid induced response (RIR) and delayed induced response
(DIR), the former having effects on insects in the same generation and the latter in
future generations. The existence of DIR has been well documented in mountain
birch Betula pubescens ssp. czerepanovii against the geometrid Epirrita autumnata
(Haukioja et al. 1988), although the magnitude of the resistance effect and the plant
traits involved are still not fully understood (Kaitaniemi et al. 1998). Another
documented case of DIR is the European larch and the larch bud moth Zeiraphera
diniana (Baltensweiler and Fischlin 1988 ). There are a number of systems,
however, where extensive damage in one year has not resulted in any increased
resistance to insects in the following year (Niemelä et al. 1991; Šmits and Larsson
1999). It seems as if coniferous trees are less prone to induction by folivorous
insects than deciduous trees, possibly because of differences in carbon allocation
strategies (Tuomi et al. 1988). It should be pointed out, however, that all these
examples have evaluated effects by bioassaying insect larvae. It is possible that
other insect life stages can be affected by induced changes in the plant. For example,
Šmits et al. (2001) estimated that realized fecundity of the geometrid Bupalus
piniarius can be reduced by about 50% when females are forced to lay eggs on Scots
pine trees totally defoliated by larvae in the previous year. Few systems have been
studied with respect to host tree effects on egg production (Leather et al. 1987;
Tammaru and Javois 2000). Clearly, more research on this aspect of induction is
necessary.
The RIR referred to by Haukioja and Neuvonen (1987) is a process that operates
on a time scale of weeks rather than years. Most evidence of RIR come from
bioassays with insects fed damaged and undamaged plant tissue, from phenotypic
measures including accumulation of secondary chemicals, or morphological changes
in the tissue close to the damage (Tallamy and Raupp 1991). Insect feeding almost
always induce at least some changes in the quality of plant traits, but such responses
do not always translate into reduced insect performance, and thereby increased
resistance (Agrawal 2000a). One difficulty when interpreting data on induced
resistance, and indeed variable resistance in general, is how to interpret small but
still statistically significant effects. In a provocative paper Fowler and Lawton
(1985) questioned the relevance of induction effects because they may be marginal
in comparison with other factors influencing insect populations.
The RIR in conifers following attack by bark beetles is especially well studied.
Resistance to bark beetles can be both of a constitutive and of an induced type
(Raffa and Berryman 1983; Raffa 1991). Recent work on Norway spruce (Picea
abies) with simulated bark beetle attack (wounding or inoculation with a
phytopathogenic fungus) has shown induction of traumatic resin duct formation and
polyphenolic parenchyma cells within weeks of infection (Francheschi et al. 2000;
Nagy et al. 2000). Because bark beetle attack was simulated by mechanical
wounding and inoculation with a fungus, it is difficult to know to what extent these
responses represent resistance against the insect (but see Christiansen and Krokene
1999). But on the other hand, bark beetles, and probably many other insects, carry
with them microorganisms that are essential for the insect’s normal development.
Thus, it may turn out that many of the plant responses that we presently interpret as
insect induced in fact are triggered by the microorganisms that are associated with
the insect (cf. Barbosa et al. 1991).
14 S. LARSSON
Rapid induced resistance following bark beetle attack has sometimes been
referred to as a hypersensitive response (HR) (Raffa and Berryman 1987).
Resistance against other insects with an intimate association with their host plant has
also been interpreted as HR (Fernandes 1990; Fernandes and Negreiros 2001). HR
as defined in the pathology literature (Heath 1998) is a rapid process resulting in cell
death, and the mounting of a defense, within hours after the attack. Because most
studies involving insects have been conducted over much longer time scales it is
unclear whether the necrotic tissue assumed to be indicative of HR in fact is just that
or whether it is a consequence of an attack that failed for other reasons (but cf.
Ollerstam et al. 2002).
The breakthroughs in molecular biology techniques we have witnessed in recent
years offer novel methods to study insect induction at the cellular level. Thus, the
time scale in the processes under study is reduced to hours or days rather then weeks
or months as in RIR sensu Haukioja and Neuvonen (1987). Sometimes insect
damage induces the same genes as other biotic agents (Forslund et al. 2000).
However, there are clearly herbivore-specific responses, and these are also different
from mechanical wounding (Korth and Dixon 1997; Havill and Raffa 1999;
Reymond et al. 2000; Halitschke et al. 2001). However, because adapted insects
have evolved ways to cope with induced changes in the plant (Duffey and Stout
1996; Baldwin and Preston 1999) it is not clear to what extent the gene products
affect the performance of the insect. In some cases performance is reduced at a
statistically significant level (Thaler et al. 2001), but in other cases resistance genes
are induced without any measurable effects on the performance of the insect (Stotz
et al. 2000).
The most powerful way of applying molecular methods on plant/insect
interactions is, where it is possible, to use mutants or transformation techniques. By
such methods molecular responses have been studied in detail in Arabidopsis
thaliana (Reymond et al. 2000; Moran & Thompson 2001; Nielsen et al. 2001). Few
similar data exist for woody plants. Most research on transformed woody plants has
focused on introducing resistance genes from other plant species and then studying
effects on bioassay insects (Leple et al. 1995, Confalonieri et al. 1998, Dowd et al.
1998, Delledonne et al. 2001). It will be interesting to see if transgenic trees, e.g.,
Populus sp., can be used to study basic tree/insect interactions in a manner similar
that now ongoing in Arabidopsis research.
6. ENVIRONMENTAL MODIFICATIONS OF RESISTANCE

Plant resistance traits are shaped by environmental factors, biotic as well as abiotic.
The traits can be modified both in ways that make the plant less (induced resistance)
or more (induced susceptibility) suitable to the insect (Karban and Baldwin 1997;
Koricheva et al. 1998b) (Fig. 3). Further, tree genotypes may respond differently to
a particular environmental factor, in which case we talk about a plastic response, or
a genotype by environmental (g x e) interaction. Phenotypic plasticity with respect
to plant resistance to insects is probably common (Smith 1989; Cronin and
Abrahamson 1999), but few data exist on woody plants (Quiring and Butterworth
1994; Orians and Fritz 1995; Björkman 2000).
Certainly the most studied biotic modification of plant resistance is when it is the
product of the attacking insect itself. This was covered in the previous section and
will not be further discussed. But other organisms can also alter plant characteristics
to the extent that the plant becomes more or less resistant to a particular insect
(Agrawal et al. 1999a). Recently, the concept of “cross talking” has been introduced
in the molecular literature to describe a situation where, for example, a fungus or
bacteria elicit plant responses that also lead to induction of resistance to an insect
(Felton et al. 1999; Paul et al. 2000; Bostock et al. 2001). Ecologists have
frequently observed induction of resistance or susceptibility when a tree has been
attacked by other organisms (Danell and Huss-Danell 1985; Faeth 1986; Hatcher et
al. 1994; Wallin and Raffa 2001). It is unclear, however, to what extent such
phenomena can be explained by cross talk (Hunter 2000).
16 S. LARSSON
The fact that insect outbreaks often occur in stands that seemingly are abiotically
stressed has led many to speculate that trees in such stands are less resistant than in
non-stressed stands (Rudnew 1963; White 1974; Bombosch and Lunderstädt 1975;
Rhoades 1979). Many putative resistance traits are modified by environmental
factors (White 1984, Koricheva et al. 1998a), and this has been claimed to be
supportive evidence for the stress hypothesis. The stressed-tree explanation for
outbreaks requires that the insect can take advantage of stress-induced changes in
the tree. This does seem to be the case for certain insect types, i.e. bark beetles and
phloem feeders (Larsson 1989; Koricheva et al. 1998b), but for the most part few
experimental data exist to support the notion that insects are favored by feeding on
stressed plant tissue (Koricheva et al. 1998b). In fact, some insects do respond
negatively to stressed plants (Koricheva et al. 1998b) which has led Price (1991) to
postulate the opposite, namely that insect performance is enhanced on vigorously
growing plants, or plant parts. It may be dangerous, however, to completely reject
the plant stress – insect performance hypothesis because in natural forests stressful
conditions build up gradually in ways that are poorly understood making proper
experimentation difficult (cf. Brown et al. 2001). Also, because stress experiments
only rarely control for tree genotype it is possible that treatment effects have been
difficult to detect if trees show phenotypic plasticity with respect to stress responses.
The underlying observation, i.e., that outbreaks frequently correlate to seemingly
stressful abiotic conditions, cannot be ignored but perhaps explanations based on
tree resistance alone are simplistic (Larsson et al. 1993).
7. RESISTANCE IN THE CONTEXT OF COMPLEX INTERACTIONS

In natural systems, plant resistance is one of many selective agents affecting
herbivore fitness. It is particularly important to recognize that effects of plant
resistance traits on insect growth and survival can be much modified by natural
enemies, i.e., tri-trophic level effects (Price et al. 1980; Agrawal 2000b).
Many plant traits, seemingly with a defensive function, do not cause mortality in
feeding insects, although insect growth rate may be reduced. When studied in the
laboratory such sub-lethal effects can in fact lead to more damage to the plant
because the insect compensates by consuming more leaf tissue (e.g., Docherty et al.
1996). Possibly, this “paradox of sub-lethal plant defense” (Moran and Hamilton
1980) can be resolved by taking into account higher trophic levels; insects feeding
on resistant plants, resulting in longer development time, are more exposed to
natural enemies, and thus, may suffer higher predation mortality compared to
conspecifics feeding on susceptible plants (Häggström and Larsson 1995; also cf.
Agrawal et al. 1999b). Because natural enemies are significant mortality agents in
most insect herbivore populations (Cornell and Hawkins 1995), it is necessary to
consider this interaction whenever sub-lethal effects are present (Kondoh and
Williams 2001). Unfortunately, it is difficult to analyze because natural enemy
population density varies spatially and temporally in ways that are most often
unknown, and thus the extent to which "slow growth-high mortality" is a significant
modifier of insect-caused plant damage in a particular environment will be difficult

to predict (cf. Gratton and Welter 1999).
In certain interactions the insect has not only evolved mechanisms to cope with
plant secondary metabolites but has taken advantage of their toxic properties for use
in defense against its enemies (Rowell-Rahier and Pasteels 1992). This type of
defense probably offers a considerable fitness gain, and thus could have been an
important factor in the evolution of host plant specialization in herbivorous insects
(Bernays and Graham 1988). For example, larvae of the leaf beetle Phratora
vitellinae suffer higher mortality from generalist predators when forced to feed on
willow leaves lacking salicin, the precursor of its anti-predator defense, than larvae
fed leaves of its normal host that contain salicin (Denno et al. 1990). Many
interactions of this kind have been described (Rowell-Rahier and Pasteels 1992).
Thus, when the plant interacts with these highly specialized insects the secondary
metabolite cannot, by definition, be considered a resistance trait because insect
fitness is enhanced rather than reduced. When considering a plant trait such as
salicin it is important, therefore, to be explicit in the formulation of the research
question. A plant-oriented hypothesis, for example whether or not there is a cost
associated with producing salicin, needs to be specified according to expected
benefits. In the case of P. vitellinae there are seemingly small, if any, benefits for the
plant to contain salicin. However, less specialized insects do suffer reduced
performance by ingesting leaf tissue that contains salicin (Hodkinson et al. 1998).
A very special kind of induced resistance is when the plant "calls for help" from
natural enemies, i.e. the damage caused by the herbivore results in the release of
novel volatile compounds that attract natural enemies (Dicke 1999; Farmer 2001).
This "indirect defense" (Baldwin and Preston 1999) involving the third trophic level
has been intensively studied in recent years. Most well-studied examples include
attraction of parasitic wasps to plant tissue damaged by caterpillar feeding (Turlings
et al. 1995). It is not clear to what extent the plant really benefits from this
interaction because most parasitized larvae continue to feed at least as much and
sometimes more than non-parasitized larvae (van der Meijden and Klinkhamer
2000). If predators also were attracted, then induction clearly would be adaptive
because increased predation mortality would lead to reduced damage to the plant. A
recent study has indeed found generalist predators to respond to volatiles induced in
Nicotiana attenuata leaves following damage by three species of leaf-feeding
herbivores (Kessler and Baldwin 2001). Still, it is possible that volatile induction is
simply a by-product of feeding when caterpillar saliva is mixed with the plant cell
content. An interesting alternative, albeit not mutually exclusive, explanation is that
the volatiles are produced primarily for the benefit of the herbivore, for example, by
acting as deterrents for egg-laying females and thereby reducing competition among
conspecific larvae (De Moraes et al. 2001; Kessler and Baldwin 2001). Most
detailed studies on herbivore-induced volatile emission are from herbs or grasses
(Dicke 1999; Dicke and Bruin 2001). Volatiles were implicated as a possible
underlying mechanism in the "talking trees" studied during the 80's (Baldwin and
Schultz 1982; Rhoades 1983); however, interpretations of these experiments are
problematic. Havill and Raffa (2000) recently found increased parasitoid attraction
18 S. LARSSON
to volatiles from poplar leaves damaged by gypsy moth larvae, compared to non-
damaged leaves (also cf. Dolch and Tscharntke 2000; Tscharntke et al. 2001). Thus,
it seems reasonable that future studies on trees, based on the same protocols as used
with herbs and grasses, will document volatile induction also in woody plants.
8. RESISTANCE AND INSECT POPULATION DYNAMICS

Time scale is an essential component for assessments of the "importance" of plant
resistance to insects. When testing hypotheses on an evolutionary time scale, it may
be appropriate to ask, for example, whether or not differences in resistance among
plant genotypes lead to statistically significant variation in insect fitness. If so, then
there is potential for plant traits to influence the evolution of insect life history traits.
However, when examining processes on an ecological time scale, the magnitude of
the effect, not only statistical significance, needs to be taken into account (Fowler
and Lawton 1985; Kytö et al. 1996). For example, whether or not variation in a
particular resistance trait can account for ups or downs in insect numbers needs to be
examined in the context of other factors influencing the performance of the insect, in
particular, density dependent factors that may overshadow any effects that plant
traits have on the performance of insect individuals (Hunter 1997).
Few systems have been examined in enough detail to allow such analyses. The
natural variation in the expression of the resistance trait, responses of insect
individuals to the full range of plant resistance variation, the magnitude of other
factors acting on insect individuals, and the behavior of density dependent factors
are most often not all known for any single system. For the European pine sawfly
Neodiprion sertifer reasonably good data exist on larval responses to variable needle
terpenoid (resin acid) concentrations (Larsson et al. 1993), and there is good reason
to assume that cocoon predation by small mammals is the most important density
dependent mortality factor (Hanski 1990). Larval survival and sawfly fecundity are
reduced at high resin acid concentrations (Larsson et al. 1986). However, high resin
acid concentrations are, at the same time, beneficial because larval defense against
predators is enhanced (Björkman and Larsson 1991); thus, the pine/sawfly system is
a case where tri-trophic interactions are potentially important. These observations
formed the basis for the development of a simple population model to evaluate the
importance of variable needle resin acid concentrations for the onset of sawfly
outbreaks (Larsson et al. 2000). In the model, data on individual responses were
combined with literature data about cocoon predation at the population level. The
analysis showed that the probability of plant-mediated escape from natural-enemy
control, i.e., risk for an outbreak, is high when needle resin acid concentration (r) or
larval predation pressure (p) is low, and by analyzing different scenarios it was
found that small changes in r and p can result in the sawfly population moving from
low to high outbreak risk (Fig. 4).
In the sawfly model, one resistance trait, concentration of needle resin acids, was
examined. In a natural situation, plant traits interact and the sum of their effect on
performance of insect individuals is complex (Duffey and Stout 1996).
Nevertheless, formal analyses including processes both at the levels of the
individual and the population are urgently needed before anything can be said about
the "importance" of plant resistance traits for the dynamics of insect populations.
One serious complication is that the temporal and spatial variation in traits of
importance for insect performance is unknown for the great majority of tree species.
Still, in order for plant traits to contribute to insect population dynamics one has to
assume variation in trait quantity, and thus effects on the performance of insect
individuals. With regard to the onset of insect outbreaks abiotic stress has been
implicated as the factor that induces changes in trait quantity, e.g., increased
concentrations of soluble amino acids (White 1974) or decreased concentrations of
secondary metabolites (Rhoades 1979). Unfortunately, data from forest stands
suitable to test this hypothesis are difficult to collect, and experimental data are
inconclusive (Koricheva et al. 1998b). Future research efforts will have to combine
20 S. LARSSON
a multitude of approaches, including long-term monitoring of plant and insect,

manipulative experiments, and modeling in order to successfully address hypotheses
involving the importance of tree resistance at the population level.
ACKNOWLEDGMENTS
I thank Christer Björkman, Erik Christiansen, Barbara Ekbom, Bob Fritz, Julia Koricheva,
and Tim Paine for helpful comments on earlier drafts of this chapter. Financial support was
provided by the Swedish Council of Forestry and Agricultural Research (SJFR), and the
Royal Swedish Academy of Agriculture and Forestry (KSLA).
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CHAPTER 2
MECHANISMS OF RESISTANCE IN CONIFERS

AND BARK BEETLE ATTACK STRATEGIES
FRANÇOIS LIEUTIER
Université d’Orléans, Laboratoire de Biologie des Ligneux et des Grandes Cultures B.P.
6759, F.-45067 Orléans Cedex, France. and :
INRA, Unité de Zoologie Forestière BP 20619 Ardon, F-45166 Olivet Cedex, France.
1. INTRODUCTION
Bark beetles are the most damaging pests of coniferous forests worldwide. It is well
established that the key-factor in their population dynamics is food quantity, or the
number of host trees in a condition that makes them susceptible to successful
colonization. The role of the host is central in all aspects of the bark beetle life
cycle. As with any other living organism, trees are able to defend themselves
against attacks and, during the colonization process the beetles must overcome
various resistance mechanisms. Host resistance is absent in freshly felled trees that
are always successfully colonized and thus represent an easily accessible source of
food. It can reach very high levels in healthy and vigorously growing trees that are
unsuitable for beetle establishment and thus are an inaccessible source of food. The
quantity of food available for the beetle population directly depends on the
efficiency of the tree’s resistance mechanisms, which are thus the real key-factor of
bark beetle population dynamics for species that attack living trees.
Consequently, it is not surprising that the study of the relationships between bark
beetles, their associated phytopathogenic fungi and their host tree, especially its
resistance, has led to dramatic improvements in knowledge about bark beetle
biology and population dynamics. Here, I present an overview of the state of the art
in this field, emphasizing advances in knowledge during the last 5 years. I will
consider only the mechanisms themselves, not their variations with genetic and/or
environmental factors. First, the different defense systems involved in resistance of
conifers to bark beetles will be covered. Next, I will describe how trees resist
attacks, the mechanisms involved, and the respective roles of the defense systems.
31
32 F. LIEUTIER
Then, I will consider how beetles overcome the resistance of the trees including the
mechanisms of attack and establishment and the different colonization strategies that
beetles use. Conclusions will focus on research prospects and potential application
of resistance to bark beetles.
2. LEVELS OF TREE RESISTANCE

According to Karban and Baldwin (1997), resistance must be distinguished from
defense. Resistance is considered from the beetle’s perspective and refers to the
difficulty of establishing in the host, whereas defense refers to the host facing the
beetles. These may or may not be the same thing. Moreover, defense often
supposes an active mechanism (particularly in response to aggression), while
resistance can also include passive non-induced phenomena.
There are 2 main types of resistance in plants facing attack by living organisms.
Preformed resistance mechanisms exist in the absence of attack by the beetles.
There is no gene activation and transcription control resulting in increased synthesis
following damage. The plant has invested resources in defense before damage
occurred (preformed defenses). Induced resistance mechanisms are “turned on”
only when beetles attack the tree. Genes are activated by the damage, resulting in
increased synthesis of specific compounds. The plant invests resources in defense
after damage has begun (induced defenses). I summarize the main types of defenses
(preformed and induced) occurring in conifers subjected to bark beetle attacks and
their potential role in host resistance in the sections that follow. For convenience,
these mechanisms are presented separately but they are not independent constituents
of tree resistance. They develop simultaneously and complement each other, even if
their effects on the beetles do not occur at the same time.
2.1 PREFORMED DEFENSES

The cells responsible for the syntheses of the defensive chemicals involved in
preformed defenses are secretory structures already specialized in that function.
There is no change in the metabolism of the secretory cells, which are generally
localized, in well-defined tissues. These structures are present in any tree organ and
are responsible for the first line of resistance met by the invaders (beetles and
eventually fungi). There are, however, two possibilities in preformed resistance
(Karban and Balwin, 1997). When the defensive structures are active in the same
state as they were before aggression, they correspond to the “constitutive resistance”
or “constitutive defense”. When they need to be activated to play a role in
resistance, either because a wound is necessary to release an active compound or
because an inactive precursory compound becomes active after being released by a
wound, they correspond to the “activated defense” or “preformed induced defense”.
2.1.1. Constitutive defense

Bark thickness can be an efficient constitutive defense against bark beetle species
that usually attack the upper parts of the trees, such as Pityogenes chalcographus on
BARK BEETLES ATTACK AND TREE DEFENSES 33
spruce and Ips acuminatus on pine in Europe. Lignin located in the outer bark and
the phloem of various conifer species is often concentrated in numerous patches
disseminated in the tree tissues (Figure 1). These structures, sometimes called
“stone cell masses”, are inevitably met by the beetles when boring their galleries,
and their hardness can dissuade the beetles from continuing the attack if they are
abundant, as in the case of Dendroctonus micans in Norway spruce (Wainhouse et
al., 1990, 1998).
Nevertheless, although absolutely passive, this constitutive defense may influence

the development of induced mechanisms. In Norway and Sitka spruces, a negative
correlation was found between the size of the lesions induced by artificial
inoculations of fungi and the concentration of the lignified stone cell masses in the
phloem (Wainhouse et al., 1997). This interaction between such distinct defense
systems illustrates the complementarity and interdependence of the mechanisms
involved in the various kinds of defense.
2.1.2. Preformed induced defense

Two main anatomical systems in conifers are sites for storage of secondary
metabolites that are released or become active after wounding by aggressors.
Blisters and resin ducts store monoterpenes and resin acids (Johnson and Croteau,
1987), while specialized phloem parenchyma cells store soluble phenols as well as
more complex polyphenolic compounds (Franceschi et al., 1998).
Resin ducts form an elaborated resin system in the genera Pinus, Picea, Larix
and Pseudotsuga, which do not possess blisters (Bannan, 1936). Vertical and radial
ducts are connected to each other and resin is synthesized by secretory cells lining
these ducts (Bannan, 1936; Shrimpton, 1978) (Figure 2). Vertical ducts are the most
abundant and are located in the sapwood only, while radial ducts occur in both the
sapwood and the phloem. There is contiguity between the sapwood radial ducts and
those of the phloem but usually no communication exists between them (Shrimpton,
1978). However, communications exist between the vertical and radial ducts of the
sapwood. Consequently, the main location of the resin duct system is sapwood and
the amount of resin flow exuded by a wound has been correlated with the density of
34 F. LIEUTIER
vertical resin ducts (Blanche et al., 1992) which represent the most important
reservoir of preformed
resin in conifer species that have resin ducts. The beetles cut resin ducts in the
phloem and superficial sapwood when they bore their galleries. When galleries do
not sever the sapwood, trees respond to the wound by creating continuity between
the sapwood and phloem radial ducts (Gambliel et al., 1985), thus allowing the
mobilization of the sapwood reservoir. The resin flow released by slashing of the
duct system is thus typically a preformed induced defense. Indeed, resin is
synthesized before aggressions but requires damage to tissues and building of a
communication between phloem and sapwood to be released and to get in contact
with the aggressors. This resin flow involves the rapid transport of chemicals to the
site of damage. In fact, although no induced synthesis is involved in it, the
preformed resin flow is often mixed with the induced resin flow and the resin
exuding from the saturated tissues involved in the hypersensitive response (see
below).
The direction of gallery boring is important for this kind of defense system to
play a significant role in tree resistance (Berryman, 1972; Lieutier, 1992). Because
of the organization of the resin duct system, vertical galleries are sectioning both
vertical and radial ducts at the beginning of the beetle tunnelling activity, but only
radial ducts later on. Since the vertical ducts are the most abundant, the effect of
resin flow in that case is mostly limited to the moment of gallery initiation. On the
other hand, horizontal galleries cut both vertical and radial ducts during the whole
tunnelling activity, which gives the resin flow a greater chance to play a role, as
demonstrated for D. micans in Picea abies (Lieutier et al., 1992). Moreover, the
chance for this defense system to counteract beetle attacks is especially high in tree
species (mostly pines) where the resin network is particularly developed and for
those that are able to rapidly exude large quantities of resin. Among pines, however,
geographic or between species differences exist. The preformed resin flow is
presumed to be the main defense system against D. frontalis in several pine species
in the southern United States. Interspecific variation in its characteristics would also
explain why different tree species in this area diverge in their susceptibility to attack
(Hodges et al., 1979; Matson and Hain, 1985; Nebeker et al., 1988, 1993). It has a
much more limited impact against D. ponderosae in lodgepole pine (Pinus contorta)
in the north-western US (Raffa and Berryman, 1982a) and against Ips and Tomicus
species in Scots pine (Pinus sylvestris) in Europe (Lieutier et al., 1988, 1995;
Schroeder, 1990). Spruces have a limited resin flow as observed in Norway spruce
(Picea abies) during I. typographies attacks (Christiansen and Horntvedt, 1983;
Christiansen, 1985a).
Blisters are cavities mainly located in the outer bark of Abies, Tsuga and Cedrus,
which do not possess resin ducts (Bannan, 1936). In these species, large quantities
of resin exude when blisters are damaged and could play a role in arresting the
aggressors. However, beetles apparently avoid these resin pockets while attacking a
tree, as demonstrated for Scolytus ventralis in Abies concolor (Ferrell, 1983).
The role of resin flow is wound cleansing by flushing the wounded tissues and
then sealing the wound through resin crystallization (Berryman, 1972; Nebeker et
al., 1995). It can also have a physical effect on the aggressors through flushing,
viscosity and crystallization rate; oleoresin exudation pressure has been reported to
be correlated with tree resistance (Vite 1961; Cates and Alexander, 1982). In
addition, a chemical effect obviously exists since terpenes from preformed resin can
be repellent or toxic for the beetles and their associated micro-organisms (Reid and
Gates, 1970; Raffa et al., 1985; Paine and Hanlon, 1994; Raffa and Smalley, 1995).
However, fungi can often tolerate the preformed resin flow (Cobb et al., 1968;
Shrimpton and Whitney, 1968), as do many beetles that are able to swim in it. On
the other hand, this resin flow dries up very rapidly (Nebeker et al., 1992; Raffa and
Berryman, 1983a). Moreover, when the flow is efficient, beetles often can escape.
Then, owing to the high variability of the resin flow within a tree (Schroeder, 1990),
they can succeed in initiating a gallery elsewhere in the same tree, thus
circumventing this defense system (Lieutier et al., 1995). When effective however,
in addition to its physical and direct chemical effects, the constitutive resin flow can
interfere with pheromone emission and thus stop beetle aggregation (Raffa and
Berryman, 1983a).
The polyphenolic parenchyma cells (PP cells) of conifers are located in the
phloem where they represent the second numerically important cell category, after
the sieve cells. They are organized mainly in concentric parallel rows all around the
tree with one row per year (Franceschi et al., 1998; Krekling et al., 2000) (Figure 3).
As the tree is enlarging, additional PP cells can be produced in
36 F. LIEUTIER
the already existing rows, by differentiation of axial parenchyma cells or by division

of already differentiated PP cells, thus forming permanently continuous layers of
cells (Krekling et al., 2000). This particular organization inevitably results in the
destruction of many PP cells and rows when a beetle bores a gallery or when its
associated fungus invades the phloem. Under such wounding conditions, large
quantities of phenolics previously stored in the PP cells can be released (Franceschi
et al., 1998). The assumption that these cells contribute to the tree’s preformed
defense is based on the observation that, in Norway spruce, their density is much
higher in resistant than in susceptible trees and their content also seems to be in a
more soluble form in resistant trees (Franceschi et al., 1998). This is of interest
since it has been demonstrated that resistance in Norway spruce clones is correlated
with the content of their phloem in certain soluble phenols before any aggression
(Brignolas et al., 1998). However, we still have no direct demonstration of the
effectiveness of this preformed defense system, although phenols are known to have
antifungal properties and to be feeding deterrents for phytophagous insects
(Nicholson and Hammerschmidt, 1992; Appel, 1993).
2.2. INDUCED DEFENSES

These defenses are considered as plant responses, and are typically categorized as
short term or long-term inducible responses or mechanisms (Mattson et al., 1988).
Another classification uses the complexity of the changes occurring in the cells
involved in the tree response (Franceschi et al., 2000). Limited changes in the
metabolism of cells already specialized in the same function before aggression
would be at one end of the ranking, while complex changes involving cell division
and differentiation would be at the other end. Presently these two classification
systems overlap closely in regard to tree responses to bark beetles, since limited
changes are associated with short term responses while complex changes occur
under long term responses. The three main steps in these classification systems are
induced resin flow, hypersensitive reaction, and delayed resistance. Each step
corresponds to a particular kind of induced defense.
2.2.1. Induced resin flow

Ruel et al. (1998) recently described this type of induced defense in loblolly pine (P.
taeda) in the southern U.S. Trees were wounded repeatedly over several days, while
measuring the resin flow periodically (Figure 4). After a rapid (24 hours) drying up
of the preformed resin flow, a new resin flow appeared in two days and increased
during the following days, reaching 2 -3 times the values of the preformed flow in
five days. Such a considerable and rapid increase of the resin flow cannot be
explained by a simple refilling of the ducts. At least a large-scale resin translocation
was involved. However, according to the authors, large-scale translocations are
unlikely to occur in pines because resin ducts in these trees do not form a true
network. Moreover, this would require a decrease of resin flow in other parts of the
tree. Thus, although not yet proved, it was concluded that the new resin flow was a
reaction of the tree induced by the wounds and not specifically linked to the
stimulus.
Induced resin flow appears only after preformed resin flow (preformed induced
defense) has stopped. Similarly, the classical hypersensitive reaction also is not
specific and exists after repeated wounding but it is less rapid. Another difference
compared to the hypersensitive reaction is the category of cells responsible for
syntheses of the induced resin. Indeed, the cells involved in induced resin flow are
very likely those that are already responsible for the synthesis of preformed resin,
while those involved in resin synthesis of the hypersensitive reaction differ
completely (see below). Induced resin flow would thus correspond simply to a
stimulation of the metabolism of cells already specialized in the same function,
which would explain the rapidity of the response. However, until a study of the
chemical composition of induced resin flow is carried out, it is impossible to know if
this stimulation is accompanied by modifications of cell metabolism.
Certainly induced resin flow can stop beetle boring and thus extend the role of
the preformed resin flow. It can also play a role in perturbing pheromone emission
and thus stopping beetle aggregation. However, nothing can be concluded regarding
38 F. LIEUTIER
a possible chemical effect since its chemical composition is still unknown. The
resistance mechanism of preformed resin flow is certainly more efficient in pines
than in other conifers. It may be significant that it has been discovered in loblolly
pine.
2.2.2. Hypersensitive reaction

Reid et al. (1967) first described the hypersensitive reaction induced by a bark beetle
attack in conifers and presented the role of the fungi associated with the beetles in
amplifying the reaction mechanisms. They suggested that this so-called
“secondary” reaction (as opposed to “primary” preformed resin flow) plays the most
important role in conifer resistance to bark beetles. Berryman (1972) generalized
these ideas and presented the first synthetic hypothesis of tree resistance and beetle
success taking into account the tree’s hypersensitive reaction. Berryman (1976)
proposed a model of bark beetle population dynamics taking the tree resistance
mechanisms into account. Subsequently, a considerable amount of research has
been developed in this field, and the hypersensitive reaction has been demonstrated
to play a basic role in the resistance of many conifer species to many bark beetles
species and their associated fungi (Safranyik et al., 1975; Raffa and Berryman,
1982a,b; Christiansen et al., 1987; Raffa, 1991; Paine et al., 1997). However,
Nebeker et al. (1993) reported it plays only a minor role against pine bark beetles in
the southern U.S.
This tree reaction develops around each point of aggression, in both the phloem
and the sapwood. It is visible as a longitudinal resin impregnated zone associated
with extended cell necrosis (Reid et al., 1967; Berryman, 1969, 1972; Lieutier and
Berryman, 1988a; among others) (Figure 5). The zone is considerably enriched with
terpene and neosynthesized phenolic compounds and impoverished with sugars
(Shrimpton, 1973 and see section III.2 below). The synthesized compounds invade
intercellular spaces and sieve cells, thus leading to the death of the affected tissues
(Lieutier and Berryman, 1988a). The reaction develops at a distance, ahead of the
area infested by the insects and their associated fungi. In the phloem of Norway
spruce, intercellular communications exist between the PP cells and the ray
parenchyma cells, which are highly interconnected to each other through
plasmodesmata. These connections could be the way the signal for the response is
transmitted at a distance from the aggressor (Krekling et al., 2000). The reaction
acts both physically and chemically against the aggressors in addition to depriving
them of nutrients (see below). In resistant trees, these physical and chemical
changes in tree tissues contribute to stop fungal growth (fungistatic effect) and
prevent gallery construction and oviposition by the beetle (Reid et al., 1967;
Berryman, 1969 and see below).
Chemical, histological, anatomical and cell studies have revealed that the
hypersensitive reaction is a wound reaction induced by the mechanical stress caused
by the tunnelling activity of the beetle, and that it is not induced by the fungi
introduced by the beetle in its gallery (Lieutier et al., 1988, 1995; Franceschi et al.
1998). However, the reaction can be considerably stimulated and amplified when a
fungus is present in the beetle gallery (Lieutier et al. 1988, 1995). Raffa and
Smalley (1995) suggested that both structural and metabolic properties of the fungi
are important because an inoculation with an autoclaved unviable fungus induced a
reaction with an intensity intermediate between that induced by an aseptic wound
and that induced by a living fungus. Because of the role of wounding in the
induction, the direction of the beetle gallery is certainly important for the
development of the reaction. Indeed, due to the anatomical structure of the tree, the
hypersensitive reaction develops naturally mainly in the longitudinal direction.
Consequently, it is strongly stimulated by longitudinal beetle galleries. The
induction by wounding and the amplification by the fungi associated with the
beetles had been mentioned by Reid et al. (1967), Wong and Berryman (1977),
Raffa and Smalley (1995) and others, but without assigning specific roles to the
beetle tunnelling activity and the fungi. Lewinsohn et al. (199la, b) suggested that
pines do not respond to mechanical wounding by increasing synthesis of resin but
rather use translocation in resin ducts, which means that there would be no
hypersensitive reaction after wounding. However, the chemical composition of tree
tissues in the reaction zone of the hypersensitive reaction, differs greatly from that in
the unwounded tissues in both terpenes and phenolic compounds, even after
wounding alone (Russel and Berryman, 1976; Raffa and Berryman, 1982b;
Gambliel et al., 1985; Paine et al., 1987; Delorme and Lieutier, 1990; Lieutier et al.,
1991a; Brignolas et al., 1995a; Bois and Lieutier, 1997). This would not be possible
if only translocation of resin occurred. Moreover, gene activation (Chiron et al.,
2000) and neosyntheses with increased enzyme activities (Brignolas et al., 1995b)
have also been demonstrated to occur after wounding. In addition, the cytological
modifications observed after wounding in the PP cells involved in phenol syntheses,
are the same as those observed after a biotic aggression (Franceschi et al., 1998).
Although the rapidity and the extension of the hypersensitive reaction depend on
the aggressor, the patterns of response development, as well as the associated
qualitative (chemical, anatomical or histological) changes are identical in a tree,
40 F. LIEUTIER
whatever the aggressor (different fungi, different beetles, or wounding). This non-
specific response to various aggressors was observed by Reid et al. (1967) and
Wong and Berryman (1977) through similarities of the tree’s response to wounding
and fungus aggression, but they did not specifically mention it. It has now been
clearly demonstrated at the chemical level through analyses of the monoterpene and
phenol contents of the phloem reaction zones, in various conifer species (Cook and
Hain, 1985; Delorme and Lieutier, 1990; Lieutier et al., 1991b; Raffa and Smalley,
1995; Popp et al., 1995; Brignolas et al., 1995a; Bois and Lieutier, 1997) and at the
histological level (Lieutier and Berryman, 1988a; Franceschi et al., 1998). Changes
in the nature of the aggressor elicit only quantitative variations in the tree’s
hypersensitive response.
Metabolic modifications associated with the hypersensitive reaction are much
more extended than those involved with induced resin flow. Specialized phloem
parenchyma cells, without relation to the cells involved in the synthesis of the
preformed resin, are responsible for induced delocalized syntheses of terpenes
(Cheniclet et al., 1988; Lieutier et al., 1988). The same PP cells involved in the
preformed defense seem to be responsible for the neosyntheses of phenolics
(Franceschi et al., 1998), although heavy changes occur in their metabolism
(Brignolas et al., 1995b; Chiron et al., 2000). However, no changes in cell division
and differentiation seem to be associated with this reaction. Because the
hypersensitive reaction is a wound reaction not specifically linked to the stimulus, it
is logical to hypothesize that the elicitors involved originate from the tree itself and
not from the aggressors (Wong and Berryman, 1977; Berryman, 1988; Lieutier and
Berryman, 1988; Lieutier, 1993). A simple working diagram of these mechanisms
has already been proposed (Figure 6, and Lieutier, 1993), taking into account these
particularities, the relationships between the hypersensitive reaction and the
aggressors, and the possible role of the wound periderm (see below).
The hypersensitive reaction is completed by the formation of a wound periderm

containing an impervious cell layer which develops after the aggressors have been
stopped or at least considerably slowed down (Reid et al., 1967, Müllick, 1977;
Wong and Berryman, 1977; Berryman and Ferrell, 1988; Lieutier et al. 1990, 1993),
while traumatic resin ducts are built up in the sapwood that closely surrounds the
reaction (Safranyik et al., 1988). This is the final step of the reaction, which leads to
the isolation of the reaction zone (dead tissues) from the rest of the tree, in a
compartmentalization process (Shigo, 1984). In fact, according to the criteria of the
classification system presented above, the formation of the wound periderm is a
long-term induced response since it involves changes in cell division and
differentiation (see below).
2.2.3. Delayed resistance

This type of induced defense concerns long term inducible responses with complex
changes involving cell division and differentiation. Two kinds of resistance
mechanisms are associated with bark beetle attacks –
the wound periderm and the induced protection phenomenon.
Development of wound periderm has been studied in detail by Müllick (1977)
with different aggressors such as the balsam woolly adelgid (Adelges piceae
[Ratzeburg]) and various pathogens and wounds. Development of wound periderm
was covered in the previous section in relation to attacks by bark beetles and their
associated fungi. It is mainly involved in the wound healing processes after the
hypersensitive reaction is terminated and is thus not a real defense mechanism.
42 F. LIEUTIER
Nonetheless, wound periderm is worth mentioning because it may contribute to

limiting further extension of fungus. From his histological studies, Müllick (1977)
concluded that it is basically a wound reaction oriented towards tissue restoration,
and not specifically linked to a stimulus.
The phenomenon of induced protection has been recently discovered and

described in P. abies regarding artificial mass inoculations with Ophiostoma
polonica, a pathogenic fungus associated with Ips typographus (Christiansen et al.,
1999a; Krokene et al., 1999). When the boles of Norway spruce trees were pre-
treated with mass inoculations of fungus at below the lethal density, they became
resistant to mass inoculations made three weeks later in the same zone of the tree
with the same fungus but at a deadly dosage (Figure 7). Trees pretreated with malt
agar alone also exhibited increased resistance to further mass inoculations, although
at a lower level than that of trees pretreated with the fungus. This induced
protection has been hypothesized to be related to building of traumatic resin ducts
around the wounds, although they have not been observed in the same experiment
and their role in the increase of resistance not been demonstrated directly (Krokene
et al., 1999). Indeed, in the same tree species, traumatic resin ducts appeared locally
at wound sites at least two weeks after wounding (Christiansen et al., 1999b; Nagy
et al., 2000). This is the same delay at which the induced protection was observed
in the experiment reported above, and it seemed to be more developed in resistant
compared to susceptible clones (Nagy et al., 2000). Traumatic resin ducts have
often been observed in trees surviving beetle attacks or fungal infection (Berryman,
1969; Christiansen and Solheim, 1990; Kyto et al., 1996). They have even been
observed at a distance of several meters one year after wounding (Christiansen et al.,
1999b). Reid et al. (1967) also reported the existence of traumatic resin ducts after
one year at 3-4 feet from the wound in pines. These observations are very similar to
what has been observed in the leader shoot of white spruce (Picea glauca) attacked
by Pissodes strobi (Alfaro, 1995; Alfaro et al., 1996).
Regarding bark beetle population dynamics, the build-up of induced
protection could accelerate the collapse of outbreaks by protecting the trees from
further attacks (Christiansen et al., 1999b). Indeed, the establishment of a network
between the traumatic ducts and the radial ducts would form an important reservoir
of resin, which could be rapidly mobilized in case of attacks that sectioned the radial
ducts. Under these conditions, if the formation of traumatic resin ducts effectively
increases tree resistance, the presence of these ducts at a distance from the wounds
may lead to systemic induction of resistance. However, one year after pretreatment,
mass inoculations at a distance from the pretreatment zone did not reveal any
induced protection, although the protection was still effective in the inoculated zone
(Krokene et al., 2000).
If the hypothesized role of traumatic resin ducts is accepted, the induced
protection phenomenon corresponds effectively to a long term and complex induced
reaction involving cell division and differentiation. Alternatively, the fact that trees
pretreated with malt agar exhibited the same response, but at a lower level, as those
pretreated with the fungus, suggests that the phenomenon is induced by wounding,
is not specifically linked to aggressors, and is amplified by the presence of the
fungus. This non-specificity has also been observed at the histological level
(Franceschi et al., 2000). The same conclusions can be drawn regarding the
formation of the traumatic resin ducts. They have been known for a long time to be
induced by wounds (Bannan, 1936), they correspond to a non-specific response of
the tree, and their formation is stimulated by the presence of the fungus (Tomlin et
al., 1998; Christiansen et al., 1999b; Nagy et al., 2000).
3. MECHANISMS OF INDUCED DEFENSE

3.1. INDUCTION AND TREE RESPONSES
All the recent results presented above support the following two properties shared
by all types of tree defense induced by bark beetle attacks: 1- the role of mechanical
wounding in inducing the tree response; 2- the non specificity of the tree response.
A third observation concerns the almost generalized and ubiquitous role of the
phloem parenchyma cells.
3.1.1. Induction by mechanical wounding

I hypothesize that, in all induced defenses in trees that concern bark beetle attacks,
mechanical wounding is the initial stimulus that induces the tree’s reaction and that
this reaction can be stimulated (amplified and accelerated) when fungi are present in
the wound. This is in agreement with the pioneer conclusions by Müllick (1977) for
the balsam wooly adelgid in Abies, root rot (Phellinus weirii) in Pseudotsuga
menziesii, arid blister rust (Cronartium rubicola) in Pinus monticola regarding the
generality of the role of wounding. However, Müllick’s observations did not deal
with tree defense but basically with tissue restoration (wound periderm). Moreover,
44 F. LIEUTIER
only a positive or negative interference of the aggressors with tissue restoration was
reported, without mentioning a possible stimulation. Regarding bark beetle attacks,
Reid et al. (1967) already mentioned the role of fungi in aggravating and expanding
wound effects for attacks on Pinus contorta by Dendroctonus ponderosae, but they
did not make conclusions regarding induction, nor did they generalize their
observations. In experiments with Scots pine (Pinus sylvestris) submitted to attack
by Ips sexdentatus and Tomicus piniperda, Lieutier et al. (1988, 1995) suggested
that wounds caused by the tunnelling activity of the beetles induced a hypersensitive
reaction which was eventually completed by an amplification of the tree response by
the fungi. Lieutier (1993) generalized this cause-and-effect relationship to all
interactions among conifers, bark beetles, and fungi . It also seems possible to
extend these conclusions to delayed induced resistance (Krokene et al., 1999) and
the formation of traumatic resin ducts (Nagy et al., 2000). Franceschi et al. (1998,
2000) corroborated these conclusions by observations at the cellular level for the
hypersensitive reaction and induced resistance in Norway spruce. Induced resin
flow, by definition, is a wound response (Ruel et al., 1998); the presence of fungi
could probably enhance it but no information is available yet to test this prediction.
3.1.2. Non specificity of tree responses

This non-specificity results from the fact that tree responses are responses to
wounding. I thus also hypothesize that all tree-induced reactions against bark
beetles and their associated fungi are non-specific, which is that the corresponding
qualitative changes in the tree tissues do not depend on the aggressors. Only the
intensity of the changes varies with the nature of the aggressor. That has been
demonstrated directly for different levels of tree reactions, through biochemical
(terpenes and phenols) or histological approaches: hypersensitive reaction (Wong
and Berryman, 1977; Delorme and Lieutier, 1990; Lieutier et al., 1991b; Brignolas
et al., 1995a; Raffa and Smalley, 1995; Franceschi et al., 1998); wound periderm
(Müllick, 1977); induced protection (Krokene et al., 1999); and traumatic resin
ducts (Tomlin et al., 1998; Nagy et al., 2000). It is also a priori true for induced
resin flow because it is typically a wound reaction.
3.1.3. Role of phloem parenchyma cells

The phloem parenchyma cells play an essential role in the development of the
hypersensitive reaction in regard to the syntheses of both terpenes and phenols.
Previously suggested by Reid et al. (1967), Berryman (1972) and Lieutier and
Berryman (1988a), Franceschi et al. (1998) recently demonstrated this role.
Franceschi et al. (2000) subsequently generalized the role of the phloem
parenchyma cells to all cases of tree response to bark beetles (except induced resin
flow), although their influence on the formation of traumatic resin ducts (and the
resulting induced protection) and wound periderm is indirect, as previously
suggested by Bois and Lieutier (1999). The structure and development of the PP
cells in Norway spruce have recently been presented in detail by Krekling et al.
(2000).
3.2. BIOCHEMICAL CHARACTERISTICS OF THE RESPONSE

The products synthesized by the tree have been identified for the case of the
hypersensitive reaction, but not for induced resin flow or traumatic resin ducts.
Furthermore, studies have been conducted almost exclusively at the phloem level,
where an increase of more than 100 times in terpene concentration was observed
(Shrimpton, 1973; Raffa and Berryman, 1982b; Lieutier et al., 1991b; Raffa and
Smalley, 1995), accompanied by an increase in the level of phenols and a reduction
in free sugar concentration (Shrimpton, 1973). Although the relative composition of
monoterpenes and resin acids varied slightly (Russell and Berryman, 1976; Raffa
and Berryman, 1982b; Langström et al., 1992), the most important alteration was an
absolute increase in the concentration of these substances (Delorme and Lieutier,
1990; Lieutier et al., 1991b; Raffa and Smalley, 1995). Phenols however show a
considerable change in their relative composition, with the concentration of some
compounds decreasing while others increase, some even being new for the tissue
(Brignolas et al., 1995a; Lieutier et al. 1996a). However, no new compounds are
synthesized at tree level, since the final composition of the phloem reaction zone
resembles that of heartwood (Shrimpton, 1973; Lieutier et al., 1991a).
Nonetheless, these compounds are new in the tissues where the reactions took
place, at least for phenols. They originate from neosynthesis and not from a
degradation of pre-existing products, since both an alteration of the enzymatic
activity of the stilbene synthase (STS) and chalcone synthase (CHS) (Brignolas et
al., 1995b), as well as gene activation (that is an increase of the mRNA of the
enzymes STS and PMT [pinosylvine methyl transferase]), were observed (Chiron et
al., 2000). For terpenes, the observed increase in terpene cyclases (Steele et al.
1995) and terpene synthases (Steele et al. 1998) results from a stimulation reaction,
since the final products were previously present in the phloem. Although the
synthetic pathways mentioned were studied in isolated reactions, they are correlated
with tree resistance, as demonstrated by different authors, for the terpenes (Raffa et
Berryman, 1982b; Christiansen, 1985b; among others) and the phenols (Shrimpton,
1973; Brignolas et al. 1995b, 1998; Bois and Lieutier, 1997).
3.3. ORIGIN OF THE ENERGETIC COMPOUNDS USED IN THE INDUCED

RESPONSES
Research in this field has tackled the hypersensitive reaction only. Since sugar and
starch concentration in the phloem decrease rapidly in the close vicinity of the
reaction zone (Shrimpton, 1973, Christiansen and Ericsson, 1986; Miller and
Berryman, 1986), these compounds are certainly used by the tree as an energy
source for the induced response. However, they may also be consumed by the
fungus for its growth, at least inside the reaction zone. Also, the energy demand is
considerable during the reaction process, especially when attacks are numerous, and
most studies have concluded there is a mobilization of products from the current
photosynthesis, at least at a high level of attack density (Christiansen and Ericsson,
1986; Miller and Berryman, 1986; Christiansen et al., 1987; Christiansen, 1992;
Dunn and Lorio, 1992; Christiansen and Fjorne, 1993).
46 F. LIEUTIER
3.4. MODE OF ACTION UPON THE AGGRESSORS

The deterrence of the hypersensitive reaction upon the aggressive agents results
from a combination of both physical and chemical effects, as well as from nutrient
depletion in the reaction zone, which results in a reduced access to nutrients in the
living tissues. Considering both types of aggressors, insects and fungi, the physical
effects mainly consist in hardening of the resin impregnated tissues and resin
flooding from the saturated tissues into the galleries; these have consequences on the
beetles and fungi comparable to those of the preformed and induced resin flows.
The chemical effects themselves result from complementary actions of several
compounds from different chemical families rather than one particular group. In the
following, I shall focus on the chemical effects.
Reaction tissues and their resin are more toxic and repellent for beetles than
control tissues and preformed resins, and they also inhibit fungal growth more
efficiently (Bordasch and Berryman, 1977; Paine et al., 1987). This is certainly
because a minimum concentration of defensive chemicals in the reaction zone
appears to be crucial to contain the aggressors (Raffa and Berryman, 1983a;
Christiansen et al., 1987). Assays with purified compounds point to which
compounds are involved. At concentrations present in the reacting tissues, terpenes
are toxic or repellent for beetles either by contact or vapor (Smith, 1963, 1965;
Coyne and Lott, 1976; Bordasch and Berryman, 1977; Raffa and Berryman, 1983b,
Raffa et al., 1985; Delorme and Lieutier, 1990; Raffa and Smalley, 1995). Contact
and vapor have also inhibitory effects on the beetle-associated fungi (Cobb et al.,
1968; Shrimpton and Whitney, 1968; Raffa et al., 1985; Bridges, 1987; Delorme
and Lieutier, 1990). Raffa and Berryman (1987) claimed that, in general, terpenes
showing the largest increases in the reacting tissues have the most deleterious effects
on the beetles and their fungi. However, although some compounds such as
limonene may be more toxic than others (Raffa et al., 1985), all monoterpenes
exhibit a high toxicity for beetles and a high inhibitory effect for fungi at
concentrations close to that in the reaction zones (Delorme and Lieutier, 1990).
Effects of terpenes on both beetles and fungi thus seem to be due more to the total
quantity of monoterpenes rather than to some particular compounds (Berryman and
Ashraf, 1970; Raffa and Berryman, 1982a, b; Delorme and Lieutier, 1990; Lieutier
et al., 1991b; Raffa and Smalley, 1995).
Phenols have been assayed against fungi only and exhibited an effect by contact
(Brignolas, 1995; Bois et al., 1999; Evensen et al., 2000). In opposition to terpenes,
this effect is mainly due to particular compounds (Brignolas; 1995), and it is
remarkable that these compounds are generally those which are neosynthesized in
the reaction zone: pinosylvin and pinocembrin for pines (Hart and Shrimpton, 1979;
Hart, 1981; Bois et Lieutier, 1997), stilbene aglycons for spruce, with some acting
synergistically (Brignolas, 1995). However, the role of phenols is not clear yet and
they have not been directly demonstrated to play a role in nature. Moreover, in vitro
assays with wood pieces showed a very limited effect of phenols on various fungi
and particularly species of Ophiostoma (Loman, 1970; Hart and Hillis, 1974; Hart
and Shrimpton, 1979).
4. ROLE OF THE DEFENSE SYSTEMS

4.1. RAPIDITY
Rapid tree responses to attack by beetles and their associated fungi are critical in tree
resistance, and the timing of the different sequences of the response is important.
Under favourable climatic conditions, high populations of an aggressive bark beetle
can completely terminate their aggregation in 4-5 days to one week and sometimes
less (Payne, 1980; Raffa and Berryman, 1983a; Anderbrandt et al., 1988), whereas it
can take two or three weeks when the climatic conditions are less favorable or for
less aggressive bark beetles. Under these conditions, it is interesting to compare the
delay of beetle aggregation with the rapidity at which the different resistance levels
are built by the tree and at which the corresponding products can affect the
aggressors. Even when the mechanisms of the response start very early, the
essential delay for the tree is the appearance of sufficiently high concentrations of
the secondary metabolites, since these are the final products that act on the
aggressors.
Preformed defenses need practically no delay to occur since they are present
before the attack. High quantities of terpenes that are toxic for beetles (see
references above) are liberated at the moment of wounding, but also decrease very
rapidly. A reduction of the resin flow by 65% in 2-3 days has been reported for P.
contorta subjected to high attack densities (Raffa and Berryman, 1983a). Resin
flow can even dry up completely in 24 hours after wounding in loblolly pine (Ruel
et al., 1998).
Induced defenses, on the other hand, involve gene activation followed by
important changes in cell metabolism or cell division patterns and differentiation,
which takes time until the secondary metabolites appear at a high concentration.
The quicker responses are those that involve the lowest changes. Induced resin flow
needs three days to reach a high level (Ruel et al., 1998). This can allow it,
however, to relieve the preformed resin flow. Then, the induced resin exuded from
the sursaturated tissues involved in the hypersensitive response could, in turn,
relieve the induced resin flow. Under these conditions, and if the three systems are
effectively acting in the same tree, resin could potentially be emitted continuously
by the tree. However, the existence of the induced resin flow has not been
demonstrated yet in conifers other than loblolly pine.
Resin impregnation of tissue due to the hypersensitive reaction is clearly visible
in the phloem of pines, as soon as three days after fungus inoculation (Lieutier and
Berryman, 1988a). Although maximum after three weeks, the extent of the reaction
zone and the terpene content of the lesion are already very well developed in 10 to
15 days, while terpene concentration itself also reaches a maximum in 10 to 15 days
(Raffa and Berryman, 1982b; Lieutier et al., 1990; Raffa and Smalley, 1995).
However, the concentrations reached in the reaction zone, even if not maximum,
rapidly become sufficient to be lethal for a majority of insects. In P. resinosa and P.
banksiana, after three days, the concentrations reached in the phloem can kill 90-
95% of Ips pini (Raffa and Smalley, 1995). Regarding phenols, important
modifications in the relative proportions are observed in less than 10 days, with
some compounds increasing dramatically during that period (Brignolas at al.,
48 F. LIEUTIER
1995a,b). Histological changes in the PP cells were considerable at 12 days

(Franceschi et al., 1998). More complex changes are slower. The traumatic resin
ducts need more than two weeks to be built locally, one year or more at a distance of
several meters (Christiansen et al., 1999b, Nagy et al., 2000).
Consequently, the very fast preformed response corresponds to the beginning of
resistance, but it needs to be rapidly completed by other mechanisms for the tree to
resist bark beetle attacks. Induced responses, especially induced resin flow when it
occurs and the hypersensitive response, can certainly constitute a significant
resistance to the aggressors, at least with terpenes, relaying and completing the
effects of the preformed resin. The above considerations demonstrate that there is a
remarkable complementarity and “cooperation” between the preformed and the
different induced systems for at least two or three weeks following attack.
However, the above reported changes associated with the development of the
hypersensitive reaction have been observed after low-density inoculations. One may
wonder, however, if the tree can produce the secondary metabolites so quickly in
case of mass attacks (see below “beetle mechanisms of establishment”). Thus, the
hypersensitive reaction may not be so efficient against outbreak populations, except
when unfavorable climatic conditions occur for the beetles or when the resin flows
(preformed and induced) slow the aggregation process significantly. Nevertheless,
the most frequent situation is that of non-outbreak populations, which have
difficulties reaching high densities rapidly. In such conditions, the hypersensitive
reaction certainly plays a decisive role to protect the trees. The traumatic resin ducts
probably interfere with the long-term resistance only.
4.2. RELATIVE ROLE OF THE PREFORMED AND INDUCED DEFENSES: A

TREE STRATEGY?
The mechanisms of the tree responses are increasingly elaborated and complex
going from preformed to long term induced defenses. All defense systems are
costly in terms of energy demand but they differ in the way the energy is used for
defense. The advantage of the preformed system is that, since defenses are built
before beetle attack, they are ready to act, with no delay, at the very moment beetles
attack. However, a high quantity of energy has been mobilized, which can be of no
use if no attack occurs. Alternatively, the advantage of induced defenses is to
mobilize the energy for defense only if attacks occur and only at a quantity
necessary to stop the aggressors. But this introduces a delay in the response of the
tree, which is the longest for the most elaborate defense systems.
On this energy basis, Matson and Hain (1985) have suggested that, in pines,
preformed defenses would be predominant in situations (seasons, regions, tree
species) where trees are subjected to heavy and repeated (continuous) attack
pressure. Induced responses would be mainly used in situations where repeated
attacks occur over multiple generations in a season. Indeed, preformed induced
defenses have been observed to play an important role in loblolly pine and other
southern pines which are subject to asynchronous attacks all year round, while the
hypersensitive reaction plays the major role in lodgepole pine and other western and
northern pines exposed to only a few beetle generations per year. Christiansen et al.
(1987) have extended this hypothesis to all conifer genera, arguing that spruce and
firs, which have non-efficient preformed defenses, live in cooler and more humid
climates than pines where bark beetle attacks are less frequent. These theories
presume that bark beetles have played a significant role in shaping the evolution of
conifer defenses.
The role of resin flow relative to the hypersensitive reaction seems however to
depend essentially on the particular direction of the beetle maternal galleries (see
below), in relation to the anatomy of the resin duct system. D. frontalis bores
winding galleries, which sever numerous vertical resin ducts in loblolly pine. In
beetles with vertical galleries such as D. ponderosae in the northern U.S. and I.
typographus in Northern and Central Europe, few resin ducts are cut, while the
hypersensitive reaction is stimulated because of its preferential development in the
vertical direction. In Norway spruce, the hypersensitive reaction plays the main role
in stopping the attacks of I. typographus (Christiansen and Horntvedt, 1983) while
preformed defenses in the same trees are responsible for stopping attacks by D.
micans (horizontal galleries) (Wainhouse et al., 1990; Lieutier et al., 1992). Pine
Ips species can have more than two generations per year, especially in Southern
Europe (Chararas, 1962), and although the hypersensitive reaction plays the most
important role (Lieutier et al., 1988; 1995), they have vertical galleries. In
southwestern China, Yunnan pine (P. yunnanensis) is attacked simultaneously by T.
piniperda (vertical galleries) and T. minor (horizontal galleries) (Ye and Ding,
1999). In firs, which have no resin duct system, of course only induced defenses
interfere regardless of the orientation of the galleries, as for S. ventralis and its
horizontal galleries.
In fact, it seems that all kinds of galleries and beetle behaviors can be found in
all tree species. Closer to the theory proposed by Raffa and Berryman (1987), it
thus seems more reasonable to consider that the beetle species have adapted (in
various ways) their behavior and attack strategy to the existing host mechanisms of
resistance than to consider that tree defense strategies have evolved in response to
the attack behaviour of few beetle species. Submitted to attacks by various
xylophagous insects, conifers have probably elaborated a wide array of defense
mechanisms, all present in the different conifer species to varying degrees, to try and
contain all kinds of attacks (this may be the reason why all tree responses are
basically not specific as to the aggressors). Then, beetle strategies have evolved to
try and cope with the host defense mechanisms, but differ according to beetle
species, each of them evolving its own attack strategy, even in the same conifer
species (See below beetle strategies). This does not preclude, however, the
possibility that some particular tree compounds may have evolved under the effect
of bark beetle attacks (Sturgeon and Mitton, 1982). Lombardero et al. (2001) have
suggested that environmental factors could have different effects on the constitutive
and induced defenses (resin flows) in loblolly pine. The predominance of one or the
other defense system in the same tree could thus depend on environmental
conditions. If it were verified for the hypersensitive reaction also, this suggestion
would corroborate the above hypothesis, since it could explain the particular
(sinuous) pattern of D. frontalis galleries.
50 F. LIEUTIER
Otherwise, an interaction between the different defense systems is certainly

frequent. That has been mentioned above (see II.1.1.) between the constitutive
defense and the hypersensitive reaction of spruce against D. micans (Wainhouse et
al., 1997). In P. contorta, the rate of preformed resin flow conditions the emission
of aggregation pheromones by the pioneer D. ponderosae (Raffa and Berryman,
1982a). Since a rapid aggregation is necessary to overcome the tree’s induced
defenses (see VI.1.1.), this underlines again interactions between preformed and
induced defenses (Raffa et al., 1993). Moreover, at least for phenols, the same PP
cells seem to be involved in constitutive, hypersensitive and delayed resistance
(Franceschi et al., 2000), which means an interaction among these different systems.
5. BEETLE MECHANISMS OF ATTACK AND ESTABLISHMENT

With such sophisticated and elaborate defense systems complementing each other in
the tree, how can bark beetle attacks succeed? This point will be discussed while
referring to the most frequent situation: exhaustion of tree defenses associated with
beetle establishment and tree death, which corresponds to the situation of most tree
killing bark beetle species. Paine et al. (1997) stated that it is critical, at this step, to
distinguish between exhaustion of tree defenses and sapwood occlusion and
colonization by fungus. More broadly, this can be extended to phloem colonization
by beetles. However, as we shall see below, it does not seem that this distinction
can really, be done in time, since phloem and sapwood invasions start before
defenses are exhausted.
5.1. EXHAUSTION OF HOST DEFENSES

Considering the hypersensitive reaction, Shrimpton (1978) suggested that the fungi
introduced by the beetles at the moment of attack kill the tree cells, leading to no
more resin synthesis and secretion, thus allowing the establishment of the beetle
population. Tree death would thus be a pre-requisite to the invasion by the
aggressors. In fact, the stopping of resin production would not be caused by cell
death, but rather by an exhaustion of the ability of the tree to synthesize resin. The
problem would thus stand at the level of the tree itself and not at the level of the
defense reaction.
5.1.1. The mechanisms

Rapidity, together with a minimum number of simultaneous attacks, is necessary for
beetle success. Various observations demonstrate that a threshold of attack density
(number of attacks per unit bark surface) exists above which the attacks succeed,
while they fail below (Berryman, 1976, 1982; Raffa and Berryman, 1983a;
Christiansen et al., 1987). The existence of such a threshold is explained by the
necessity of weakening tree resistance. According to Hodges et al. (1985) and
Nebeker et al. (1993), in the southern US, a number of attacks would be necessary
to ensure a complete circumferential introduction of fungus into the tree, a necessary
condition for the fungus to produce toxins that would alter physiological processes
in the tree, weaken its resistance and make it more susceptible to subsequent attacks.
Another explanation, proposed for situations in the northern US and Europe, is
based on energetic considerations. Indeed, syntheses of the secondary metabolites
(terpenes and phenols) involved in resistance are energy-demanding processes
(Croteau et al., 1972; Croteau and Loomis, 1975). Their stimulation by numerous
attack points in rapidly increasing numbers would increase the energy demand
considerably. Above a certain density of attacks (threshold of attack density), the
tree would not have any more capacity to rapidly mobilize the energy necessary to
keep the induced or stimulated metabolic activities at a high level in all zones of
attack. The concentrations of defensive chemicals in the reaction zones would thus
not increase rapidly enough or to a sufficient level to contain the aggressors, and
attacks would succeed. If the beetle attack density stays below this critical
threshold, tree defenses would not be depleted and attacks would finally fail. The
existence of a threshold of attack density has been demonstrated in various tree
species after natural beetle attacks (Waring and Pitman, 1980, 1983; Mulock and
Christiansen, 1986; Langström et al., 1992; Langström and Hellqvist, 1993; Guérard
et al., 2000). According to that strategy, the role of a high number of attacks is to
induce numerous reactions that will be stimulated by the beetles tunneling activity
and the presence of fungi. The role of fungi in accelerating tree energetic
expenditures and thus lowering the threshold is evidenced by observations of natural
infestations with little or no blue stain, in which attack densities were higher than in
situations where blue stain fungi were present (Whitney and Cobb, 1972; Bridges et
al., 1985). Similarly, and simulating bark beetle attacks, it is possible to
experimentally define a critical threshold of inoculation density (for a given height
of inoculation belt) above which tree resistance is overcome and the tree is killed
(Raffa and Berryman, 1983b; Horntvedt et al., 1983; Christiansen, 1985b;
Langström et al., 1993; Solheim et al., 1993; Croisé et al., 1998a; Guérard et al.,
2000). However, this threshold is weakly related to the critical threshold of attack
density (see the reasons in VI.3).
It is important to remember that, while boring their galleries into the phloem,
beetles most often damage the cambium and the surface of the sapwood as well, and
consequently inoculate the tree with the fungi at these different levels. Artificial
fungus inoculations do the same since they are performed at the cambium level.
Tree resistance and the development of hypersensitive reactions thus take place
simultaneously in each of these tissues from the very beginning of the attack, against
the beetle and fungi in the phloem and cambium, and against the fungi in the
sapwood. The mechanisms described above of exhaustion of tree defense thus take
place in all these tissues, especially in the phloem and the sapwood because of their
larger volume.
5.1.2. The rapidity of the stimulation

In Norway spruce, artificial inoculations with a fungus (O. polonicum) have been
reported to begin to stimulate the quantity of secondary metabolites induced by
wounding after only 7 or 10 days (Brignolas et al., 1995a). This may seem too slow
for that stimulation to rapidly lower the threshold of attack density and allow beetle
establishment. However, the important thing in the above strategy is not the final
52 F. LIEUTIER
products but rather the mobilization of the energetic resources. The mechanisms of
the hypersensitive reaction start largely before seven days as does the mobilization
of the energetic resources. Regarding phenols, stilbene synthase and chalcone
synthase activities in Norway spruce are already very strongly stimulated six days
after inoculation (Brignolas et al., 1995b), demonstrating that the stimulation starts
largely before day six. In Scots pine, after wounding, the mRNA of STS and PMT
have already increased considerably in three days, indicating that the tree response
started before three days after the attack, although no earlier measurements
occurred. After a fungus inoculation, a higher increase occurs with the same delay,
thus demonstrating early stimulation (Chiron et al., 2000). Considering terpenes,
monoterpene synthase activity in the hypersensitive reaction zone has already
increased three fold six hours after wounding and ten fold in two days, with the
maximum being reached in 12 days (Steele et al., 1998). Diterpene and
sesquiterpene synthase activities increase a few days later but this is not surprising
since monoterpenes act as a solvent for these more complex compounds. It is very
likely that equally rapid responses in enzyme activities exist for the induced resin
flow too.
5.1.3. Conditions for fungus efficiency

By themselves, the fungi do not stimulate the tree defense mechanisms under any
circumstances. In the phloem hypersensitive response in particular, a minimum
number of spores must be introduced into the tree by the beetle. Indeed, the
existence of a positive relationship between the number of spores artificially
introduced and the concentration of secondary metabolites in the phloem reaction
zone has been demonstrated (Lieutier et al., 1988, 1989a). In most experiments with
trees, artificial inoculations with 5 mm diameter discs of agar cultures are used to
study the tree response and to understand the role of the fungus in the tree-bark
beetle relationships. Such discs, however, contain such a high number of spores (for
example, more than one million in a 5 mm diameter disc of a 3-week old culture of
Leptographium wingfieldii, a fungus associated with T. piniperda) that the tree
reaction is always stimulated and maximum (Lieutier et al., 1989a). Certainly, the
beetles do not carry such high numbers of spores. Interpretations and conclusions
regarding the role of the fungi during beetle attacks must be taken with care when
they are made based on experiments using artificial inoculations, because they may
not correspond to the natural situation where the fungus is introduced into the tree
by the beetle itself.
5.2. TISSUES COLONIZATION AND TREE DEATH

It is very difficult to define the moment of tree death. Paine et al. (1997) considered
that “gallery construction and oviposition can be used as a bioassay to indicate when
tree mortality has occurred”. However, tree death is very likely a continuum of
events beginning with exhaustion of tree defenses (just before oviposition) and
finishing with the blockage of sapwood water transfer and the fading of foliage
(which can take place several weeks after beetle oviposition).
According to Paine et al. (1997), the assumption that fungi play an important
role in killing trees attacked by bark beetles is based on the following observations:
most bark beetles vector staining fungi; the sapwood of bark beetle killed trees is
stained; and trees can be killed by artificially mass inoculating them with the fungi.
Many papers have been published in these directions and references can be found in
the review by Paine et al (1997). We can also add that beetles which do not vector
fungi, either succeed in establishing in their host without killing it (D. micans or
Dendroctonus punctatus for example), or are very secondary beetles which only
attack trees that are already dead. Nevertheless, all these observations do not allow
definitive conclusions about the role of fungi in the tree killing process. They even
do not allow concluding that fungi are involved in tree death at all. Indeed, there is
still the possibility that fungi exploit the beetle for transportation and invade the
sapwood after the tree has been killed by something else. Artificial mass
inoculations may not represent the situation of natural attacks (see below the case of
T. piniperda). Also, the lack of fungi associated with D. micans may be the
consequence of the beetle not killing its host and not the opposite. Moreover, trees
have been reported to be successfully colonized and killed by bark beetles without
blue stain fungi (Ophiostoma) (Whitney and Cobb, 1972; Bridges et al., 1985). On
the other hand, Pinus taeda attacked by Dendroctonus frontalis have been observed
to remain alive despite extensive blue stain in the sapwood (Nebeker et al., 1993). It
is possible, however, that fungi other than blue staining ones play a role.
However, there must be a reason why most tree killing bark beetles are
associated with blue stain fungi. Stimulating tree defenses and helping in
overcoming tree resistance is certainly a good and sufficient one. In fact, beetles do
not need fungi to kill the tree but only to exhaust tree defenses. After host defenses
are exhausted, beetle establishment can begin. But, at this moment, since
pathogenic fungi are present in the tree, they certainly play a role in the subsequent
tree killing process, although it is probably not their primary role. Another
important fact to consider is that, although variations in pathogenicity exist among
species of fungus, all bark beetle associated blue stain fungi are only moderately
pathogenic.
Tree death very likely results from several phenomena acting in concert.
Berryman (1972) already suggested that a tree is killed as a result of simultaneous
actions of the insect and fungus rather than successive action of vector and
pathogen. Beetles and fungi already cooperate in overcoming tree resistance and
their respective role in that step has been presented above (see also below), but little
is known regarding their respective roles in tree death. When tree resistance has
been overcome, beetle establishment begins and death of the tree is considered as
assured (Berryman, 1982; Wood, 1982). As already mentioned, exhausting tree
resistance can be completed in few days. However, tree death comes much later
with disruption of water transportation, sapwood occlusion and fading of the foliage
(DeAngelis et al., 1986; Nebeker et al., 1993; Lorio et al., 1995).
Sapwood invasion by fungi probably plays a role in tree death, but the
mechanisms are certainly more complex than this alone. Fourteen days after attack
by D. ponderosae, lodgepole pine sapwood is occluded to a depth of only 20 mm
(Solheim, 1995), and the fungus invades not more than 18 % of the tracheids until
54 F. LIEUTIER
10 weeks have passed (Ballard et al., 1984). Likewise, in Norway spruce fungi are
present in the sapwood at a depth of 18 mm five weeks after successful attacks by I.
typographus (Solheim, 1992). Several other similar observations are reported in the
review by Paine et al. (1997). One may thus wonder if tree resistance has really
been completely exhausted at this time in the sapwood, or if fungi are really
involved in tree death. Perhaps fungi can kill trees with toxins (DeAngelis et al.,
1986; Hodges et al., 1989). Moreover, the presence of a certain area of blue stained
sapwood in trees resisting beetle mass attacks or artificial mass inoculations with
fungi demonstrates that colonization of tree tissues starts during the process of
defense exhaustion. This phenomenon has even been frequently cited to account for
comparisons of the resistance levels of different tree categories (Christiansen and
Berryman, 1995; Christiansen and Glosli, 1996; Bois and Lieutier, 1997; Brignolas
et al., 1998; Krokene et al., 1999, among others). In addition, in response to
increasing densities of fungus inoculations staying below the critical threshold,
sapwood occlusion gradually increases along with the quantity of non-functional
sapwood (Guérard et al., 2000).
Mechanisms other than fungus invasion also obviously interfere. The beetle
population itself while colonizing the phloem, and consequences of other events
taking place in this tissue, certainly play a role at this stage, since tree death is more
rapid after insect attacks than after artificial mass inoculations. Moreover,
the relations between foliage symptoms, sapwood drying and occlusion, and fungus
extension into the sapwood are not clear (Parmeter et al., 1992; Harrington, 1993;
Hobson et al., 1994). As in the exhaustion of tree defenses, tree death certainly
results from a combination of effects from bark beetles and the fungi they vector. In
addition, sapwood tree defense mechanisms themselves may also contribute

significantly in sapwood occlusion and tree death when defense reactions lead to
extended resin soaking in the sapwood. Indeed, following artificially induced mass
attacks by T. piniperda on Scots pines baited with terpenes, some of the killed trees
had about 30% of their sapwood section soaked with resin with no blue stain; the
resin impregnated zones were located exactly beneath the galleries (Figure 8 and
Lieutier et al., unpublished).
5.3. CONCLUSIONS
It is not at all obvious that the death of the tree is a prerequisite for beetle
establishment. Rather, it seems that beetle population establishment proceeds in two
successive (and not simultaneous) steps: 1- exhaustion of tree defense; 2- tree killing
and completion of invasion of the tree tissues by the aggressors. This statement is in
agreement with the conclusions by Parmeter et al. (1992), Nebeker et al. (1993) and
Hobson et al. (1994). Meanwhile, Berryman’s statement about tree killing (1972)
can be enlarged and specified by inferring that both insect and fungi are needed to
kill the tree after both are needed to overcome its resistance. The phenomena
involved during the time sequences leading to beetle establishment would be the
following: First, tree resistance is weakened, through the stimulation of tree defense
mechanisms leading to their exhaustion by the aggressors. During that first step, the
aggressors begin to invade the tree tissues (beetles and fungi in the phloem, fungi in
the sapwood), but their extent remains very limited by the still efficient defenses of
these tissues. Next, after the tree defenses are exhausted, the aggressors freely
invade non-resistant tree tissues, while the tree dies as a result of exhaustion of its
defenses. The free invasion of the tree tissues has two components: 1- rapid
invasion of the phloem by the insects, with oviposition and brood development, i.e.,
beetle population establishment; 2- slow invasion of the sapwood by the fungus,
associated with sapwood occlusion. The establishment of the beetle population thus
begins before the tree is killed, as soon as the tree’s resistance is overcome.
One may wonder why the tree killing bark beetles are not associated with highly
pathogenic fungi. Indeed, such fungi would exhaust tree defenses and kill the tree
with just a few inoculation points, whereas moderately pathogenic fungi need many
inoculation points for the same results. The reason could be the necessary existence
of the above two steps for successful brood development. Indeed, if a highly
pathogenic blue stain fungus exhausted a tree’s defenses and killed the tree very
rapidly, it would also certainly invade the whole tree very rapidly before the beetle
and its brood became established, making the host tissues unsuitable for brood
development. An association with a moderately pathogenic fungus is a better
strategy for the beetle. It allows beetles to overcome tree resistance while limiting
fungus extension, thus preserving the quality of the substrate for the beetle’s
progeny. Protecting the quality of the tree’s tissues may also be a reason for not
killing the tree before beetle establishment begins. The existence of the two
successive steps presented above is thus a necessity for the brood to find a suitable
substrate, as well as the logical consequence of an association with only moderately
pathogenic fungi.
56 F. LIEUTIER
6. BEETLE COLONIZATION STRATEGIES

Raffa (1991) proposed three kinds of colonization strategies for bark beetles
attacking living trees: overwhelming the defenses of healthy trees; avoiding resistant
trees; and avoiding/tolerating resistant responses within trees. According to Raffa et
al. (1993), the first situation corresponds to an aggressive strategy developed by the
regular tree killers (near-obligate parasites), while the second one corresponds to a
non-aggressive strategy developed by saprophytic (facultatively parasitic) species.
However, since the resistance of living trees is never nul, beetles belonging to the
second group, when arriving on their host tree, necessarily still have to choose
between overwhelming tree resistance and avoiding tree responses. If they were
able to avoid tree responses, very likely they would be able to develop in healthy
trees. Consequently, they certainly use the strategy of overwhelming tree resistance.
Closer to what has been suggested by Lieutier (1992), I thus propose to distinguish
two basic colonization strategies for all bark beetle species attacking living trees: 1-
Exhausting tree defenses and killing the tree, corresponding to the above
presentation. In that strategy, two sub-groups can be distinguished according to host
vigor (healthy versus weakened). 2- Avoiding / tolerating tree defenses and keeping
the tree alive.
6.1. EXHAUSTION OF TREE DEFENSES: THE COOPERATIVE STRATEGY

Overcoming tree resistance is the first task that the beetles must perform. It is
accomplished through exploiting tree defense mechanisms by stimulating the
induced responses. This can be done in various ways but a high number of
simultaneous attacks are always necessary, leading me to call this strategy the
“population strategy” or the “cooperative strategy”. The tree is then killed as an
unavoidable consequence of defense exhaustion, especially through invasion of its
tissues by the aggressors: fungi in the sapwood, and beetles in the phloem. This
strategy can thus also be compared to that of a parasitoid. Most bark beetle species
attacking living trees belong to that category, be they primary or secondary species.
Only the way used to exhaust tree defenses and to overcome its’ resistance differs.
Examples of variations on such a strategy are presented below.
6.1.1. The “typical / classical” situation

This corresponds to the above-described mechanisms. A quick aggregation is
necessary to rapidly weaken the tree and not allow it enough time to develop an
extended local hypersensitive reaction or to build traumatic resin ducts.
Aggregation pheromones are thus a very useful tool for species using that strategy
(Wood, 1982; Raffa and Berryman, 1983a). As long as the critical threshold of
attack density is not reached, the beetles that have already arrived continue to release
aggregation pheromones. If too low a number of beetles rapidly aggregate on the
tree, the attack density stays below the threshold, tree defenses cannot be exhausted
and the attack finally fails. On the contrary, if a sufficiently high number of arrivals
allow the beetle population to rapidly reach the critical threshold, tree resistance is
overcome. The pheromone emission is then stopped which limits further

intraspecific competition among the brood members (larvae and callow adults)
(Berryman, 1982; Raffa and Berryman, 1983a; Birgersson and Bergström, 1989;
Raffa et al., 1993). During the aggregation process, all contributions to deplete the
tree’s ability to synthesize secondary metabolites and thus to exhaust the tree’s
defenses are important in order to overcome the tree’s resistance. , Anything that
lowers the critical threshold helps to improve the probability that the attack will be
successful. In this context, the pathogenic fungi introduced by the beetles play an
essential role through stimulating tree syntheses (Berryman, 1976; Whitney, 1982;
Raffa and Berryman, 1983a; Christiansen et al., 1987; Lieutier, 1992; among
others). Similarly, attacks during the season of active tree growth and vertical beetle
galleries fit in with this strategy because they stimulate the tree’s metabolic activity
(Lieutier, 1992).
As a summary, the “classical” situation in the strategy of exhausting tree
defenses is that of bark beetle species typically filling and sharing the following four
main conditions: ability to release aggregation pheromones; association with
phytopathogenic fungi; attack during the season of maximum tree activity; and
vertical egg galleries. On the other hand, tolerance to resin can change with beetle
species, depending on the vigor of the trees that are usually attacked. That strategy
concerns I. typographus, D. ponderosae, D. brevicomis, I. acuminatus, etc., and
most other bark beetle species that synthesize aggregation pheromones and attack
Pinus, Picea or Larix. Although using the same general strategy, all these species
can be ranked along a vigor gradient defined by the quality of the hosts that they can
attack, from the real tree killers that attack healthy trees to the species attacking very
weakened trees. It is also a ranking of beetle efficiency in overcoming tree
resistance. Because they have developed the most efficient mechanisms for that
task, the tree killing species have access to a large quantity of food that is not
available for the other ones. This has led to considering them as the most evolved
species (Raffa et al., 1993).
6.1.2. Other closely related situations

There are situations where the above 4 conditions are not all filled, although the
same strategy is used.
T. piniperda has no aggregation pheromone but aggregation occurs due to the
attractiveness of monoterpenes emitted through the wounds caused by the pioneer
beetles (Byers et al., 1985; Schroeder, 1987). This beetle is associated with a
fungus of the genus Leptographium everywhere this association has been looked for:
L. wingfieldii in Europe (Lieutier et al., 1989b; Gibbs and Inman, 1991; Solheim and
Langström, 1991), Leptographium yunnanensis in southern China (Zhou et al.,
2000). However, the beetles themselves, without the help of a fungus, overcome
tree resistance. Indeed, the associated pathogenic fungus L. wingfieldii is unable to
stimulate the hypersensitive reaction when it is introduced into the host tree by the
beetle itself (Lieutier et al., 1989a, 1995; Lieutier, 1995), although artificial
inoculations lead to violent reactions and its’ pathogenicity is high (Lieutier et al.,
1989b; Solheim et al., 1993; Croisé et al., 1998a). This discrepancy has been
attributed to the low number of spores introduced into the tree by the beetle (Lieutier
58 F. LIEUTIER
et al., 1989a, Lieutier, 1995). Moreover, the percentage of beetles carrying the
fungus is very low, around 5% (Lieutier et al., 1989b; Solheim et Langström, 1991).
Thus, during attacks by T. piniperda, only the repeated mechanical wounds caused
by the tunnelling insects can stimulate the tree’s hypersensitive reactions, which lead
to exhaustion of the tree’s defenses (Lieutier, 1993; Lieutier et al., 1995). Under
these conditions, overcoming tree resistance is difficult. Lieutier (1995) suggested
that it is the reason why T. piniperda can only establish successfully on very weak
trees in Europe. In such a situation it is also certainly easier to exhaust the host’s
defenses when tree metabolism is low. Attacks by T. piniperda always take place
largely before the trees start their activity in spring. After tree resistance is
overcome and certainly also because the fungus pathogenicity is rather high, L.
wingfieldii can invade the sapwood, even if the number of inoculation points is low.
The situation with T. piniperda is a clear example that intense hypersensitive
reactions (after low density artificial inoculations) and high pathogenicity (measured
through mass artificial inoculations) are not proof that the fungus plays a role in
stimulating the defense reactions, and thus in exhausting tree defense during natural
attacks (see above V.1).
D. frontalis follows the same general strategy in P. taeda, but it bores winding
galleries. P. taeda is the species where the existence of the induced resin flow has
been reported. The particular boring behavior of D. frontalis leads the beetles to cut
numerous resin ducts while boring the horizontal part of the galleries, which
probably explains why resin flows (constitutive and induced) play an important role
in tree resistance (Nebeker et al., 1993; Paine et al., 1997; Ruel et al., 1998). But
the hypersensitive reaction also plays a role (Paine and Stephen, 1988) because it is
actively stimulated while the beetles bore the vertical and oblique parts of their
galleries. Tree defenses are thus probably exhausted through stimulation of both the
induced resin flow and the hypersensitive reaction. In addition, D. frontalis has
aggregation pheromones and it attacks trees during their period of physiological
activity. Fungi also certainly play a role in helping the beetle in overcoming tree
resistance. However, in some situations and as for T. piniperda, death can occur
without sapwood invasion by blue stain fungi (Bridges et al., 1985).
S. ventralis bores transversal galleries in Abies. This behavior is not a handicap
since there are no resin ducts containing preformed resin in firs. Only resin pockets
(blisters) are disseminated in the cortex of the bark and thus are not met after the
phloem has been reached. Moreover, the beetles seem to be able to avoid them
(Ferrell, 1983). It is not known if aggregation pheromones exist but aggregation
occurs and a symbiotic fungus is present which stimulates the hypersensitive
reaction and then kills the tree by invading the sapwood after exhaustion of tree
defenses (Berryman and Ferrell, 1988).
Artificial mass inoculations with fungi are probably relevant to the same strategy
when they lead to tree death. At first, tree resistance is overcome through wounding
followed by stimulation of the hypersensitive reaction by fungi. Invasion of the
sapwood and the phloem by the fungi may be thought to occur after tree defenses
are exhausted. This is why the fungus model can be valuable for studying many
aspects of the conifer - bark beetle relationships.
6.2. AVOIDING / TOLERATING TREE DEFENSES: THE SOLITARY

STRATEGY
These beetles do not exploit the tree’s defenses to overcome the resistance of their
host, but they avoid or tolerate them. Typically, everything is done to minimize the
development of tree defenses. Only the local particularities of the stem or branches
of the host, at the place of each beetle attack, determine the success or the failure of
the attacks. Since there is no need for exhausting tree defenses, no cooperation is
necessary and the beetles behave individually, leading me to call this strategy the
“individual strategy” or the “solitary strategy”. As a logical consequence, the whole
beetle life cycle can take place without killing the tree, making that strategy
comparable to that of a parasite. Very few primary bark beetle species attacking
living trees are representative of this situation. Examples are given below.
6.2.1. The typical situation

Dendroctonus micans in Norway spruce in Europe is a good example. The
hypersensitive reaction is minimized by boring transversal female galleries and by
the absence of associated pathogenic fungi (Lieutier et al., 1992). Because of its
transversal gallery, the boring female must face the preformed resin flow but this
flow is weaker in spruce than in pines and the adults of D. micans are highly
resistant to resin (Grégoire, 1988). Aggregation pheromones do not exist at the
adult stage corresponding to an individual attack behavior. Local particularities of
the bole (preformed defenses) determine if the female can lay eggs. They include
preformed resin flow (Lieutier et al., 1992), stone cell masses (Wainhouse et al.,
1990, 1998), and moisture and stilbene content (Storer and Speight, 1996). Eggs
and larvae, which are directly facing the hypersensitive reaction since larvae are
boring vertically, are also very tolerant to resin (Everaerts et al., 1988). Broods
develop without killing the tree and several beetle generations can follow each other
in the same tree before tree death occurs (Vouland, 1991).
Opposite to the previous strategy, the “classical” situation in the strategy of
avoiding or tolerating tree defenses is bark beetle species that meet the following
four main conditions: no aggregation pheromones at the adult stage; no association
with a phytopathogenic fungus; horizontal galleries; and a high tolerance to resin for
both the adult and the larval stages. On the other hand, the period of attacks can be
anytime in the year since defenses are avoided. D. punctatus in North America
corresponds to the same situation as D. micans in Europe.
Because the trees stay alive while undergoing successful attacks for several
years, the question is raised regarding the role of the traumatic resin ducts.
Numerous resin ducts are built around the zone of brood development. Moreover, a
tree already attacked by D. micans is more easily attacked the following years with
the new attacks localized preferably in close vicinity to the previous ones, which is
at the place where the traumatic resin ducts are the most developed. The effective
role of these ducts is thus questionable and one may wonder if they interfere with
beetle establishment and tree resistance. Beetles are very tolerant to resin and it is
also possible that, by obliging the tree to build resin ducts continuously year after
60 F. LIEUTIER
year, they weaken it until it dies. Nothing is known about the cause of the death in a
tree attacked by D. micans.
6.2.2. Other closely related situations

D. valens and D. terebrans have a biology very similar to that of D. micans and D.
punctatus and they probably use the same strategy. They have no aggregation
pheromone at the adult stage, do not mass attack their host trees, and can reproduce
in living trees without killing them (Raffa, 1991). Their eggs are also very tolerant
to resin. They differ from D. micans in that they are associated with a highly
pathogenic fungus (L. terebrantis) which causes extensive defense reactions when
artificially inoculated to the host at a low density (Barras and Perry, 1971, Raffa and
Smalley, 1988). However, it has not been demonstrated that this fungus causes the
same hypersensitive reaction when introduced into the tree by a beetle, and it has
also not been shown that it plays a role in exhausting tree defenses and in promoting
beetle establishment. Likewise, no advantage has been revealed for the beetles from
harbouring the fungus . As for D. micans, the beetles’ strategy thus seems to be an
individual one of avoiding and tolerating tree defenses. The presence of the fungus
is probably just a passive vectoring of a disease.
6.3. BEETLE AGGRESSIVENESS AND FUNGUS PATHOGENICITY

The description of the cooperative versus solitary strategies above raises issues
regarding beetle aggressiveness. In the solitary strategy, the ability of the beetles to
develop in live trees makes them all aggressive (primary) species.
In the cooperative strategy, the efficacy of the fungus in stimulating the reactions
and exhausting tree defenses is essential for successful beetle attack. There is no
relationship between beetle aggressiveness (primary versus secondary beetles) and
fungus pathogenicity (Harrington, 1993; Paine et al., 1997). Pathogenicity is the
ability of the fungus to kill the tree. It is measured by artificial mass inoculations in
the case of beetle-associated fungi and it thus differs from the ability of the fungus
to stimulate tree defenses during a natural beetle attack (see comments above). O.
polonicum is associated with I. typographus, a very aggressive bark beetle, O. ips
and O. brunneo-ciliatum are associated with I. sexdentatus and I. acuminatus, two
moderately aggressive beetles, and L. wingfieldii is associated with T. piniperda
which is characterized by a very low aggressiveness (it is sometimes considered as a
secondary beetle). However, O. polonicum and L. wingfieldii are both highly
pathogenic fungi, as shown by artificial mass inoculations to the host trees
(Horntvedt et al., 1983; Christiansen, 1985b; Solheim and Langström, 1991;
Solheim et al., 1993; Croise et al., 1998a). Also, both of them strongly stimulate
tree defenses when artificially inoculated into the beetle’s host tree at low densities
(Christiansen and Horntvedt, 1983; Lieutier et al., 1989b). O. ips and O. brunneo-
ciliatum have a very low pathogenicity (Guerard et al., 2000) and moderately
stimulate host tree reactions (Lieutier et al. 1989b) when artificially inoculated.
Thus, when fungi are artificially inoculated to trees, there is no relation between
beetle aggressiveness and fungus pathogenicity. There is also no relation, in this
artificial situation, between beetle aggressiveness and the ability of the fungus to
stimulate the tree’s defenses.
However, the results of research on the relationships between I. typographus, O.
polonicum and Norway spruce have demonstrated that O. polonicum has a high
ability to stimulate the tree’s reactions in cases of natural attacks by beetles and thus
the fungus helps greatly in exhausting tree defenses (Christiansen et al., 1987).
Studies on the relations between I. sexdentatus, O. brunneo-ciliatum (or O. ips) and
Scots pine have demonstrated that O. brunneo-ciliatum has a moderate ability to
stimulate the tree’s reactions (Lieutier et al., 1995). Opposite to O. polonicum and
in spite of its similar high pathogenicity, L. wingfieldii is absolutely unable to
stimulate the hypersensitive reactions of the host in cases of natural attacks by T.
piniperda (see above). Thus, it seems that there is a relation between beetle
aggressiveness and the ability of the fungus to stimulate the tree’s reaction during a
beetle attack.
We can thus hypothesize that, for beetle species choosing the cooperative
(exhaustion) strategy, beetle aggressiveness is directly related to the ability of the
fungus to stimulate the tree’s reaction during a beetle attack. The ability to kill the
tree after exhausting its’ defenses may be related to fungus pathogenicity, but this is
nota requirement. Instead, it may be related to the ability of the fungus to grow into
the sapwood. The percentage of contaminated beetles does not need to be very high
for that step (as in the case of T. piniperda).
From the above discussion, I conclude that there is no relation between fungus
pathogenicity (measured by artificial inoculations) and the ability of the same
fungus to stimulate the tree’s hypersensitive reaction during a beetle attack.
Consequently, there are certainly only very weak relations, if any, between the
threshold of attack density and the threshold of inoculation density. This is in part
due to the fact that frequently much less than 100% of the beetle population carries
the fungus, and that the number of fungus spores introduced by a beetle into a tree
certainly differs greatly from that contained in an artificial inoculation (see VII.2).
However, determining the critical threshold of inoculation density can be very useful
to compare the resistance level of different tree categories or to compare fungus
pathogenicity.
7. QUESTIONS AND RESEARCH PROSPECTS

Several aspects of the conifer – bark beetle – fungus relationships related to tree
resistance are still not understood and need to be investigated.
7.1. DEFENSE MECHANISMS

In addition to specifying the mechanisms and the effects of the newly discovered
defenses (especially “preformed induced resin” and “induced resistance”), several
aspects of the “old” mechanisms still remain to be understood. The defense
mechanisms have almost always been studied with low-density inoculations, when
the tree easily stops the aggressors, but several questions need to be answered to
understand how tree resistance is overcome. How do the defense mechanisms work
62 F. LIEUTIER
when the attacks are close to the critical threshold of attack density? Do they work
in the same way as when inoculation (i.e., attack) densities are low? What critical
changes occur in defense mechanisms when the threshold is reached? Are the
changes qualitative or quantitative? Are the reactions suddenly inefficient or does
their efficacy decrease gradually? Is the crossing of the threshold brutal or
progressive -- do all attacks fail below the threshold and all attacks succeed above,
or is there a progressive increase in the percentage of successful attacks?
The hypersensitive reaction has been mostly studied in the phloem but the
existence of resin-impregnated zones in the sapwood demonstrates that resistance
takes place at this level also. However, sapwood defense mechanisms have almost
never been investigated in the case of bark beetle attacks. Paine et al. (1997) stated
that exhausting the host defense system corresponds to phloem colonization, but the
development of sapwood defenses also certainly contributes to exhausting the host’s
defenses.
7.2. STIMULATION OF THE INDUCED REACTIONS

The importance of wounding in the elicitation and development of all kinds of tree
defenses emphasizes the role of the insect itself and its boring activity. This role has
been largely under-estimated until now and should be investigated thoroughly. The
respective role of the beetle and the fungus in the stimulation of tree defense
reactions must be clarified, as well as the way the fungus stimulates the defense
mechanisms (additional wounds, enzymes). In addition, the real demonstration of
this role for the fungus should be looked for in several tree - bark beetle - fungus
relationships. Indeed, the presence of a pathogenic fungus carried by the beetle is
not sufficient proof by itself (cf. T.piniperda ).
The percentage of beetles contaminated by a fungus varies greatly among beetle
species, and even for the same fungus and beetle species among different localities
and years (Paine et al., 1997). It is usually very low for I. typographus (Solheim,
1993; 1995; Viiri and von Weissenberg, 1995) and Ips cembrae (Redfern et al.,
1987), but it reaches almost 100% for I. sexdentatus and I. acuminatus (Lieutier et
al., 1989b; 1991c). The meaning of the percentage of beetles contaminated by a
given fungus species is thus questionable. If the fungus is needed to exhaust tree
defenses, why is the percentage of association not always 100%, and what is the
exact role of the fungus in stimulating the tree’s reactions if the percentage of
association varies? If we consider the strategy of exhausting tree defenses, the
answer may relate to variations in the ability of the fungus to stimulate the tree’s
reaction. For the same beetle species, the role of the fungus may also depend on
beetle population levels (see below VII.7.). In addition, the composition of the
fungus flora associated with a given beetle species varies considerably among
localities (Harding, 1989; Solheim, 1993), raising questions similar to those
presented for the percentage of contamination. Related questions refer to the
mechanisms involved in these variations.
There are several questionable aspects regarding the relations between the
thresholds of inoculum density and of attack density. It has been suggested above
(VI.3) that they are not related. An important question relates to the observation that
these two thresholds are frequently very close to each other, even when the
percentage of association between the fungus and the beetle is very low [see
Langström et al. (1992) compared with Solheim et al. (1993), Christiansen (1985b)
compared with Mullock and Christiansen (1986), Raffa and Berryman (1983a),
Lieutier (1995), Guérard et al. (2000) among others)]. In the later case, we would
expect a much higher value for the threshold of beetle attack density. A similar
value for the two thresholds thus means there is no fungal role in stimulation of tree
defenses during natural attacks. What are the implications of this? The answer could
greatly help in our understanding of the tree - bark beetle - fungus relationships. It
is not likely that the wound stimulation due to beetle boring compensates for the
lack of fungus. The number of spores carried by the beetle (lower than the number
in the artificial inoculations) may explain the lack of role of L. wingfieldii in
stimulating the tree’s defense reactions during T. piniperda attacks (Lieutier et al.,
1989a, 1995). In some situations, the threshold of inoculation density is even higher
than the threshold of attack density although the frequency of beetle infestation is
below 100% (Guérard et al., 2000), thus emphasizing the crucial role of the beetles
themselves.
The nature of the elicitor is also unknown. It has been proposed to originate
from the tree itself (Berryman, 1988; Lieutier, 1993) but that has never been
demonstrated.
7.3. TREE DEATH

A number of questions relate to this difficult problem: How is the tree killed? What
are the respective roles of and the interactions among sapwood invasion by the
fungus, release of fungal toxins, and decrease in water exchanges? What are the
roles of fungi other than the blue staining ones? When do the fungi invade the
sapwood? I proposed above that this invasion starts before the tree defenses are
completely exhausted and then extends freely without constraint, but it seems also to
occur after the water conductivity has decreased. However, the tree can recover and
survive after a dramatic decrease of water conductivity if the fungus has not
completely invaded the sapwood tissues (Guérard, Lieutier and Dreyer,
unpublished). What is the chronology of events in the sapwood (drying, decrease of
water conductivity, sapwood occlusion and fungus invasion)? What is the role of the
sapwood defense mechanisms themselves in sapwood occlusion and tree killing?
What is the role of the beetle and phloem invasion in the tree killing process?
Kinetic experiments are needed that following the various events in the sapwood, in
parallel to the development of the defense reactions and the success of beetle
establishment in the phloem. Such studies must be done in situations close to (just
below and above) the critical thresholds of attack / inoculation density, extending
from the beginning of beetle attack until tree death is complete.
64 F. LIEUTIER
7.4. EFFECTS ON THE AGGRESSORS

The effects of tree resistance mechanisms on the aggressors are very poorly
understood because most assays have been performed in vitro. The effects of
terpenes, at least monoterpenes, on both the fungi and the beetles have been
extensively investigated.. However, the role of the other secondary metabolites
involved in the tree’s defenses, particularly phenols, is not understood. The effects
of phenolic compounds on the blue stain fungi is a difficult problem, complicated by
the fact that in vitro results seem opposite to results obtained in presence of wood
(Hart and Shrimpton, 1979), but few Ophiostoma have been assayed in both
situations. Bioassays with insects are difficult to carry out because of problems
related to the stability of the compounds isolated from the tree reactions in presence
of oxygen. Nevertheless, research is needed in this field because of the important
qualitative and quantitative variations in these chemicals in relation to conifer
defense mechanisms against bark beetles and their associated fungi (Brignolas et al.,
1995a, 1998; Bois et Lieutier, 1997).
7.5. ENVIRONMENTAL FACTORS

It is well known that the ability of a tree to resist beetle attacks depends on its’
vigour and environmental conditions (Safranyik et al., 1975; Berryman, 1976;
Waring and Pitman, 1983; Raffa and Berryman, 1983a; Paine et al., 1984; Mullock
and Christiansen, 1986). How environmental factors influence the tree – fungus -
bark beetle relationships is very poorly understood, however. They can act on the
defense mechanisms themselves, on the fungi, or on the beetles. This very complex
and difficult topic has been approached only relatively recently in most situations.
Many studies of the effects of environmental factors, especially water stress and
nitrogen fertilization, on defense mechanisms have been conducted (as examples,
Paine and Stephen, 1987; Lorio, 1988; Paine et al., 1988; Dunn and Lorio, 1993;
Christiansen, 1992; Christiansen and Glosli, 1996; Croisé et al., 1998b, 2001; Kyto
et al., 1998; Viiri et al., 2001). Results are not presented here but they often lead to
conflicting conclusions and various theories have been proposed to explain the
observed effects (Lorio, 1986; Mattson and Haack, 1987; Lorio et al., 1990; Tuomi
et al., 1991; Herms and Mattson, 1992; Koricheva et al., 1998 among others).
Lombardero et al. (2001) suggested that these contradictions could be due to the fact
that environmental factors may act in different ways on constitutive versus induced
defenses.
7.6. TREE GENETIC FACTORS

Genetic factors have also been studied relatively recently on clones and provenances
with different resistance levels. Results not presented here, concerned preformed
resistance (Nebeker et al., 1992) as well as induced defense (Ferrell et al., 1993;
Ferrell and Otrosina, 1996; Brignolas et al., 1995b, 1998; Lieutier et al., 1996b;
Bois and Lieutier, 1997, 2000; Franceschi et al., 1998; Nagy et al., 2000, among
others). In some cases, predictors of tree resistance have been proposed (Brignolas
et al, 1995a, 1998; Lieutier et al., 1996c; Bois and Lieutier, 1997). However,
further research is needed in this field to yield practical applications (see below).
7.7. POPULATION ASPECTS

Beetle population levels clearly play a decisive role in beetle establishment in
relation to reaching the critical threshold of attack density (see references above).
However, other population aspects, more related to the “quality” of the population,
may also influence the tree – fungus - bark beetle relationships. For a given tree
vigour, does the threshold of attack / inoculation density depend on the beetle
population level? In other words, are outbreak populations intrinsically more
aggressive or does their high aggressiveness results only from their high number of
individuals? It has already been suggested that beetle pheromone production
(Schlyter and Birgersson, 1989) and beetle host selection behaviour (Raffa, 1991)
could vary with the population level. The percentage of beetles carrying fungus, and
the ability of the fungus to stimulate tree defenses, could also depend on population
levels. Since outbreak populations attack vigorous living trees, a high percentage of
beetles with fungal spores can be expected in this case, as well as a high ability of
the fungus to stimulate tree defenses, making the association more efficient in
exhausting tree defenses. In non-outbreak populations, the number of beetles is too
low to allow establishment on trees other than very weakened ones. Fungal
associates are thus not an absolute necessity for the beetles to colonize trees. In such
a case, the percentage of beetles vectoring fungi can be expected to stay at low
levels, and the ability of the fungus to stimulate tree defenses would also remain
low. In addition, fungus pathogenicity as well as fungus species composition could
vary with beetle population levels (Solheim, 1992; 1993), and thus also contribute to
increasing the aggressiveness of the beetle population. All these aspects, however,
still need to be investigated.
Studies on the genetic structure of the populations of beetles and fungi have
never been developed in relation to tree resistance mechanisms, although some have
considered the possible effect of the host on the population genetics of the beetles
(see references below in VIII.2). This could be, however, an important factor to
consider in the context of the adaptation of the aggressors to host resistance (see
below).
8. SOME POTENTIAL APPLICATIONS OF CONIFER RESISTANCE TO

BARK BEETLES
A general overview of the possibilities for utilizing tree resistance to insects in forest
pest management is presented in several other chapters of this book. As for other
insect species, there are numerous potential applications of conifer resistance to bark
beetles. I will focus on a few selected research topics only, those that I consider to
be the most likely to yield practical applications at large scales in the context of
forestry.
66 F. LIEUTIER
8.1. TREE SELECTION FOR RESISTANCE

This is the most classical application of research on tree resistance to insect attacks.
It results from the existence of a genetically controlled intra-specific variability of
the effectiveness of the mechanisms of resistance. In studies conducted on clones
and provenances, predictors of resistance to bark beetles have already been proposed
for Norway spruce and Scots pine (see references above and Heidger and Lieutier,
this volume). These predictors are related to the phenolic content of the phloem.
They can be present before the aggressions or neosynthesized in response to attacks
but, in all cases, they are correlated with the critical threshold of attack density and
the role of the hypersensitive reaction. Such predictors may be used as resistance
markers in genetic breeding programs taking into account resistance to bark beetles
in addition to other desirable characteristics of trees (Bastien, 1999; Heidger and
Lieutier, this volume). However, further research is needed before this can be a
practical and effective approach for use in such programs (Heidger and Lieutier, this
volume).
Selecting trees for resistance, however, involves a risk. Indeed, as mentioned by
Raffa (1991), increasing the resistance of all trees in a stand can create an intense
selective pressure for beetles able to overcome tree resistance, thus bearing the risk
of further dramatic epidemics. This risk is classical in all programs concerned with
genetic selection of plants for resistance to insects. Nevertheless, it might be less
important for bark beetles than for other forest insects, because of their particular
biology and because of the essential role of the hypersensitive reaction in conifer
resistance to bark beetles. For example, suppose that the genetic modifications
allowing a beetle to overcome tree resistance, and hence to become a “super-
aggressive” beetle, is an increase in its capacity to tolerate some tree secondary
metabolite synthesized in the hypersensitive reaction. This is very likely what has
the higher chance to occur since the hypersensitive reaction is the most common and
important mechanism of resistance in most conifers to most bark beetles species.
Two situations can be distinguished.
With typical endemic populations of beetles, only very weakened or dead trees
can be successfully colonized. Such trees do not exhibit any significant resistance
because no or very little hypersensitive reaction can occur. No pressure for selecting
super-aggressive individuals thus exists in endemic populations of bark beetles,
contrary to situations with other insects where host resistance is due to constitutive
compounds. During epidemic (outbreak) populations, because the percentage of
pre-existing super-aggressive beetles is naturally very low, mass aggregation on
living trees will necessarily involve both the super-aggressive beetles and the
“normal” beetles. All will cooperate in overcoming tree resistance and the normal
beetles will benefit from the presence of the super-aggressive beetles. The threshold
of attack density may be lowered but probably not very much. After the success of
the attacks, all beetle categories will be able to reproduce and, consequently, the
percentage of super-aggressive individuals will not change in the whole beetle
population. The super-aggressive individuals thus do not appear to be particularly
favoured during the epidemic populations either, plus outbreak periods generally last
for only a few beetle generations. For the proportion of super-aggressive beetles to
increase in the population, it is necessary topresume, that in addition to the genetic

modifications mentioned above, they respond to a more or less specific attraction
during aggregation, or that their intrinsic biotic potential has increased. This is, of
course, not impossible, but the chance for such phenomena to occur together is low.
8.2. ADAPTATION OF THE AGGRESSORS TO HOST RESISTANCE

This field of research is relatively new but it should develop rapidly in the near
future. One aspect results directly from selecting trees for resistance to bark beetles.
The risk of adaptation exists with bark beetles controlled by induced resistance
mechanisms, even if it is lower than with insects controlled by constitutive
resistance. Before using tree resistance in large tree genetic breeding programs, it is
thus important to understand the possible ways that bark beetles and their associated
fungi could adapt to induced resistance.
Another aspect is related to potential shifts by bark beetles and their associated
fungi to new host species. This can result from accidental introductions of beetles
and fungi to new areas or from voluntary introductions of exotic tree species for
extensive plantations. These man made situations are rather common nowadays.
The repeated accidental introductions and the establishment of T. piniperda from
Europe in North America (Mattson et al., 1994) illustrate the first situation, when
exotic beetles are accidentally introduced into a new region. The introductions of
Douglas-fir (Pseudotsuga menziesii) from North America and the Atlantic cedar
(Cedrus atlantica) from Morocco for plantations in Europe during the 20th century
are examples of the second, when exotic host trees are deliberately introduced into
new areas. Owing to its particular biology involving shoot feeding, T. piniperda has
no competitor in the North American pines. Similarly, in Europe, Douglas-fir and
cedar represent empty ecological niches and abundant and monospecific sources of
food for several bark beetle species. In any of these situations however, no
extensive damage due to bark beetles has been reported yet. The reasons for this are
unknown but the resistance mechanisms of the hosts are certainly involved.
Nevertheless, adaptation of the beetles and their associated fungi to the resistance of
their potential new hosts cannot be discarded in the more or less near future.
More generally, global change, by modifying climate parameters, will very likely
result in modifications of the geographic distributions of bark beetle species since
temperature is an important factor in their biology (Chararas, 1962). Species will
thus get in contact with new tree populations and new tree species, leading to the
situation described above on a wide scale.
Foresters urgently need information allowing them to evaluate the risk of
damage and the options available for forest protection. All the above considerations
thus emphasize the necessity for developing research on the factors that allow
beetles and fungi to adapt to tree resistance mechanisms. In this context, resistance
should even be enlarged to host attraction and deterrence. Such studies depend on
understanding the relationships between, on the one hand, the genetic structure of
the populations of beetles and fungi and, on the other hand, host quality in general,
that is host species, host populations, host physiological status, etc. Tentative steps
in that direction have already been undertaken several years ago while considering
68 F. LIEUTIER
different tree species attacked by the same beetle species, but without really
succeeding in separating the geographic effect from the effect of the host species on
the genetic structure of the beetle population (Bright and Stock, 1982; Sturgeon and
Mitton, 1982). This research is presently expanding rapidly with the development
of efficient molecular technics, especially for the beetles themselves (Sturgeon and
Mitton, 1986; Langor and Spence, J.R., 1991; Kelley et al., 1999, 2000), but these
programs should also consider the associated fungi.
8.3. EFFECT OF STRESS AND ENVIRONMENTAL FACTORS ON THE TREE

– AGGRESSORS’ RELATIONSHIPS
Effects of stresses and environmental factors on tree resistance mechanisms to bark
beetles and their associated fungi, as well as on the aggressors themselves, is a wide
and very important research topic to consider, especially in the present context of
pollution and climatic changes. Practical applications concern risk prediction, as
well as physiological improvement of trees by adapted silvicultural methods.
Several investigations have already been conducted, but no general results or
applications are available yet, mainly because of the complexity of the underlying
physiological problems and the variety of the models (see above VII.5). Significant
advancements in this field will be possible only through close cooperation among
entomologists, pathologists, and tree physiologists who should coordinate such
research. Regarding possible applications to silviculture, it has been underlined that
there is generally a high degree of compatibility between enhancing tree resistance
and forest management objectives, especially because of a positive relation between
tree growth rate and resistance levels (Raffa, 1991). However, positive correlations
between growth rate and resistance are not always true since some bark beetle
species, such as D. micans, seem to prefer healthy trees (Grégoire, 1988).
Moreover, some management tactics can favor bark beetle attacks, either directly or
indirectly. As an example, thinning favours the pine processionary caterpillar
Thaumetopoea pityocampa of pine (Géri, 1980), and their attacks weaken the trees,
making them more susceptible to bark beetles. Thus, forest management tactics and
the various forest pest problems must be considered as a whole system and not as
separate parts. This corresponds to the philosophy of integrated pest management.
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CHAPTER 3
MECHANISMS OF RESISTANCE IN TREES TO

DEFOLIATORS
KAREN M. CLANCY
USDA Forest Service Research and Development, Rocky Mountain Research

Station, Southwest Forest Science Complex, 2500 South Pine Knoll Drive
Flagstaff, AZ 86001-6381 USA
1. INTRODUCTION
Insects that feed on the foliage of trees (i.e., defoliators or folivores) include species
in the orders Lepidoptera, Hymenoptera, Coleoptera, Diptera, Orthoptera, and
Phasmida (Barbosa & Wagner, 1989). The most renowned forest defoliators are
species that are characterized by periodic population outbreaks, such as the gypsy
moth (Lymantria dispar) and tussock moths in the family Lymantriidae, spruce
budworms (Choristoneura species) in the family Tortricidae, and the pine butterfly
(Neophasia menapia) in the family Pieridae. All of these species are lepidopterans.
Some hymenopterans can also cause widespread defoliation of trees, such as the
pine sawflies (Neodiprion species) in the family Diprionidae. There are also species
of phasmids (i.e., walking sticks) that are occasionally important defoliators in
hardwood forests.
At least 10 mechanisms are known to be important in resistance of trees to insect
defoliators. Many of these mechanisms are not independent of one another, and it is
likely that linked suites of mechanisms interact in determining host plant resistance
to insect folivores.
1.1 PHENOLOGICAL ASYNCHRONY BETWEEN HOST TREES AND THEIR

INSECT HERBIVORES
This is often an important mechanism of resistance for species that are early-season
feeders on the expanding new buds and leaves of trees; early or late bud burst can
directly affect both the quantity and quality of suitable food available to herbivores
at specific times (Quiring, 1992; Lawrence et al., 1997). If emergence of larvae or
79
80 K. M. CLANCY
nymphs is too early in relation to budburst of host trees, the insects will be forced to
disperse to find suitable food resources. Increased dispersal invariably leads to
higher mortality from natural enemies or starvation. Alternatively, if insect
emergence is too late, folivores will be forced to feed on leaves or needles that are
too mature to be an optimal food source; this can result in slower larval growth
rates, smaller (and less fecund) adults, and increased larval mortality.
1.2 HOST TREE TOLERANCE OF DEFOLIATION

The ability to simply tolerate defoliation can also confer resistance to some insect
defoliators (sensu Painter’s [1958] definition). This mechanism is frequently
associated with inherently higher growth rates of the trees, or increased tree vigor
(but also see Price [1991]).
1.3 HOST TREE COMPENSATORY PHOTOSYNTHESIS AND GROWTH

Trees commonly respond to defoliation via compensatory growth, which involves
stimulation of photosynthesis, increased leaf nitrogen, and greater allocation of
carbohydrate reserves to growth of new foliage instead of roots (Clancy et al.,
1995). Increased rates of photosynthesis and growth in response to insect herbivory,
or compensatory photosynthesis and growth, can help promote tree recovery from
defoliators. Although most plants compensate for herbivory to some extent, the
degree of compensation varies widely (Trumble et al., 1993). Differences in
photosynthetic compensation among individual trees of the same species have not
been widely evaluated as a mechanism of tree resistance to insect herbivory (Chen et
al., 2001 a).
1.4 TOUGHNESS OF LEAVES AND NEEDLES

Tough leaves or needles can be an important deterrent to some insect folivores. For
example, ponderosa pine (Pinus ponderosa) trees with tougher needles were more
resistant to attack by Neodiprion fulviceps sawflies (Wagner & Zhang, 1993).
Needle toughness negatively influenced the feeding success of sawfly larvae
(Wagner & Zhang, 1993), and it may also have caused increased wear on the saw-
like ovipositor of the females as they inserted their eggs into mature needles (M. R.
Wagner, personal communication). Lawrence et al. (1997) concluded that needle
toughness was an important factor in defining the “phenological window of
susceptibility” for spruce budworm (Choristoneura fumiferana) feeding on white
spruce (Picea glauca); this example emphasizes the linkage between host plant
phenology and needle toughness.
MECHANISMS OF RESISTANCE IN TREES TO DEFOLIATORS 81
1.5 LOW NUTRITIVE QUALITY OF FOLIAGE

Plant tissues that do not provide a good match to the defoliator’s requirements for
protein, carbohydrates, or minerals can reduce growth rates of larvae and cause
lower rates of reproduction in the adults. Survival rates of all life stages, including
eggs, can also be reduced. However, Larsson (Chapter 1 of this volume) noted that
“Because there is so much variation that is seemingly of ontogenetic and
physiological origin primary metabolites are rarely considered to be part of plant
resistance, although this may be erroneous.” Hanover (1975) also observed that
“although resistance mechanisms involving host nutritional status may actually be
quite prevalent, they are most difficult to prove because the net effect is likely to be
more quantitative or subtle than that of the other resistance types.”
1.6 DEFENSIVE COMPOUNDS IN FOLIAGE

Larsson (Chapter 1 [section 3.2] of this volume) presented a good summary of the
role of secondary metabolites as resistance traits. Host plant defensive compounds
(or allelochemicals) that are always present in leaves or needles are known as
constitutive (or preformed) defenses. These constitutive defensive compounds in
foliage can function as digestibility reducers or toxins for insect defoliators, or they
may act as feeding or oviposition deterrents.
1.7 INDUCED DEFENSES IN HOST TREES

Induced resistance may also include host plant allelochemicals, but in this case
defensive chemicals are produced in response to defoliation, and they increase the
tree’s resistance to subsequent herbivory in the short- or long-term. Induced
resistance can also include changes in foliar nutrients, leaf toughness, or other
characteristics that increase the tree’s resistance to folivores. Larsson (Chapter
1[section 5] of this volume) discussed induced resistance, and noted that coniferous
trees seem to be less prone to induced defenses following defoliation by insects than
are deciduous trees. Toumi et al. (1988) suggested that the difference might be
explained by different carbon allocation strategies – deciduous trees have large
carbohydrate reserves in their roots, whereas coniferous trees store most of their
carbohydrates in the evergreen needles they retain for multiple years.
1.8 INDUCED SUSCEPTIBILITY IN HOST TREES

Some host trees become better sources of food for insect defoliators with successive
years of defoliation; changes can occur in concentrations or balances of foliar
nutrients or defensive compounds, or in other traits such as growth rates or
phenology of bud break. For example, McMillin & Wagner (1997) concluded that
ponderosa pine trees that were chronically defoliated by Neodiprion autumnalis
sawflies became better sources of food for the sawfly larvae via decreased ability of
82 K. M. CLANCY
the trees to produce carbon-based defensive chemicals and improved foliar nitrogen,
resulting in a positive feedback loop. On the other hand, trees that do not exhibit
this type of induced change in foliar chemistry etc. will be more resistant to damage
from defoliators over the long-run.
1.9 THREE-TROPHIC-LEVEL INTERACTIONS

A more complicated mechanism of resistance involves three-trophic-level
interactions among host trees, their insect folivores, and natural enemies of the
defoliators, an idea first proposed by Price et al. (1980). Larsson (Chapter 1
[sections 7 and 8] of this volume) covers this topic in more detail. The basic
concept is that characteristics of some host trees may increase susceptibility of the
insect defoliators to predators, parasites, or pathogens. On the other hand, insects
can also exploit host plant traits to help defend themselves against natural enemies,
so tri-trophic interactions can also end up benefiting the insect herbivores in some
cases.
1.10 HOST TREE MICROBIAL MUTUALISTS

Finally, another complex mechanism of resistance may include host tree microbial
mutualists such as mycorrhizae or fungal endophytes (see Saikkonen & Neuvonen
[1993] for an overview). Ectomycorrhizal fungi improve a tree’s ability to obtain
water and nutrients such as nitrogen and phosphorus from the soil, in exchange for
simple sugars they extract from the trees’ feeder roots for nourishment (Molina et
al., 1993; Mathiasen & Albion, 2001). Gehring & Whitham (1991) demonstrated
that high levels of insect herbivory could reduce the ability of pinyon pine (Pinus
edulis) trees to support ectomycorrhizal symbioants. It is possible that
ectomycorrhizal mutualists can also influence the resistance of host trees to insect
defoliators via effects on the tree’s growth rates or foliar biochemistry. In other
words, perhaps trees that are inherently better hosts for ectomycorrhizae are more
resistant to insect defoliators because of the benefits the trees gain from this
symbiosis. The fungal endophytes that are ubiquitously present in leaves and
needles may also enhance host tree resistance to insect folivores through the action
of deterrent or toxic compounds they produce (Saikkonen et al., 1998).
2. MECHANISMS OF RESISTANCE OF DOUGLAS-FIR TREES TO THE

WESTERN SPRUCE BUDWORM
My collaborators and I have investigated the potential role of most of these
mechanisms using the western spruce budworm (Choristoneura occidentalis) and
Douglas-fir (Pseudotsuga menziesii var. glauca) as a model system. We choose to
study this insect-plant system in detail because the budworm is the most important
forest defoliator in western North America (Brookes et al., 1987), and Douglas-fir is
a commercially important host tree species (Silen 1978; Hermann & Lavender,
1990; Hardin et al., 2001).
The remainder of this chapter summarizes what we know about mechanisms of
resistance of Douglas-fir to damage from the western spruce budworm. I have not
investigated the role of three-trophic-level interactions in this system, so I will not
present any information on this potentially very important mechanism.
The various mechanisms of resistance reported below were evaluated using a
combination of laboratory and greenhouse experiments, plus field observations on
40 pairs of mature Douglas-fir trees that are phenotypically resistant versus
susceptible to damage from the budworm (Clancy, 2001). Three-generation
laboratory diet bioassays (Clancy, 1991b) were used to quantify the budworm’s
nutritional niche with regard to levels of nitrogen (Clancy, 1992a), sugars (Clancy,
1992b), minerals (Clancy & King, 1993; unpublished data), and monoterpenes
(Clancy et al., 1992; Clancy, 1993; unpublished data) that occur in Douglas-fir
foliage. The budworm’s response curves from the diet bioassays were compared to
levels of the nutrients and terpenes in current-year foliage from pairs of Douglas-fir
trees that appeared to be “resistant” versus “susceptible” to western spruce budworm
defoliation. Twelve pairs of trees on the Pike National Forest (NF) in Colorado
were sampled in 1988, 1989, and 1990; the trees were 45-123 years old when annual
growth rings were counted on increment cores collected in 1990 (Clancy, 199la;
Clancy et al., 1993). Another 12 pairs of trees on the Kaibab NF in Arizona were
sampled in 1989 and 1990; the trees were 67-115 years old in 1990 (Clancy et al.,
1993). Sixteen pairs of trees on the San Isabel NF in Colorado were sampled in
1995 and 1996; the trees were 37-118 years old in 1995 (Clancy, 2001). Most of the
trees from the Pike and Kaibab NF sites were successfully cloned (by whip grafting)
in 1991 and 1992. Clones from 12 pairs of trees from these two sites were used in
greenhouse experiments in 1998 and 1999 (Chen, 2001). Chen et al. (2001a) also
grew half-sib seedling progeny from 13 of the 40 pairs of trees to use in greenhouse
studies. Finally, Chen et al. (2001b) established that there are genetically-based
differences between the resistant and susceptible parent trees, suggesting that the
phenotypic differences observed in resistance of these interior Douglas-firs to
budworm defoliation are at least partly caused by genetic differences among trees.
2.1 PHENOLOGICAL ASYNCHRONY BETWEEN DOUGLAS-FIRS AND THE

WESTERN SPRUCE BUDWORM
Variation in bud phenology is particularly important for early-season feeders like the
western spruce budworm. Budworm larvae can damage all types and developmental
stages of tissues (Frank & Jenkins, 1986), but they prefer to feed on nutrient-rich
tissues such as swollen buds, current-year needles, and pollen (Shepherd, 1992;
Dodds et al., 1996). Budworm larvae can also feed on less nutritious older needles
as a survival strategy until swollen buds and new needles are available (Shepherd,
1992).
84 K. M. CLANCY
Several lines of evidence suggest that differences in bud break phenology are an
important mechanism of resistance in Douglas-fir trees. First, field observations of
bud break phenology of paired resistant and susceptible trees clearly showed that the
resistant trees consistently had later budburst phenology than the susceptible trees (
Table 1) (Clancy et al., 1993).
Second, current-year buds on the susceptible clones flushed earlier than those on
the resistant clones, when the trees were grown in a common environment in
greenhouses (Chen et al., 2001a). These results support a genetic basis for the
differences I observed in bud break phenology in the field. Phenology of bud break
is known to be a highly heritable trait in Douglas-fir (Silen, 1978).
Third, Chen (2001) reared western spruce budworm larvae on resistant and
susceptible clones in greenhouse bioassay experiments to establish how host tree
phenotype affected budworm survival and reproduction. Two different bioassays
were used to assess the importance of bud burst phenology as a factor determining
host plant resistance. In the 1988 experiment, budworm feeding was matched to the
bud flush of each individual plant. Larvae reared on the resistant clones had 1.7
times greater realized fitness (i.e., number of larvae produced) compared to those
reared on the susceptible clones (Fig. 1). In the 1999 experiment, budworm feeding
was matched to bud flush of the whole population of plants. The susceptible clones
had an earlier budburst phenology compared to the resistant clones, which mimicked
the pattern observed for the parent trees in the field. In this case, budworm larvae
reared on the susceptible clones had 1.4 times higher realized fitness than budworms
reared on the resistant clones (Fig. 1). Chen (2001) concluded that western spruce
budworm survival and reproduction is indeed better on susceptible phenotypes of
Douglas-fir under conditions similar to those that the insects and trees experience in
the field. Moreover, the results confirmed that variation among trees in budburst
phenology is an important mechanism of resistance influencing interactions between
the budworm and its Douglas-fir host trees.
86 K. M. CLANCY
Fourth, Chen et al. (2001a) also discovered in the 1998 greenhouse bioassay
experiment that when larvae were placed on each grafted tree when buds were
highly suitable for feeding, the resistant clones were defoliated more than the
susceptible clones However, in the 1999 experiment, when larvae were
placed on all trees on the same date regardless of bud burst stage, resistant clones
were defoliated less than susceptible clones Thus, budworm defoliation
of clones depended on the degree of synchrony between bud burst phenology and
budworm larval feeding.
2.2 DOUGLAS-FIR TOLERANCE OF BUDWORM DEFOLIATION, AND THE

ROLE OF HOST TREE VIGOR
Trees that have inherently greater growth rates may be able to tolerate the loss of
needles (i.e., photosynthetic capacity) to budworm defoliation without experiencing
as much physiological stress as more slowly growing trees do (Chen et al. 2001a).
In general, the evidence indicates that mature Douglas-fir trees that are resistant to
budworm damage tend to have greater growth rates than susceptible trees do.
Furthermore, open pollinated seedlings from resistant trees also have higher growth
rates than seedlings from susceptible trees, implying there is a genetic basis for the
difference.
I evaluated this mechanism for mature trees in the field by comparing radial
growth rates of the 40 paired resistant and susceptible trees. Five-year radial growth
increments were measured on increment cores collected from the trees.
The resistant trees at the Pike and Kaibab National Forest sites appeared to be
more vigorous than the susceptible trees – they had sustained less impact on their
radial growth from budworm defoliation compared to the susceptible trees (P <
0.001; Table 2) (Clancy et al., 1993). This implies that resistant trees may be more
tolerant of defoliation because they can compensate better for photosynthetic area
lost from herbivory. Overall, the resistant trees at the Pike and Kaibab sites had
1.48 times greater radial growth than the susceptible trees did from 1966-1990.
However, this pattern was not consistent across all three sites. There were no
detectable differences in radial growth increments between the resistant and
susceptible trees at the San Isabel National Forest site from 1970-1994 (
Table 2).
Chen et al. (2001a) grew half-sib seedlings from open-pollinated seeds collected
from 13 of the 40 pairs of resistant and susceptible mature trees (i.e., 26 families).
In the absence of budworm defoliation, height and base diameter of half-sib
seedlings from resistant trees were significantly greater compared with seedlings
from susceptible trees in all 3 years of growth in a greenhouse (P < 0.001); total
biomass of the resistant seedlings was also greater in years 2 and 3 (P < 0.001)
(Chen et al., 2001a). The authors concluded that resistant trees were genetically
88 K. M. CLANCY
predisposed to grow faster than susceptible trees, and suggested that inherently
higher growth rate may promote tree resistance or recovery from budworm
defoliation by rapid regrowth.
2.3 DOUGLAS-FIR COMPENSATORY PHOTOSYNTHESIS AND GROWTH

IN RESPONSE TO BUDWORM DEFOLIATION
Chen et al. (2001a) hypothesized that clones of resistant Douglas-firs would respond
to budworm defoliation with a greater increase in net photosynthetic rate than clones
of susceptible trees, but they concluded that this hypothesis was not supported in
greenhouse bioassay experiments. There was evidence of a stronger compensatory
photosynthetic response to defoliation in resistant compared to susceptible clones
after 1 year of defoliation in the 1998 bioassay, when the resistant clones were
defoliated more than the susceptible clones (see Fig. 1 for details regarding the
bioassays). However, in the 1999 bioassay, the susceptible clones were defoliated
more, resulting in similar cumulative defoliation of the resistant and susceptible
clones over 2 years, and similar responses in terms of compensatory photosynthesis
in the 1999 bioassay measurements. Chen et al. (2001a) noted, “Because late bud
burst phenology apparently enabled resistant trees to avoid heavy budworm
defoliation, there is probably little selection for mechanisms leading to
compensatory photosynthesis in resistant genotypes”.
2.4 TOUGHNESS OF DOUGLAS-FIR NEEDLES

It appears unlikely that Douglas-fir needle toughness is a mechanism of resistance to
the western spruce budworm. Both field observations on mature trees and
greenhouse measurements on vegetatively propagated clones failed to produce any
evidence that needle toughness was associated with resistance to budworm
herbivory (Table 3).
Burr & Clancy (1993) assessed the possibility that one or more anatomical
characteristics of Douglas-fir needles might affect susceptibility to herbivory by the
budworm. They compared 23 anatomical characteristics of current-year needles
collected from five of the pairs of phenotypically resistant and susceptible trees at
the Pike National Forest site. They discovered that needles from resistant trees
actually had thinner epidermal layers than needles from susceptible trees (P = 0.038;
Table 3). However, they noted that the differences they observed in thickness of the
epidermal layer of needles between the putatively resistant and susceptible trees
were “probably the result of dissimilar defoliation histories”. Burr & Clancy (1993)
suggested that anatomical characteristics of needles might emerge as a mechanism
of resistance if vegetatively propagated scions from the resistant and susceptible
trees were grown without dissimilar defoliation histories.
Chen, Kolb, & Clancy (unpublished data) subsequently evaluated the toughness
of current-year needles collected from 12 pairs of cloned Douglas-fir plants derived
from resistant and susceptible mature trees (Table 3). Foliage toughness did not
differ between the resistant versus susceptible clones
2.5 LOW NUTRITIVE QUALITY OF DOUGLAS-FIR FOLIAGE

There is abundant evidence indicating that low nutritive quality of foliage may be an
important mechanism of resistance in Douglas-firs against the western spruce
90 K. M. CLANCY
budworm (Clancy, 1991a, 1992a, 1992b, 2001; Clancy & King, 1993; Clancy et al.,
1993). This is somewhat surprising given the tremendous variation in foliar
concentrations of primary metabolites (i.e., nitrogen, carbohydrates, and minerals) in
trees that is associated with the age of the tree and the leaves or needles, the
genotype of the tree, and the environment the tree is growing in (Clancy et al.,
1995).
Nitrogen (N), or protein, is considered to be the most important nutrient for
insect growth and survival (Mattson, 1980; Mattson & Scriber, 1987). However, the
importance of N as a key nutrient is probably not strictly cause and effect, but is
related to the strong link between N and many other important nutritional factors in
plants (Clancy et al., 1995). The western spruce budworm’s response to increased
N in artificial diets was neither positively linear nor convex, and it was dependent on
levels of minerals in the diets (Clancy, 1992a). Host plant N appears to determine
the amount of food the budworm ingests, which in turn affects the amounts of other
nutrients consumed; this implies that a proper balance of many different nutrients is
probably the most important factor in the nutritional ecology of the budworm
(Clancy, 1992a). Indeed, Clancy (2001) reported that the resistant Douglas-fir trees
from three different sites consistently had higher levels of foliar N compared to the
susceptible trees (P < 0.001; Fig. 2). This result lends further support to the
importance of a proper balance of N, minerals, carbohydrates, etc. in determining
the quality of foliage as a source of food for budworm larvae. Clearly, higher levels
of foliar N do not invariably promote improved budworm survival and reproduction.
92 K. M. CLANCY
Likewise, Douglas-fir trees resistant to budworm defoliation had higher levels of

sugars in their foliage than susceptible trees at all three sites (Clancy, 2001). This is
in agreement with results from artificial diet bioassays; budworm fitness was best on
artificial diets with sugar (i.e., sucrose) concentrations of 6% dry weight, which is
near the lower limit observed for Douglas-fir foliage (Clancy, 1992b) (Fig. 3).
The budworm’s response curve to different levels of sugar in artificial diets can
be used to estimate how budworm populations would grow over three generations if
they were feeding on trees that had the average concentration of foliar sugars that
occurs in susceptible (10.20 %) versus resistant (11.53%) Douglas-firs (Fig. 3). I
simply extended the susceptible and resistant points indicated on the x- (% Sucrose)
axis up to the response curve for the appropriate generation (see the y-axis) and
projected that point over to the z-axis (No. larvae [log scale]) to estimate the number
of first instars alive at the beginning of the and generations. Then, I
plotted the projected population growth data to illustrate the comparison for resistant
versus susceptible trees. This exercise indicated that budworms feeding on
susceptible trees with 10.2% sugars would have 1.4 times greater population growth
than budworms feeding on resistant trees with 11.5% sugars (Fig. 4). The
differences I have observed between resistant and susceptible trees in concentrations
of foliar sugars could have real biological significance in affecting population
dynamics of the western spruce budworm.
94 K. M. CLANCY
Resistant Douglas-fir trees at all three sites also had lower mineral/N ratios in
their current-year foliage than susceptible trees for phosphorus (P)/N magnesium
(Mg)/N, potassium (K)/N, and zinc (Zn)/N (Clancy, 2001). I repeated the exercise
described above for sugars using the response curves for ratios of K/N and Mg/N
(unpublished data). It was obvious that differences between resistant versus
susceptible trees in K/N and Mg/N ratios could also affect budworm population
dynamics (Figs. 5 and 6). Budworms feeding on susceptible trees with average K/N
ratios of 0.768 were projected to have 2.1 times greater population growth compared
to budworms feeding on resistant trees with average K/N ratios of 0.642 (Fig. 5).
The predicted effects of variation in Mg/N ratios were even more dramatic.
Budworm populations were estimated to increase 8.2 times more when feeding on
susceptible trees with average Mg/N ratios of 0.0780 than when feeding on resistant
trees with average Mg/N ratios of 0.0661 (Fig. 6).
2.6 DEFENSIVE COMPOUNDS (MONOTERPENES) IN DOUGLAS-FIR

FOLIAGE
Evidence that foliar monoterpenes function as a mechanism of resistance in
Douglas-fir to the western spruce budworm is mixed, and thus, controversial (Chen,
2001). Certain monoterpenes (e.g., tricyclene, camphene, and bornyl acetate) have
been reported to have adverse effects on budworm performance (Cates et al., 1983;
Redak & Cates, 1984; Cates & Zou, 1990; Zou & Cates, 1995). However, the
studies that my collaborators and I have conducted do not support an important role
for monoterpenes as defensive compounds against the budworm.
Clancy et al. (1992) evaluated the effects of terpene compounds on budworm
survival and reproduction by forming gelatin-walled microcapsules around eight
terpenes that are common constituents of Douglas-fir oleoresin. The
microencapsulated terpenes were mixed into artificial diets to determine the effects
they had on budworm fitness, using the three generation bioassay technique
developed by Clancy (1991b). Five monoterpenes tested (
camphene, myrcene, and limonene) had little or no detectable effect on budworm
fitness, when they were tested at concentrations found in Douglas-fir foliage
(Clancy et al., 1992; Clancy, 1993; unpublished data). One oxygenated
monoterpene, bornyl acetate, had negative effects on budworm fitness at higher
concentrations, implying it may function as a defensive chemical (Clancy, 1993).
The other two oxygenated monoterpenes assessed (linalool and ) had no
detectable effects on budworm fitness at concentrations that occur in host foliage
(Clancy, 1993).
Furthermore, there were no detectable differences in foliar concentrations of
total ( Fig. 7) or individual terpenes between Douglas-fir trees
that were resistant versus susceptible to budworm defoliation at any of the three sites
(Clancy, 1991a; Clancy et al., 1993; Clancy, 2001). Chen (2001) also failed to find
consistent differences in foliar terpenes between resistant and susceptible clones in
greenhouse studies. In the 1998 greenhouse bioassay, there were significant
differences between the resistant versus susceptible clones. However, the
susceptible clones had higher concentrations of monoterpenes in their foliage, which
is opposite to what one would expect if terpenes were important in determining
96 K. M. CLANCY
resistance to budworm defoliation in the field. There were no differences between

the resistant and susceptible clones in the concentration or composition of
monoterpenes in the 1999 experiment. Collectively, these results suggest that
budworm population growth is probably largely unaffected by foliar terpenes.
98 K. M. CLANCY
2.7 INDUCED DEFENSES IN DOUGLAS-FIR FOLIAGE

Chen (2001) addressed the question of whether induced changes in foliar
monoterpenes are likely to be involved in resistance of Douglas-fir to the western
spruce budworm in the greenhouse bioassays he conducted with resistant and
susceptible clones. Two years of defoliation by budworm larvae had similar effects
on monoterpene concentrations of clones from resistant and susceptible trees. This
result does not support induction of monoterpenes as a mechanism of resistance.
2.8 INDUCED SUSCEPTIBILITY IN DOUGLAS-FIR FOLIAGE

Clancy et al. (1993) speculated that the biochemical differences they observed
between putatively resistant and susceptible Douglas-fir trees at the Pike and Kaibab
National Forest sites could be the result of different budworm defoliation histories.
If this is the case, it suggests that budworm defoliation could have a positive
feedback for subsequent generations, as in the “resource regulation hypothesis”
proposed by Craig et al. (1986). The authors conjectured that “Perhaps the foliar
chemistry of susceptible trees is more prone to change in response to defoliation,
whereas the resistant trees are less prone to induced changes in chemistry from
defoliation. Consequently, susceptible trees may become a better source of food for
the larvae with consecutive years of damage, but resistant trees do not become
progressively better hosts for the insects. This could explain why budworm
outbreaks have persisted for many years in some locations (Brookes et al., 1987).”
In addition to addressing the question of induced resistance described in the
previous section, Chen (2001) also tackled the issue of induced susceptibility in the
greenhouse bioassays he conducted with resistant and susceptible clones. Induced
susceptibility could be implicated as a mechanism of resistance if the budworm
defoliation treatments had divergent effects on foliar nutrients. (The evidence
summarized in the previous two sections leads me to dismiss a potential role for
changes in monoterpenes being involved in this mechanism.) The susceptible
clones would have to become a better match to the budworm’s nutritional
requirements subsequent to being defoliated by budworm larvae, whereas foliar
nutrients in the resistant clones should either not change, or change in a direction
that made them a poorer match. The statistical analysis of the foliar nutrient data
from Chen’s experiments is currently underway, so I cannot yet provide a
conclusive answer to this intriguing question.
2.9 DOUGLAS-FIR MICROBIAL MUTUALISTS

I do not have any evidence to support a role for microbial mutualists in determining
resistance of Douglas-firs to defoliation by the western spruce budworm. However,
only preliminary investigations have been conducted to date.
Stanley Faeth (Professor at Arizona State University, Tempe) and I collaborated
on a pilot study (1996-1997) to examine fungal endophytes in current- year needles
100 K. M. CLANCY
from the 12 pairs of resistant and susceptible trees at the Kaibab National Forest site.
There were no obvious differences in the fungal endophyte fauna of the resistant
versus susceptible trees, so we did not pursue this any further (S.H. Faeth & K.M.
Clancy, unpublished data).
On the other hand, we know that budworm defoliation can influence the ability
of Douglas-firs to support ectomycorrhizal mutualists. Kolb et al. (1999) reported
that Douglas-fir seedlings that were severely defoliated by western spruce budworm
larvae in greenhouse experiments had less ectomycorrhizal colonization than
moderately defoliated or non-defoliated trees.
Barbara Palermo (M.Sc. student at Northern Arizona University, Flagstaff)
recently completed a greenhouse experiment designed to examine the potential role
of ectomycorrhizae as Douglas-fir murualists that influence resistance to the western
spruce budworm. The data are currently being analyzed, so the results are still
pending.
Palermo used half-sib seedlings grown from open-pollinated seeds collected
from 11 of the 40 pairs of resistant and susceptible Douglas-fir trees (i.e., 22
families) to determine if there are tri-trophic interactions among Douglas-firs, their
ectomycorrhizal symbioants, and the western spruce budworm. Experimental
treatments included controls, ectomycorrhizal inoculation, or fertilization (with N, P,
Mg, and Zn) of resistant and susceptible seedlings. Budworm larval feeding
preferences and foliar levels of N, P, Mg, and Zn were measured.
Palermo hypothesized that mycorrhizal infection could increase the foliar
concentration of key mineral elements (N, P, Mg, and Zn) beyond the optimal levels
for the budworm and thus make the trees less suitable (and less preferred) hosts for
budworm larvae. The scenario Palermo envisioned is that the genetics of the host
tree (resistant versus susceptible to budworm defoliation) influence the rate of
ectomycorrhizal colonization of the roots, which in turn helps determine levels of
key minerals in the foliage. This results in less budworm herbivory on resistant
trees owing to their inherently greater capacity to support ectomycorrhizal
mutualists. This would be a very interesting discovery indeed!
3. SUMMARY
At least 10 mechanisms are known to be important in resistance of trees to insect
defoliators: 1) Phonological asynchrony between host trees and insect herbivores; 2)
Host tree tolerance of defoliation, which is linked to host tree vigor; 3) Host tree
compensatory photosynthesis and growth in response to defoliation; 4) Toughness
of leaves and needles; 5) Low nutritive quality of foliage; 6) Defensive compounds
(or allelochemicals) in foliage; 7) Induced defenses in host trees; 8) Induced
susceptibility in host trees; 9) Three-trophic-level interactions among the trees, their
insect herbivores, and natural enemies of the herbivores (i.e., predators, parasites,
pathogens); and 10) Host tree microbial mutualists such as mycorrhizae and fungal
endophytes.
The western spruce budworm and Douglas-fir were used as a model system to
investigate nine of these mechanisms. The research employed a combination of
laboratory diet bioassays, field observations of mature Douglas-fir trees that were
phenotypically resistant versus susceptible to budworm defoliation, and greenhouse
bioassays with grafted clones and half-sib seedling progeny derived from the
resistant and susceptible trees. The complicated mechanism of three-trophic-level
interactions among Douglas-firs, the budworm, and the budworm’s natural enemies
has not been explored.
Three mechanisms appear to be important determinants of Douglas-fir resistance
to the budworm: phenological asynchrony, tolerance and vigor (i.e. growth rates),
and low nutritive quality of foliage. On the other hand, the following four
mechanisms were excluded: compensatory photosynthesis, toughness of needles,
defensive compounds (i.e. monoterpenes) in foliage, and induced defenses (i.e.,
induction of foliar monoterpenes). The remaining two mechanisms, induced
susceptibility and microbial mutualists, are currently under evaluation. Microbial
mutualists may or may not be important; results from a pilot study suggested fungal
endophytes are not likely to be involved in resistance. However, the jury is still out
in regard to the potential influence of ectomycorrhizae in shaping resistance to
budworm defoliation.
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CHAPTER 4
MECHANISMS OF RESISTANCE IN CONIFERS

AGAINST SHOOT INFESTING INSECTS
The case of the white pine weevil Pissodes strobi (Peck)
(Coleoptera: Curculionidae)
René I. Alfaro 1 , John H. Borden2, John N. King3, Elizabeth S. Tomlin4, Rory L. McIntosh5,
Jörg Bohlmann6
1. INTRODUCTION
A variety of insects feed on conifer shoots. These include: defoliators, bark, wood
and cone borers, girdlers, gall makers and sucking insects, primarily in the orders
Lepidoptera, Coleoptera, Hemiptera, Homoptera and Diptera. However, these
insects usually do not have an exclusive feeding niche. Some also feed on buds,
foliage, stem and cones. For example, larvae of the pine shoot moth, Rhyacionia
buoliana Schiff., feed on shoots and cones, in addition to mining inside the newly
expanding shoots. Adults of the lodgepole terminal weevil, Pissodes terminalis
Hopping, and the white pine weevil, Pissodes strobi Peck, feed on the one-year old
or older bark of stem and branches, but the larvae feed exclusively on inner bark of
the uppermost tree internodes. As young larvae, spruce budworms, Choristoneura
spp., are bud miners, but move to feed on cones and expanding new shoots and
foliage as they mature.
An important group of shoot infesting insects includes the weevils (Coleoptera:
Curculionidae), with the most important genera being Pissodes, Cylindrocopturus
and Magdalis. Among these, the white pine weevil is the most important pest of
spruce (Picea spp.) and pines (Pinus spp.), in North America (Alfaro 1994; Lavallée
and Benoit 1989), and is used in this review as an example to describe defences in
conifers to shoot insects. In early spring (late March, April), adults of this weevil
emerge from overwintering in the duff, and after mating, females oviposit in the
upper section of the previous year's leader. The larvae mine downwards, consuming
the phloem, girdling and killing the leader. Pupation occurs in chambers excavated
in the xylem. Adults emerge from the leaders from late July to September, and
105
106 R. ALFARO et al.
when temperatures drop and photoperiod shortens, they go into hibernation in the
duff (Silver 1968). Damage from this insect has forced forest managers to eliminate
planting of Sitka spruce, Picea sitchensis (Bong.) Carr., in much of the North West
Coast of North America (Hall 1994). This insect is now also a threat to white
spruce, Picea glauca (Moench) Voss, plantations and with predicted climate change,
could expand its range northward above the Arctic Circle (Sieben et al. 1997).
Work on genetic resistance to this insect has been pursued in British Columbia
(BC), Canada, for the last 30 years, especially at the Pacific Forestry Centre of the
Canadian Forest Service, Simon Fraser University, the BC Ministry of Forests, and
the University of British Columbia (Alfaro 1996a; Ying 1991;Ying and Ebata 1994).
In the last 10 years the BC Ministry of Forests and the Canadian Forest Service
initiated a large program to screen Sitka and white spruce for resistance to the white
pine weevil. Earlier genetic resistance work was completed in eastern USA, which
provided strong evidence for resistance to this weevil on Eastern white pine, Pinus
strobus L. (Callaham 1960; Connola 1966; Plank and Gerhold 1965). The
resistance-screening program against the white pine weevil in British Columbia is
described in the WWW page:
http://www.pfc.forestry.ca/entomology/weevil/resistance/resistance_e.html
RESISTANCE IN CONIFERS TO SHOOT INFESTING INSECTS 107
This program consisted of the systematic screening for resistance of over 29,000
individual Sitka and white spruce trees in large, family progeny trials established in
replicated sites. Final ranking for resistance was assigned based on field attack rates
and laboratory studies. The search for resistant Sitka spruce, which included
families collected from Alaska to California, has yielded, so far, only three sources
of resistance: Big Qualicum, Haney and the Nass River area (a zone of hybridization
between Sitka and white spruce) (Figure 1). Studies in white spruce (also known in
BC as interior spruce because of potential hybridisation with Engelmann spruce, P.
engelmannii Parry ex Engelm.) have indicated that resistance occurs in the Quesnel
Lakes area. Resistance gene pools seem to originate in areas at the edges of spruce
distribution, suggesting that resistance is rare and that further efforts to find useful
genotypes should concentrate in these areas.
This intensive search for spruce with resistance to the white pine weevil gave us
the opportunity to conduct research into the mechanisms used by spruces to defend
against shoot insects. We found that most defences to this shoot insect also occur in
other parts of the tree and are non-specific, i.e. they protect the shoot against a
variety of attacking organisms.
1.1 HOST-INSECT INTERACTIONS

Conifers use several mechanisms to defend against stem-invading insects (Berryman
1972, 1988; Feeny 1976; Cates and Alexander 1982; Lieutier and Berryman 1988;
Mattson et al. 1988; Reid and Watson 1966; Shrimpton 1978). These often occur
simultaneously, but the relative importance of each component to successful host
defence differs with both host and insect species (Matson and Hain 1985) (Figure 2).
Plant defences have been classified according to their permanence in time, into
constitutive and induced defences (Berryman 1972,1988; Feeny 1976; Rhoades and
Cates 1976, Lunderstadt 1999). Constitutive defences are permanent structural or
chemical defence systems that occur regardless of the presence of the attacker.
Examples of constitutive defence structures include plant trichomes, thorns, latex
and resin canals and an array of chemicals, including resin constituents.
Inducible defences are activated in response to attack. Examples of inducible

defences are the mobilisation of defensive chemicals to the site of wounding, and the
production of traumatic resin in conifers in response to insect or fungal attack
(Berryman 1988; Raffa 1991; Reid et al. 1967; Reid and Shrimpton 1970;
Shrimpton 1978). Guild defences are population strategies used by plants to avoid
or confuse herbivores, for example, by virtue of being rare, occurring in mixtures
with other species or lacking visual or chemical apparency (Feeny 1976). Another
common defensive strategy in plants is preventing damage, for example, by being in
the wrong phenological stage at the time of feeding. Plants and insects also evolved
forms of multitrophic defence systems in which herbivores induce emission of
volatiles from the plant that serve as chemical attractants for predators or parasitoids
of the herbivore. Herbivores and plants have co-evolved over the millennia and
herbivorous insects have developed many adaptations to mitigate the effects of plant
defences on them (Panda and Kush 1995, Alfaro et al. 1999).
2. STUDY OF RESISTANCE MECHANISMS: METHODS

The methods used to study resistance of conifers to insects depend on whether the
objective is mass screening for accelerated breeding programs or the identification
of specific resistance mechanisms. In the case of the white pine weevil, we used
field-testing to mass screen the spruce genetic resources of BC, and we (and others)
also developed specific tests for particular resistance mechanisms, as indicated
below.
Field observations of visitation or attack rates on susceptible and resistant trees,
and correlations with tree phenology (Hulme 1995; McIntosh 1997; Alfaro et
al. 2000b)
Laboratory behavioral studies employing choice and no-choice experiments

(VanderSar 1978; VanderSar and Borden 1977a,b; Alfaro et al. 1979, 1980;
Tomlin and Borden 1996)
Dissections and life table observations and study of mortality factors (Silver
1968, Therrien 1995).
Specific studies to compare structural constitutive defences in resistant and
susceptible trees, e.g. measurement of bark thickness, density of bark resin
canals, number of sclereid cells (Stroh and Gerhold 1965, Tomlin and Borden
1994a, Alfaro et al. 1997; Grau et al. 2001; O’Neill et al. 2001).
Studies to quantitatively and qualitatively measure inducible defences at the
molecular genetic, biochemical and chemical level in species and genotypes of
spruce, including:
wound responses of naturally infested or artificially wounded shoots,
histology of wounded leaders and measurement of the strength of
traumatic resinosis (Alfaro 1995; Alfaro et al. 1996a; Tomlin et al.
1998; O’Neill et al. 2001);
kinetics of traumatic resin production by detecting the expression of
terpene synthase enzymes and genes (Martin et al. 2001; Bohlmann
unpubl. results; A. Plant, Simon Fraser U., Burnaby, BC, Canada,
unpubl. obs.); and
chemistry of constitutive and traumatic resin (Martin et al. 2001;
Tomlin et al. 2000; Nault and Alfaro 2001)
2.1 FIELD-TESTING FOR RESISTANCE

This method involves the planting of candidate genotypes in replicated trials.
Genotypes are discriminated as resistant or susceptible by exposure to natural
(Alfaro and Ying 1990; Kiss and Yanchuk 1991) or artificial (King and Alfaro
2001) infestations. Releasing weevils in plantations to create artificial infestations is
recommended, because screening is faster and more reliable than depending on
natural infestations. Artificial infestations are initiated once spruce trees reach
attackable height (1-2 meters in height in coastal BC). Results are obtained within
one or two years after infestation. This method is cheap and effective; however, it
provides only a general ranking of the resistance level, with only limited information
on the mechanisms involved.
One type of information that we found useful in understanding resistance
mechanisms to shoot insects was measuring the rate of Attack Failure among
various genotypes. Failed attacks are those cases in which the insect has laid eggs
that failed to develop into viable larval populations due to drowning of the eggs and
young larvae in toxic resin. Although the shoot survives a failed attack, egg niches
and scars due to mining by the larvae are visible.
A wide range of resistance to the white pine weevil was revealed by studying
rates of oviposition by P. strobi among Sitka spruce clones and ramets from nine
provenances tested at Fair Harbour, BC (Ying 1991) (Figure 3). In the susceptible
provenances (Aberdeen, Fair Harbour, Moresby, Tasu, Muir) virtually every leader
with eggs was killed (Figure 3). Clones from provenances with intermediate
resistance (Cedarvale, Kitwanga, Green Timbers) sustained high rates of
oviposition, suggesting strong attraction, and low feeding and oviposition
repellency. However, the leaders were killed at moderate levels, suggesting only
mild antibiotic effects, i.e. mild toxicity was exerted on the weevil larvae. Clones
from the most resistant provenance (Haney families 0 and 1) had significantly lower
oviposition and leader kill rates than the rest, suggesting high levels of repellency
(physical or chemical) and toxicity. The most resistant genotype (Haney family 0,
clone 2, also known for its registration number as #898), sustained consistently low
oviposition rates, with about 12% of the ramets having oviposition at the Fair
Harbour trial, of which only about 6% resulted in leader kill.
2.2 INSECT BEHAVIOR AS INDICATOR OF TREE RESISTANCE

Knowledge of host-selection behavior and patterns of dispersal are important to
understand plant defences and to develop ecologically durable polygenetic
resistance. Studies of visitation rates (or avoidance), disclose within and between
plant variations in plant defences. However, such studies require standardization
since there is significant variability in circadian and seasonal movement and
dispersal behavior (McIntosh et al. 1997).
Studies of marked P. strobi (McIntosh 1999) in white spruce showed circadian
and seasonal movement within and between trees (Figure 4) (McIntosh et al. 1996;
McIntosh 1997). Extensive feeding activity occurred in the lower stem and the
undersides of lateral branches before weevils moved to the one-year old terminals to
feed and lay eggs, suggesting a temporal variation in within-plant resistance.
Interestingly, weevils spent a relatively short amount of time at the site of
oviposition and brood development, the one-year old leader, preferring to remain on
the lower stem and in the foliage of lower order branches particularly during times
of the day when temperatures were high (Figure 4). These observations supported
the contention that, in addition to localised, within-plant resistance, feeding and
oviposition behavior is strongly influenced by environmental conditions (Sullivan
1961).
In studying seasonal dispersal patterns of weevils, McIntosh (1997) and (Harman
1975) showed that most movement occurred locally, on average within 3-4 trees
(approximately 3-5 m) in a series of small steps. The result is a highly uneven
spatial distribution of insects in the plantation, with some susceptible plants
escaping attacks and some moderately resistant plants sustaining heavy insect
pressure. Therefore, such skewed distributions must be taken into consideration
when ascribing resistance ranking to tree genotypes. We concluded that
comparative studies to understand within-plant variation in resistance by observing
the presence of the insect on the plant must be preceded by a clear understanding of
the insect's behavior and preferences.
2.3 PLANT APPARENCY

Barring escape, trees that survive without oviposition under heavy weevil pressure,
are either not apparent, i.e. they lack visual or chemical stimuli that cue the insect
into the plant, (Feeny 1976), or they contain feeding or oviposition deterrents
(Tomlin and Borden 1996). Attributes that are attractant or repellent influence the
intensity, distribution and duration of weevil attack in space and time. Apparency
increases by having an appropriate leader silhouette (VanderSar and Borden 1977b),
or potentially attractive odors (Tomlin et al. 1997).
In evaluating genotypes of Sitka spruce (all from resistant provenances) for total
amounts of foliar terpenes, we found one genotype with almost twice the amounts as
in susceptible trees (Tomlin et al. 1997). Assuming that volatile terpenes are
involved in host selection, this genotype would be very apparent. Some genotypes
had similar levels of foliar terpenes as susceptible control trees, but five had levels
that were <23% of these in susceptible trees, including one that had no detectable
foliar terpenes. Thus lack of chemical apparency may be one of several constitutive
resistance mechanisms.
Highly apparent spruces must rely heavily on other constitutive defences such as
high densities of bark resin canals, and induced defensive responses such as the
development of traumatic resin canals (Shrimpton 1978; Berryman 1988; Raffa
1991; Alfaro 1995; Martin et al. 2001). The speed and intensity of the defensive
response most likely influence the ability of the tree to resist attack by P. strobi.
2.4 CAGE TESTING GENOTYPES FOR RESISTANCE

Testing genotypes in cages, which are inoculated with insects, provides the
researcher with more information than field studies, on the nature of the resistance.
However, this method is laborious and therefore suited for detailed study of only a
few particularly interesting genotypes. Also, confined insects do not display all
behaviors associated with the encounter and selection (or rejection) of a putative
resistant plant, because the cage interferes with within- and between-tree dispersal
(McIntosh et al. 1996; McIntosh 1997). Insects may be exposed to a selection of
genotypes, a choice between two genotypes, or given no choice at all. In no-choice
experiments, insects on a highly resistant plant must feed or starve, oviposit or re-
absorb their eggs. In these situations, weevils may feed on highly resistant spruce
trees, but reject them for oviposition. They may also fail to develop their ovaries,
may sustain ovarian regression and the inhibition of the expression of genes
involved in reproductive development (Gara and Wood 1989; Sahota et al. 1994;
Leal et al. 1997; Trudel et al. 1998). The precise mechanisms for induction of
physiological regression are not known, but could range from simple starvation to
complex endocrine effects.
Choice situations allow test insects to move within the confines of a cage and to
select plants according to their own preferences. Sometimes clones that are highly
resistant in the field may be readily attacked in a cage. For example, the highly
resistant Sitka spruce clones from the Haney provenance, which have shown field
resistance (Alfaro and Ying 1990; Ying 1991) (Figure 3), were colonized in cage
experiments (Alfaro 1996b, and unpublished obs.), apparently because confined
weevils could not disperse to more suitable hosts, and eventually were forced to
oviposit in a host that would normally be rejected in the field.
Cage experiments allow the controlled study of insect behaviour. Alfaro (1996b)
observed the movements of weevils in choice experiments in which the highly
resistant Haney clones were mixed with susceptible stock. Test weevils moved
away from the resistant clones and settled on susceptible genotypes, possibly in
response to olfactory or gustatory stimuli (Figure 5). Host repellency and/or
deterrency to P. strobi has been demonstrated in laboratory feeding bioassays using
paired twigs (Tomlin and Borden 1996; Alfaro 1996b), or paired agar disks (Alfaro
et al. 1979, 1980), and by study of rates of visitation in the field or in cages
(McIntosh 1997; Alfaro 1996b).
Klimaszewski et al. (2000) used cage experiments to test Sitka spruce genotypes
of the Big Qualicum Sitka spruce provenance in a choice situation. He confirmed
the resistant status of the Big Qualicum provenance and concluded that toxicity to
larvae, possibly by resin, was a major cause of resistance in these genotypes.
2.5 TESTING FOR SPECIFIC RESISTANCE MECHANISMS.

Variation in several traits has been associated with resistance to white pine weevil
attack. These include variation in the chemical composition of feeding stimulants
and deterrents (Alfaro et al. 1980), differences in resin canal density (Alfaro et al.
1997; Tomlin and Borden 1994a,b; 1996) associated with bark thickness (Stroh and
Gerhold 1965; Tomlin and Borden 1997a, Alfaro et al. 2000a), high density of
sclereid cells (Grau et al. 2001), and production of traumatic resin (Alfaro 1995;
Tomlin et al. 1998). Differences in the physical and chemical properties of the resin
are also thought to play a role in resistance (Tomlin et al. 2000). These mechanisms
often occur simultaneously, each one playing some role, but the relative importance
of each defence system varies in different spruce genotypes. Specific tests are
required to determine the importance of each mechanism.
2.5.1 Plant phenology

Phenology plays an important role in trophic relationships within an ecosystem.
Early or late budburst (Figure 6) or rate of shoot growth affects quality and quantity
of food available for herbivores at specific times (Quiring 1993, Carroll and Quiring
1994; Langvatn et al. 1996), directly affecting herbivore population levels.
Differences in phenological development of allopatric plant populations may be
correlated with seasonal variation in plant defences, such as synthesis of resin and
other defensive chemicals (Muzika et al. 1993).
Conifer shoots are a challenging feeding substrate for herbivores. During

dormancy, the bark cortex is covered with a thick and tough outer layer or
epidermis, the needles are hard and fibrous, and the buds are tightly packed under
thick scales. Young bud mining larvae of many insects, such as those of the spruce
budworm, Choristoneura spp. (Shepherd 1983), and the spruce bud moth,
Zeiraphera canadensis (Carroll and Quiring 1994), have difficulties penetrating the
shoot buds, which are their preferred feeding sites after they emerge from
overwintering. However, as the season progresses, bud scales soften, separate and
new, tender foliage is exposed to herbivory (Figure 6).
Testing for phenological defences involves the comparative study of the tree
phenology (stages of budbreak and shoot elongation) and the concurrent progress of
insect development: oviposition, larval maturation, pupation and emergence. Hulme
(1995) and Alfaro et al. (2000b) found that resistant Sitka spruce families tended to
initiate growth earlier than susceptible families. However, considerable family-to-

family variation existed. Hulme (1995) also demonstrated that if the synchrony
between the phenology of the clones and the phenology of P. strobi was altered, the
white pine weevil could successfully attack resistant genotypes. Phenology is
generally considered to be a static constitutive defence system. However, recently,
A. Carroll (Pacific Forestry Centre, Can. For. Serv., Victoria, BC, Canada, pers.
comm.) documented modifications in white spruce phenology induced by spruce
bud moth feeding, in years that follow attack. These induced changes improved the
budburst-insect synchrony and reduced phenological resistance.
2.5.2 Bark resin canals

The most salient features of the internal anatomy of the conifer shoot are the
presence of constitutive resin canals in the xylem and the inner bark. Constitutive
xylem resin canals develop from the cambium, and occur in low densities at
somewhat regular intervals. Bark resin canals originate from the apical meristem at
the time of shoot development and branch frequently (Jou 1971). In spruce, two
distinct sets of constitutive resin canals can be distinguished in the shoot bark: large
and ubiquitous inner resin canals arranged in a ring close to the cambium, and small
(outer) resin canals lying toward the periphery of the bark, just below the epidermis.
The latter occur in pairs, usually in the bark ridges (Figure 7).
Severing of these ducts results in a passive flow of resin which serves to cleanse
and seal wounds, as well as to repel invading insects (Berryman and Ashraf 1970,
Christiansen and Horntvedt 1983; Christiansen et al. 1987; Berryman 1988; Baier
1996, Alfaro et al. 1997; Tomlin and Borden 1997a; Cornelissen and Fernandes
1998). Bark resin canals form “chemical mine fields” which the weevil adults and
larvae must avoid during feeding and oviposition. Therrien (1995) and Silver (1968)
indicate that drowning of the eggs and young larvae by constitutive or traumatic
resin is an important mortality factor for the white pine weevil.
Using an image analysis system, we conducted extensive studies of bark resin

canal density in Sitka and white spruce and its relationship with weevil resistance.
Our studies indicate that most resistant Sitka and white spruce populations rely
heavily on dense constitutive resin canal systems for defence (Alfaro et al. 1997,
2000a; Grau et al. 2001; Tomlin and Borden 1994a; Tomlin et al. 1998) (Figure 8).
An important finding from our studies was that the density of resin canals in the
previous year’s leader (the preferred feeding site of P. strobi) diminishes throughout
the growing season because of shoot radial growth (Brescia 2000). Reduction of the
resin canal defence could contribute to the successful attack found by Hulme (1995)
in late spring on resistant trees. Therefore, measuring resin canal densities requires
standardisation of seasonal sampling dates.
This constitutive resin canal resistance mechanism may be enhanced by thin
bark, which increases the proportional area of bark occupied by resin canals (Tomlin
and Borden 1977a). Sitka spruce from the Queen Charlotte Islands, where there are
no P. strobi, have few to no outer resin canals, suggesting a lack of selection
pressure to acquire or retain this trait (Tomlin and Borden 1994a). Because highly
resistant trees from the Big Qualicum provenance have low densities of outer and
inner resin canals (Tomlin and Borden 1994a, 1997a, Brescia 2000), we concluded
that other powerful mechanisms of resistance must occur in these genotypes, e.g.
feeding and oviposition deterrency (Tomlin and Borden 1996) and toxicity to eggs
and larvae (Klimaszewski et al. 2000).
In his studies of reciprocal white spruce crosses, McIntosh (1997) found

evidence of constitutive resistance to P. strobi in a number of ways. In the two top-
ranked families, a high proportion of trees had numerous feeding punctures,
suggesting weevils adequately tested and then rejected these crosses as oviposition
hosts due to some antixenotic or non-preference effect.
2.5.3 Sclereid cells

Sclereid cells (Esau 1965; Fahn 1969) occur in several vegetative organs of various
trees, shrubs, and herbaceous species. Among conifers, they have been noted in the
leaves and shoots of Pseudotsuga, in the cortex of Cedrus and Larix, and in the pith
of Picea and Abies (Sterling 1947). Sclereids originate from parenchyma cells that
enlarge, lignify and thicken their walls, and have been mostly associated with
mechanical support (Carlquist 1984; Nyffeler et al. 1997; Lev-Yadun 1994; Quilhó
et al. 2000). A few studies on angiosperm species link sclereids with resistance to
insects (Chakravarthy et al. 1985; Carlquist 1984; Nyffeler et al. 1997). We found
that sclereid cells are present in the shoot phloem, the food for weevil adults and
larvae, and that they were significantly more numerous in some resistant Sitka and
white spruce genotypes, relative to susceptible genotypes (Figure 9) (Grau et al.
2001). In resistant Big Qualicum Sitka spruce trees, a high density of sclereids
could compensate for a generally low number of outer resin canals, and could
contribute significantly to feeding and oviposition deterrency.
2.5.4 Inducible defences.

An important breakthrough in our studies was the discovery of the production of
traumatic resin in Sitka and white spruce shoots in response to natural weevil
wounding (Alfaro 1995, Alfaro et al. 1996a, McIntosh 1997) (Figure 10A). When
wounded, the cambium switched from production of tracheids and phloem, to the
production of traumatic resin canals (Alfaro 1995). These produce a resin with a
much higher monoterpene to resin acid ratio than in constitutive resin, which makes
traumatic resin less viscous and more likely to flood out egg niches and new larval
mines, killing the occupants (Tomlin et al. 2000). If the tree repels the weevil, the
production of traumatic resin canals stops and the cambium reverts to producing
normal xylem and phloem. The traumatic resin canals remain in the xylem, forming
a ring buried in the wood, which can be used to detect past encounters with P. strobi
(Figure 10B). Some trees were able to develop two, and in some cases three layers
of traumatic resin canals in response to feeding and subsequent oviposition and
larval feeding by P. strobi (Alfaro et al 1996a, McIntosh 1997). The formation of
traumatic resin canals in response to feeding by P. strobi, was also demonstrated to
occur in Norway spruce, Picea abies (L.) Karst. (Lavallée et al. 1999). A number of
studies followed which developed techniques to artificially induce the response and
measure its intensity in resistant and susceptible trees (Figure 11) (Tomlin et al.
1998, McIntosh 1997, Martin et al. 2001, O’Neill et al. 2001). Also, studies
calculated its dosage/response relationships (Brescia 2000), measured the speed of
the response using chemical (Nault and Alfaro 2001), biochemical (Martin et al.
2001), or molecular genetic techniques (J. Bohlmann U. of British Columbia, A.
Plant, Simon Fraser U., unpubl. obs.).
At the molecular genetic and biochemical level, the traumatic resinosis response
in spruce is both rapid and transient. Increased expression of terpene synthase (TPS)
genes responsible for resin terpenoid formation can reach a maximum within two
days after wounding of bark tissue or upon other treatments that simulate weevil
attack (J. Bohlmann, unpubl. obs., A. Plant, pers. comm). In Norway spruce,
simulated weevil attack leads to increased activity of two classes of enzymes of
resin terpenoid biosythesis, prenyltransferases and terpene synthases (Martin et al.
2001), which ultimately results in induced de novo resin terpenoid formation and
accumulation in newly formed traumatic resin canals in the developing xylem,
within one to two weeks after onset of simulated weevil attack (Martin et al. 2001).
This rapid response at the molecular genetic, biochemical and chemical levels is
well tuned with the timing of cell differentiation, which leads to traumatic resin
canal development (Martin et al. 2001). This response is also timed with the weevil
activities of egg laying and larval development, allowing the tree to mount this
second line of induced defence against the developing next generation of weevils.
Wounding also causes other changes in the conifer shoot. We found a significant
increase in bark thickness after artificial wounding of spruce shoots, which we
interpreted as a compensatory defence to repair damaged tissue. We also measured
a significant increase in the diameter of bark resin canals after artificial wounding,
suggesting an increase in their defensive function (Brescia 2000).
122 ALFARA ET AL.
2.5.5 Chemical defences

Chemical defences against P. strobi are just coming under investigation. Conifers
produce many secondary metabolites, which can have functions in defence and
resistance against insects and pathogens. These chemicals include alkaloids,
phenolics and terpenoids (Rowe et al. 1989). Terpenoids, or isoprenoids, occur as
defensive chemicals in conifers in hundreds of different chemical structures
(Bohlmann and Croteau 1999; Bohlmann et al. 2000; Trapp and Croteau 2001). The
early evolution of terpenoid defences has played a key role in the evolutionary
success of conifers (Seybold et al. 2000). As components of constitutive and
traumatic resins, terpenoids serve both chemical and mechanical defensive roles.
Many terpenoids appear to be toxic against insects and insect-vectored microbial
pathogens, and massive resin flow at the site of penetration physically immobilizes
insects or flushes the wound site. Volatile terpenoids also provide important
chemical cues for insects in host identification (Seybold et al. 2000). Upon
herbivory, changes in volatile terpenoid profiles of the host tree may serve as
chemical signals in attracting predators or parasitoids of the insect herbivore in
multitrophic plant insect interactions. Juvabione-type terpenoids of conifers,
derived from the common sesquiterpenoid E-alpha-bisabolene (Bohlmann et al.
1998a), can interfere with insect development regulated by juvenile hormone.
In the last five years, much progress has been made in deciphering the
biochemical processes and molecular genetic regulation of terpenoid formation in
conifers (Bohlmann and Croteau, 1999; Trapp and Croteau 2001). The enzymes
that determine the quality and quantity of terpenoid mixtures are the terpenoid
synthases that form the 10-carbon monoterpenoids, e.g. alpha- and beta-pinene,
limonene, myrcene, and 3-carene, the 20-carbon hydrocarbon skeletons of diterpene
resin acids, e.g. abietic acid and levopimaric acid, and the less abundant 15-carbon
sesquiterpenoids, e.g. farnesene and bisabolene. Monoterpenoids and diterpenoids
are the most abundant resin components of conifers, but sesquiterpenoids can serve
important defensive functions.
Eleven different terpenoid synthase genes (TPS ) were identified and
functionally characterized in grand fir (Bohlmann et al. 1998b, Bohlmann et al.
1999), in which formation of resin and non-resin terpenoids is genetically controlled
by multiple TPS genes that encode single-product and multi-product enzymes
(Bohlmann et al. 1997; Steele et al. 1998a,b). Many of the multi-product TPS
enzymes have a few major products and additional minor products (Bohlmann et al.
1999). Product profiles of the grand fir TPS can be partly overlapping, but each of
the eleven synthases has a unique product profile. Several TPS in grand fir respond
to simulated insect attack with increased gene expression and enzyme activities
(Bohlmann et al. 1997, Bohlmann et al., 1998a, Steele et al. 1998b).
This genetic background allows for variation of defensive terpenoid composition
in conifer evolution. While the basic metabolic pathways for terpenoid formation
are the same in spruces and in grand fir, the TPS genes and their biochemical
functions in spruces are different from those in grand fir, and their functions and
roles cannot be predicted based on similarities with grand fir genes (Bohlmann et al.
2000; Martin et al. 2001; J. Bohlmann, A. Plant et al., unpubl. results).
Our recent studies in spruce revealed that the effect of stem boring insects on
terpenoid gene expression, terpenoid biosynthesis, and emission, and resin
accumulation in traumatic resin canals can be mimicked by treatment of spruce trees
with elicitors without inflicting mechanical wounds (Martin et al. 2001). Externally
applied jasmonates induced the expression of TPS genes, TPS enzyme activities,
resin terpenoid accumulation and volatile terpenoid emission (Martin et al. 2001;
Bohlmann et al. unpubl. results). Surprisingly, application of jasmonates also
triggered the de novo formation of traumatic resin canals in the developing xylem.
We are currently exploring strategies for applications of jasmonates and other
environmentally safe elicitors for protection of trees against attack by insects and
pathogens.
3. MULTICOMPONENT RESISTANCE INDEX

The development of a multicomponent resistance index was conceived as a potential
measure of confidence in selecting parents for, and progeny from, a breeding
program that strives for durable resistance (Brooks and Borden 1992, Tomlin and
Borden 1994b, Alfaro et al. 1996b). Tomlin and Borden (1997b) reviewed a series
of studies and assigned power values to seven traits associated with resistance: bark
thickness, number of outer resin ducts, total amount of foliar terpenes, total amount
of cortical resin acids, feeding deterrency, oviposition deterrency and repellency.
Summing the power values for these individual traits gave a multicomponent score.
The highest negative correlation (-0.81, P<0.00017) between the multicomponent
index scores for 12 genetic sources of Sitka spruce and the actual incidence of
weevil attack observed in the field was achieved when feeding deterrency and
repellency were removed. As resistance becomes better understood, e.g. through
elucidation of its molecular basis, and breeding programs advance, evaluation of
resistance may be facilitated by the use of a standardized multicomponent index that
scores for a small number of highly desired, proven resistant traits.
4. CONCLUDING DISCUSSION
We found that an array of defences, some physical others physiological, some
constitutive others induced, protect spruce apical shoots against feeding and
oviposition by P. strobi (Table 1). These mechanisms occur simultaneously and
vary in strength in different spruce genotypes. Of paramount importance in shoot
defence against this weevil is the presence of resin canals in the bark at sufficient
density to form a barrier to feeding and oviposition. Similarly, thick-walled sclereid
cells in the bark form a sort of armour plating of the shoots, making the bark and
phloem tough and difficult to consume. If these first, constitutive barriers to weevil
feeding and oviposition are breached, spruce trees invoke induced responses,
particularly the formation of traumatic resin canals, which secrete resin directly into
oviposition punctures and larval galleries. A variety of chemicals, are involved in
defence against shoot infesting insects. Some of these chemicals are constitutive but
others are produced in direct response to insect feeding. Terpenoids in particular
occur in a variety of structures and are toxic to eggs and young larvae. Spruce
phenology is an important mechanism of defence dictating the timing of physical,
physiological and molecular events involved in resistance. As a tool for screening
spruce genotypes, these resistance mechanisms can be combined into a
multicomponent resistance index, and may potentially be exploited in developing
resistant planting stock that can be used to minimise the impact of the white pine
weevil in young plantations.
For successful colonisation of terminals, female P. strobi must quickly lay their
complement of eggs during a short period of time. Oviposition should coincide with
a window of susceptibility, in which the array of constitutive defensive mechanisms
is at its lowest, and before the tree is capable of mounting a strong induced defence.
We are currently in the process of identifying a set of spruce genotypes that have
particularly high levels of specific resistance mechanisms (e.g., high density of bark
resin canals, or high levels of sclereids cells). Using the conventional methods of
tree breeding, we hope to combine these mechanisms into new genotypes that will
have higher chances of surviving weevil attack with minimal damage. We are also
developing methods to deploy the resistant genotypes using silvicultural systems
that reduce the likelihood of insect adaptation to the new genotypes.
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Proceedings of a meeting held Jan. 19-21, 1994, in Richmond, B. C., Canada. Can. For. Serv. FRDA
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CHAPTER 5
HOST TREE RESISTANCE TO WOOD-BORING

INSECTS
TIMOTHY D. PAINE
Department of Entomology, University of California, Riverside, CA, USA 92521
Insect orders that include species that are commonly referred to as borers include the
Hymenoptera, Diptera, Lepidoptera, and Coleoptera (Furniss and Carolin 1980,
Soloman 1995). Larvae of the primitive horntails (Siricidae) and wood wasps
(Xiphydriidae and Syntexidae) construct feeding galleries in the wood and adults
prefer to oviposit on weakened host trees. In contrast, larvae of boring sawfly
species in the families Tenthredinidae and Cephidae often feed within the center of
tender shoots, twigs, and stems of their host plants. The larvae of a small number
of fly species in family Agromyzidae mine the cambial tissue of their host tree
(Green 1914, Wallner and Gregory 1980). The trees overgrow the galleries so that
the mine remains in the wood leaving injury patterns that can be characterized as
boring damage.
Wood boring life history strategies can be found in a large number of moth
families in the Lepidoptera. However four families, the Hepialidae (ghost moths or
swifts), the Sesiidae (clearwing moths), the Cossidae (carpenterworm moths), and
the Tortricidae (twig borers and tip moths), are comprised of species that only have
a boring life history or that have significant numbers of boring species (Soloman
1995). Ghost moth and carpenterworm larvae can cause significant damage as they
tunnel extensively in the wood of their host plants. The life histories of species of
Sesiidae can be highly variable and may include boring in bark, cambium, wood,
roots, or gall tissues. Larvae of many of species of Tortricid moths bore through the
twigs and tender terminals of vigorous trees and shrubs. There also are a number of
other families of Lepidoptera, including Agonoxenidae, Argyresthiidae,
Gelechiidae, Momphidae, Nepticulidae, Noctuidae, Pterophoridae, Pyralidae, and
Thyrididae, with at least some species that can be characterized as borers.
131
132 T.D. PAIN
Coleopterans are probably the most widely represented among wood boring
insects. A large number of families are comprised of species with larvae that are
exclusively boring or have very few representatives that have evolved alternative
life history strategies to boring in woody tissues. Although not an entirely
comprehensive list, the families include Anobiidae (deathwatch beetles),
Bostrichidae (false powderpost beetles), Brentidae (timber worms), Buprestidae
(metallic or flatheaded borers), Cerambycidae (longhorned or roundheaded borers),
Lyctidae (powderpost beetles), Lymexyliidae (timber beetles), Platypodidae
(ambrosia beetles), and Scolytidae (bark beetles) (Furniss and Carolin 1980,
Soloman 1995, USDA 1985). Curculionidae (weevils) is a very diverse family with
a large number of species, including several species with larvae that bore into plant
tissues.
Borers can colonize all plant tissues. Larvae of species in a number of families
(e.g., Cerambycidae and Hepialidae) may construct feeding tunnels, or galleries,
within the large roots of broadleaf trees and conifers which can weaken the trees
directly or provide entry points for invasion by pathogenic fungi (Gross and Syme
1981, Hanks 1999). At the other extreme, there are many species of insects that
colonize the meristematic tissues at branch terminals, tips, twigs, and canes. Some
of these insects feed in the phloem tissues, girdling the twigs, while larvae of other
species burrow through the growing tips and into the elongating stems. These types
of larval feeding can reduce plant growth, apical dominance, and plant form
(Holsten and Gara 1975).
The woody xylem tissues, cambial layers, phloem tissues, and bark of trees may
all have different groups of specialist borers. For example, larvae of a few species
of clear winged moths feed within the bark of their host plant (Brown and Eads
1965). Scribble-barked gums are species of eucalypts in Australia that derive their
common name from the twisting galleries constructed between the old and new
layers of outer bark of Eucalyptus haemastoma by Ormograptis scribula
(Lepidoptera:Yponomeutidae) (Norris 1970). Bark beetle larvae feed within the
cambial and phloem tissues of their hosts (Furniss and Carolin 1980), while larvae
of many species of longhorned and flatheaded borers feed in the outer layers of
phloem and cambium but then bore deep into the wood to pupate (Hanks et al.
1993). Larvae of cossid moths feed almost entirely within woody tissues and may
take several years to complete their larval development (Hay and Morris 1970). Not
only do the larvae bore in woody tissues, the adults in a number of species within a
variety of families (e.g., some species of Scolytidae and Platypodidae) bore into the
plant. The larvae of ambrosia beetles are found in galleries excavated within the
wood of weakened, injured or dying trees; they feed on a fungus inoculated into the
tissue by the parental adults rather than on the plant itself (Nord and McManus
1972).
Plants in a wide range of physiological conditions may be subject to colonization
by borers. While some species of borers utilize healthy hosts or healthy host tissues,
many others are either attracted to or are arrested by plants that are suffering from
some type of stressful condition (Furniss and Carolin 1980, Soloman 1995).
Weakened or stressed host plants may result from chronic growing conditions (poor
HOST TREE RESISTANCE TO WOOD-BORING INSECTS 133
quality site) or from acute detrimental changes (e.g., fire, flood, drought, lightning)
(Paine and Baker 1993). Open wounds, stressed, damaged, or weakened plant
tissues may be subject to invasion. Recently killed and dying trees are particularly
suitable for colonization by a range of borers. For example, there are several species
of wood wasps and roundheaded borers that are attracted to trees that have been
recently killed by fires (Wickman 1964, 1967). In addition, previous infestation by
other insect herbivores or pathogens may weaken the host plant and increase
susceptibility for subsequent borer colonization (Linit and Kinn 1993, 1996). Borers
that are adapted to colonize the woody tissues of dead or dying plants may also
colonize trees that have been cut during commercial logging or even timber that has
been milled into lumber. It is not unusual for adult borers to emerge from products
or materials constructed from infested wood that has not been kiln-dried or
otherwise treated to kill the infesting insects.
The resistance mechanisms that are under some living control (i.e., induced and
preformed defenses) are important against phloem feeders and other primary
colonizers and may become critical factors if wood borers colonize relatively
healthy trees (Paine et al. 1997). In many conifers, the preformed or primary
resistance associated with terpenoid oleoresin has long been recognized as a barrier
to bark beetle attack (Nebeker et al. 1992, Raffa and Berryman 1983). Conifers also
have inducible physical and chemical processes that are associated with resistance
following insect and fungus colonization (Lieutier et al. 1995, Paine et al. 1997).
However, these resistance mechanisms that may be effective against phloem feeders
may not be critical factors if the insects are colonizing dead and dying trees. Many
wood borers are frequently part of a guild of secondarily invading scavengers of
host material weakened by environmental factors, disease, or other insect activity
(Hanks 1999). The physical factors that are associated with the bark or wood (e.g.,
lignin stone cells [Wainhouse et al. 1990]) can remain and may affect the survival of
wood borer larvae.
In his comprehensive evaluation and classification of cerambycid reproductive
behavior, Hanks (1999) divides longhorned borer species into four groups based on
the physiological condition of the host plant normally attacked by ovipositing adults:
healthy, weakened, stressed, and dead. Implicit in the classification is the
assumption that there is a direct relationship between weakness or stress and host
resistance to insects. While this has been extensively studied for bark beetles
(Nebeker et al. 1993, Paine et al. 1997), there are few examples where resistance
characteristics have been directly tested for wood borers. Bark moisture (Qin et al.
1996)), sap flow (Duffy 1968), and secondary chemistry (Wang et al. 1995) have
been studied in a few instances.
Host resistance to one wood borer has received a significant amount of attention
because of the economic damage caused by the insect. The eucalyptus longhorned
borer, Phoracantha semipunctata F. (Coleoptera: Cerambycidae), has been
introduced from Australia into many parts of the world where Eucalyptus is grown.
In Australia, the beetle colonizes weakened trees or fallen branches (Pook and
Forrester 1984). Resistance of living Eucalyptus to infection and invasion has been
associated with induced production of a polyphenolic resin, or kino (Hillis 1978).
134 T.D. PAIN
However, there may be differences in tree colonization patterns of wood-borers in

Australia compared to exotic environments in North America, South America,
Africa, and in the Mediterranean basin where colonization of water stressed trees
appears to be critical (Hanks et al. 1991, 1995, 1999).
In California, Eucalyptus resistance to Phoracantha semipunctata colonization
appears to be independent of the induced response, but rather is a function of a
physical factor. Hanks et al. (1995) examined the susceptibility of a broad variety of
Eucalyptus species over a period of time that included a prolonged drought.
Although some species were more susceptible than others, tree survival was
influenced by variation in moisture availability and corresponded with reported
drought tolerances. A separate study demonstrated that kino production could not
account for differences in resistance of trees under water stress (Hanks et al. 1999).
However, if the water content of the outer bark exceeded a critical level
(approximately 60%), then the larvae are virtually incapable of penetrating that
barrier. These results confirm a previous study in which bark penetration of borer
larvae was significantly improved in cut dry logs compared to logs that maintained
moisture in the bark, as well as in trees with severed roots compared to undamaged
trees (Hanks et al. 1991). Host resistance was observed in the absence of a kino
reaction, and even if induced reactions were present, they did not appear to be
critical resistance factors because of the temporal lag in response (Hanks et al. 1991,
1999).
A large number of Eucalyptus species have been introduced throughout the
world because of their importance to the timber, cellulose, landscape, and
horticultural industries. Approximately 90 species have been introduced into North
America over the last 150 years (Doughty 2000). Many of these species originate in
the southeastern quarter of the Australian continent that is characterized by warm
moist summers. The regions of the world where Eucalyptus species have been most
extensively planted have typically Mediterranean climates that are characterized by
prolonged hot dry summers. In the native range of the beetle and the host trees, the
climatic conditions would support fully hydrated outer bark during the time of year
that the beetles are most active (Hanks et al. 1993a). In contrast to conditions in the
endemic range, the rainfall patterns in regions with Mediterranean climates would
significantly limit the effectiveness of a resistance mechanism based on water
content of the outer bark. The trees would be subject to maximum annual water
stress during the time of year beetles are actively searching for suitable hosts. Adult
beetles are attracted to the volatile chemicals produced by cut wood and stressed
trees (Hanks et al. 1993b); water stressed trees may recover in the absence of the
beetles, but the combination of effective insect search behaviors and reduced tree
resistance has resulted in significant levels of tree mortality in the expanded
geographic distribution of the tree compared to the endemic range.
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Gross, H. L., and Syme, P. D. 1981. Damage to aspen regeneration in northern Ontario by the ghost
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Hanks, L. M. 1999. Influence of the larval host plant on reproductive strategies of cerambycid beetles.
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Hanks, L. M., McElfresh, J. S., Millar, J. G., and Paine, T. D. 1993a. Phoracantha semipunctata F.
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Hanks, L. M., Paine, T. D., and Millar, J. G. 1991. Mechanisms of resistance in Eucalyptus against
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Hanks, L. M., Paine, T. D., Millar, J. G., and Hom, J. L. 1995. Variation among Eucalyptus species in
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Applicata 74: 185-194.
Hanks, L. M., Paine, T. D., Millar, J. G., Campbell, C. D., and Schuch, U. K. 1999. Water relations of
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Hay, C. J., and Morris, R. C. 1970. Carpenterworm. Forest Pest Leaflet 64. Washington, D. C., U. S.
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Nebeker, T. E., Hodges J. D., Blanche, C. A., Honea, C. R., and Tisdale, R. A. 1992. Variation in the
constitutive defense system of loblolly pine in relation to bark beetle attack. Forest Science 38:457-
466.
Hillis, W. E. 1978. Wood quality and utilization. In. Eucalypts for Wood Production (W. E. Hillis and
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Holsten, E. H., and Gara, R. I. 1975. Flight of the mahogany shoot borer, Hypsipyla grandella. Annals
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CHAPTER 6
PLANT RESISTANCE AGAINST GALL-FORMING

INSECTS: THE ROLE OF HYPERSENSITIVITY
TATIANA G. CORNELISSEN1,2, DANIEL NEGREIROS2,

G.WILSON FERNANDES2
1
Department of Biology SCA 110, University of South Florida, 4202 E Fowler Avenue
Tampa, Florida, 33620-5150, USA. E-mail address: tgcornel@chuma.cas.usf.edu
2
Ecologia Evolutiva de Herbívoros Tropicais/DBG, CP 486, ICB/Universidade Federal de
Minas Gerais, Belo Horizonte MG 30161-970, Brazil.
1. INTRODUCTION
The understanding of how plants defend themselves against attack by herbivores has
been the focus of many studies since the beginning of the last century. Plants are
not passive agents under attack by natural enemies or damage caused by
environmental phenomena (Fernandes et al. 2000). Plant defense against herbivory
can be categorized into three mechanisms: either flee, fight, or weather the attack.
Plants can flee by developing before herbivore numbers are high (Feeny 1976), fight
and defend themselves by being unsuitable food for herbivores (Renwvick 1983), or
cope with herbivory through tolerance (Rosenthal & Kotanem 1994, Strauss &
Agrawal 1999).
Because herbivores are not always predictable, and plant defences may be costly
(Schoonhoven et al. 1998), it is believed that some plant species can use damage
suffered as a cue to induce resistance against subsequent herbivores. Karban &
Baldwin (1997) refer to changes in plants after damage or stress as induced
responses. These changes may or may not affect herbivores and/or plants that
express these responses. On the other hand, the induced responses that reduce
herbivore survival, growth rate, fecundity or preference for a plant are determined
induced resistance. Finally, those induced responses that decrease the negative
effects of attacks on plants are named induced defences. Induced resistance is an
arthropocentric perspective, while induced defence is a phytocentric perspective of
the changes in the plant in response to insect activity.
137
138 T.G. CORNELISSEN et al.
Induced resistance is dependent on factors present only after the host is challenge
by the external inducing agent, as opposed to constitutive resistance, which is
dependent on preformed factors. For the past six years we have been studying the
resistance of a tropical plant species, Bauhinia brevipes Vog. (Leguminosae), after it
is attacked by its major herbivore, the galling insect Contarinia sp. (Diptera:
Cecidomyiidae). This species resists the attack through a very special type of
resistance, the Hypersensitive Reaction (HR). In this chapter we discuss the
morphological and anatomical changes that the host’s hypersensitive tissues undergo
when resisting gall induction, and HR efficiency in regulating the insect herbivore
population. We also provide information on how widespread and relevant is HR
against gall induction.
2. INDUCED RESISTANCE AGAINST HERBIVORY

Studies of plant resistance against herbivores have focused on a wide range of traits,
including changes in secondary chemistry (e.g., Ayres et al. 1997, Wold & Marquis
1997), mechanical traits (e.g., Fernandes 1994, Kudo 1996, Agrawal 1999), and
plant nutrition (e.g., Jaramillo & Detling 1988, Faeth 1992). Changes that occur in a
plant after it has been induced may affect the attackers or even other herbivores that
attempt to use the plant at a later time. Induced resistance is a mechanism by which
the plant reduces the preference and/or performance of subsequently attacking
herbivores. It may be caused by a variety of nonexclusive biochemical and physical
resistance mechanisms (Agrawal 1999). The changes in the survival, growth rate,
fecundity, and herbivore behaviors should be reflected in the sizes and dynamics of
herbivore populations.
Induced resistance exists in two different forms: localized and systemic.
Systemic resistance refers to resistance that occurs at sites in the host distant from
the point of initial interaction with a potential colonizer. Localized resistance can be
detected only in the area immediately adjacent to the site of attack by the invading
organism, such as pathogens and sucking and galling herbivores. This type of
resistance is often accompanied by a rapid collapse and desiccation of host tissue,
termed a hypersensitive reaction (Sequeira 1983, Fernandes 1990).
3. HYPERSENSITIVE REACTION: DEFINITIONS AND OCCURRENCE

Plant hypersensitive reaction (HR) was a term primarily used by plant pathologists
to describe a response to infection by pathogens as well as to many nonpathogenic
stimuli (Sequeira 1983). At the beginning of the last century it was recognized as
the most important mechanism of plant resistance against microorganisms such as
fungi, bacteria and viruses (e.g., Ward 1902, Stakman 1915, Maclean et al. 1974,
Gopalan et al. 1996, Low & Merida 1996), and has now been reported against
nematodes (Jackson & Taylor 1996). HR is a localized resistance that can be
detected in the area immediately adjacent to the site of attempted penetration by the
invader. This host response includes morphological and histological changes that
PLANT RESISTANCE AGAINST GALL-FORMING INSECTS 139
cause the death of the attacked tissue (Box 1), and, thus, the localization,
containment, inactivation, and death of the aggressive agent (see Fernandes, 1990,
1998). This reaction also leads to a disruption of nutrient supplies to the invading
organism, as well as the production of toxic metabolites. Furthermore, phytoalexins
(3-deoxyanthocyanidin flavonoids) are synthesized and begin to accumulate in the
epidermal cells. The necrotic response, easily observed as a brown circular spot
around the site of tissue penetration by the invader, is the result of a disturbance in
the balance between oxidative and reductive processes, which results in an excessive
oxidation of polyphenolic compounds (Király 1980). Many resistant reactions that
result in the HR are highly specific because they are under the control of host genes
whose products interact with products of single genes in the invader organism
(Sequeira 1983).
Although the occurrence of this induced resistance against microorganisms was

well documented, there were at the end of the last century relatively few examples
of HR of plants against insect herbivores (see Fernandes 1990 for a review).

Otherwise, the pioneer study of Berryman and his group showed that HR was an
important component of pine resistance against bark beetles, a large guild of insect
herbivores (e.g., Berryman 1972, Berryman & Ferrell 1988). The host response,
was, on the other hand, to the mutualistic fungus carried by the beetle.
4. HYPERSENSITIVITY AGAINST GALL-FORMING INSECTS

The defense mechanism used by the plant is influenced by the physiological status
of the plant, damage level, type of tissue removed, and intimacy of the relationship
between the plant and herbivore (Fernandes 1990). Plant galls are remarkably close
associations between arthropods, specially insects, and plants, in which the plant
produces an abnormal growth of tissue in response to a specific stimulus from the
invading organism. Hence, the gall-inducing organism alters the physiological state
of plant tissues, especially that of cells nearest to the feeding larvae (Shorthouse
1986), which is maintained in a metabolically active state by the galling-agent.
After reviewing the literature on HR, Fernandes (1990) showed that it could be
an important, yet neglected, mechanism of plant resistance against some large guilds
of insect herbivores. The elicitation of HR ought to be observed among insects with
a tight association with their host plants, such as miners, borers, and specially
galling insects, since most of their life stages occur within the plant tissue. These
intimate interactions may select more specific and more complex defenses because
of the greater and more opportunities that the host plant has to regulate the lives of
its intimate associates. The intimacy of the association posed by the herbivorous
feeding habitat and quality of tissue removed and attacked may have set the scenario
for the development and evolution of this special, efficient, and widespread
mechanism of plant resistance.
The first reported example of HR against an insect herbivore may have been that
of grapes and the galling insect Phylloxera vastatrix (Börner & Schilder 1934).
Otherwise, records of HR to fossil herbivorous insects have now been recognized
(C. Labandeira, pers. comm.). Hypersensitivity have been also reported for Eurosta
solidaginis, a tephritid stem galler on Solidago altissima (Anderson et al. 1989).
More than 70% of Eurosta larval mortality was due to HR by the host plant. Tissue
necrosis representing a typical hypersentitive reaction was observed in rice against
the Asian rice gall midge Orseolia oryzae (Bentur & Kalode 1996). Tentative of
control of this grain pest has been through the development of resistant rice
varieties. Artificial infestations of some resistant rice seedlings with an avirulent
biotype of the Asian rice gall midge showed extensive necrosis of meristematic
tissue. This tissue necrosis was observed within 4 days of infestation, and dead first
instar larvae were also observed in the vicinity of the necrotic tissue.
We have been studying in detail the hypersensitive reaction of Bauhinia brevipes
against its major galling and free-feeding herbivores. B. brevipes is a cerrado
(savanna) leguminous shrub of approximately 3 meters high (Cornelissen et al.
1997). Several galling and free-feeding insects attack this species (Cornelissen et al.
1997) (Figure 1). During the last six years, attacks were primarily caused by
Naupactus lar (Coleoptera: Curculionidae), Pantomorus sp. (Coleoptera:
Curculionidae) and by an unidentified larva of Geometridae (Lepidoptera). Seven
still undescribed galling species attack B. brevipes: a new species of Contarinia
(Diptera: Cecidomyiidae), two other undetermined leaf gallers (Diptera:
Cecidomyiidae), and four stem gallers (one Cecidomyiidae, one Lepidoptera, and
two Curculionidae; see Cornelissen et al. 1997, Cornelissen & Fernandes 1998). The
leaf galls studied are caused by Contarinia sp. on the adaxial leaf surface of B.
brevipes. Galls are spherical, with long red hairs covering their external walls, and
contain a single chamber, with one larva per chamber (Fernandes 1998).
The hypersensitive reaction of the leaf tissues of B. brevipes against gall
formation is observed as a rounded halo around the gall induction site.
Undetermined polyphenolic substances start to accumulate around the attacked cells
soon after penetration by the galling-larva (Fernandes et al. 2000). These
substances, black at first, are easily observed in the leaf veins inside the stimulated
region. Later, cells become necrotic, characterizing the HR against the gall
formation. Initially, the necrotic process appears to be slow. A peculiar reaction
occurs in the proximity of the midvein where the cells of the bundle sheat divide
giving rise to a cambium-like tissue that forms a protective layer around the
conductive tissues. Also, the parenchyma of the minor veins reacts in a peculiar
way, disorganizing the conductive cells of the xylem and phloem (Fernandes 1998,
Fernandes et al. 2000). These veins end up collapsing completely at the HR site,
hence, impeding the flow of sap to the HR site, isolating it completely from the
normal adjacent tissue. By this way, the plant localizes and ends the invasion of the
gall-inducing larva.
5. THE WIDESPREAD OCCURRENCE OF HR AGAINST GALL-

FORMATION
Induced resistance has been found on many diverse families and habitats. The plant
families that are well represented by temperate and boreal tree species are also best
represented in the list of examples of induced resistance provided by Karban &
Baldwin (1997). Nevertheless, these authors argued that the bias toward temperate
and boreal environments probably reflects the historical development of the field,
more than actual biological patterns.
In a survey in a tropical cerrado vegetation in Brazil, we found that plant species
of very different and unrelated taxa may resist to gall induction by eliciting HR
(Fernandes & Negreiros 2001) (Table 1). The same phenomenon was also reported
in other species: Annona coriaceae (Annonaceae), Aspidosperma tomentosum
(Apocynaceae), Baccharis dracunculifolia (Asteraceae), and Tabebuia ochraceae
(Bignoniaceae) (Cornelissen & Fernandes 1998). In all cases, HR was observed as a
round, red-brownish spot around the gall initiation site. HR also constitutes the
primary line of resistance and defense of other several unrelated plant taxa against
their major herbivores [e.g., wheat (Shukle et al. 1992, rice (Bentur & Kalode 1996,
Solidago (Anderson et al. 1989), pines (Berryman & Ferrel 1988), and Fagus
(Fernandes et al. 2002)].
6. THE EFFECTIVENESS OF HYPERSENSITIVE REACTION AGAINST

GALLING HERBIVORE POPULATIONS
During a 6 year long-term study (1993 to 1998), in which more than 17,000 shoots
ofBauhinia brevipes and more than 19,000 Contarinia galls were sampled, HR was
the most important factor affecting the population of the galling herbivore on the
host plant (Figure 2). This host-driven mortality factor was stable over time and
occurred at high frequency during these six consecutive years
and
hence leaving few galls to be found and killed by natural
enemies.
HR also constitutes the primary line of resistance in four out of eight species
studied in detail in the cerrado vegetation of southeastern Brazil (see Table 1). In
four species - Bowdichia virgilioides (Leguminosae), Byrsonima verbascifolia
(Malpighiaceae), Ouratea floribunda (Ochnaceae), Terminalia brasiliensis
(Combretaceae) - this plant resistance mechanism killed more than two-thirds of the
galling population (Fernandes & Negreiros 2001). In three out of eight species, HR
rates were approximately the same as the survivorship rates, and, in just one species
– Serjania lethalis – natural enemies such as pathogens were an important gall
mortality factor.
Fagus sylvatica is one of the most common tree species in central Europe where
it constitutes various types of beech forest and is an important element of mixed tree
forests from the lowlands up to the upper montane level. Galls induced by Mikiola
fagi Htg. (Diptera: Cecidomyiidae) and Hartigiola annulipes Htg. (Diptera:
Cecidomyiidae) and brown spots resembling hypersensitive reactions are very
conspicuous and common on the leaves of Fagus sylvatica L. in the forests
surroundings Darmstadt, Germany (Fernandes et al. 2002). Most attempts to induce
galls on F. sylvatica resulted in failure due to HR (77%), therefore leaving few live
galls to be found by natural enemies, including parasites, pathogens and predators of
the gall tissue. Only 15% of the galls of the two galling species survived in the
studied population. Once again, HR was the most important factor acting against
the galling population.
These data corroborate the view that in galling insect-host plant system
interactions plant-driven factors may play a major role in determining herbivore
failure and success and perhaps in the resulting community structure.
7. TOP-DOWN OR BOTTOM-UP EFFECTS IN INSECT-PLANT

INTERACTIONS ?
The debate regarding the regulation of natural communities has shifted from arguing
whether regulation is bottom-up (plant-driven) or top-down (natural enemy-driven),
to deciphering how these forces interact and when one force or other has primacy
(Clancy & Price 1986, Preszler et al. 1996, Carson & Root 2000). There is much
accumulated information showing that predators and parasites often keep insect
herbivores from causing major damage to their host plants (e.g., Marquis & Whelan
1994, Schmitz et al. 1997), although other studies showed that plant nutritional
quality and the amounts of secondary compounds prevents insects to fully exploit
their hosts (e.g., Crawley 1989, Hartley & Jones 1997). Our studies have shown that
effects driven by the host plant, such as hypersensitivity, strongly influenced many
galling insects in the absence of other factors, such as the effects of predators and
parasites. Generally, natural enemies exerted weak mortality pressure upon the
galling herbivores (e.g., Cornelissen & Fernandes, 1998, Fernandes et al. 2000,
Fernandes & Negreiros 2001).
The explanation for the paucity of examples of this host-driven mortality factor
is that studies may have missed hypersensitivity because necrotic spots frequently
seen on attacked leaves may have been treated erroneously as spots caused by
pathogens (Fernandes & Negreiros 2001). Therefore, many life tables of galling
insects may have overestimated the effects of mortality caused by natural enemies.
The inclusion of plant resistance mechanisms in life tables of gallers may offer an
interesting way to observe the strength of induced resistance, such as HR, on the
dynamics of insect herbivores population.
8. ARE PATTERNS OF PLANT ATTACK AND RESISTANCE

PREDICTABLE?
For many plants, resistance against herbivores is a transient trait rather than a fixed
one (Tallamy & Raupp 1991, Karban & Adler 1996). Why are plant resistance and
defense sometimes inducible? Most of the models proposed to answer this question
assume that resistance to herbivory is costly to the plant, and induced traits allow the
plant to save costs when herbivores are absent. This cost of defense, together with
the unpredictability of herbivore attack may explain why some plants have evolved
inducible resistance systems.
Karban & Adler (1996) stated that if herbivory is completely predictable, then
plants should present and evolve constitutive defenses. On the other hand, if
herbivory is completely unpredictable, then plants might also evolve a level of
constitutive defense that is best on average conditions. Herbivory that is not
completely predictable might favor plants that have inducible resistance, but only if
bouts of herbivore attack are correlated for an individual over time. Induced
resistance will be favored only if herbivory (or a cue of herbivory, such the
oviposition of galling insects) to which a plant responds is a predictor of future

attack by herbivores.
An inducible strategy could also be favored if a plant experiences only one
constant regime if that regime is not predictable. This may be the case of B.
brevipes when it resists the attack of its most common galling insect, Contarinia,
through the expression of HR against gall formation. Contarinia galls are induced
at the beginning of the rainy season (November/December) and develop until
March. At the beginning of the dry season (May) B. brevipes loses all its leaves.
Although this species experiences a constant regime of galling attack, its intensity is
not predictable. Corroborating this, the mean number of galls per plant induced in
the previous year was a very poor predictor of the number of galls induced in the
following year, from 1993 to 1998, at an individual basis (Figure 3).
On the other hand, plant resistance is highly predictable at an individual basis.

HR killed more than 90.0% of Contarinia galls during six years. When we divided
the 170 studied plants into two categories of resistance (resistant plants: > 90% of
the galls killed by HR and susceptible plants: < 75% of the galls killed by HR), we
observed that most plants were resistant from 1995 to 1998 (Figure 4). Moreover,
plants that were resistant in the previous year were still resistant in the next one (see
also Cornelissen & Fernandes 1998).
Previous models of inducible strategies of defense in plants have indicated that
the information content of the environment has the potential to determine whether
constitutive or induced resistance is favored. Past or current herbivory is the most
direct cue about future herbivory. Nevertheless, for this cue to provide reliable
information, past herbivory must be a good predictor of future herbivory (Karban et
al. 1999). In the system Bauhinia-Contarinia the unpredictability of gall induction
associated with the strong efficiency of hypersensitivity may select inducible
systems of plant resistance.
9. FUTURE FOCUSES
We have just begun to examine the phenomenon of induced resistance through
Hypersensitive Reaction and to provide some contributions to the understanding of
some aspects that involves galling insects and their host plants. Future studies
should provide the fuel to address the questions related to the chemicals involved in
the expression of HR, plant memory to the attack by galling herbivores, pathogen
mediation in the expression of HR, environmental effects (such as plant nutrition,
water and chemical contents) on the expression and frequency of HR, and how can
this mechanism of plant resistance could lead to local and regional patterns in gall
diversity.
ACKNOWLEDGMENTS
We thank C Jacobi and Tim Paine for comments and criticism. Logistical support was
provided by Estação Ecológica de Pirapitinga, Parque Nacional da Serra do Cipó, and Estação
Ecológica da Universidade Federal de Minas Gerais. The project was supported by CNPq
(52.1772/95-8), FAPEMIG (Cra 2519/97), and by the Graduate Program in Ecologia,
Conservação e Manejo de Vida Silvestre / Universidade Federal de Minas Gerais. TG
Cornelissen also acknowledges CNPq (process number 200064/01-0) for a PhD scholarship
at USF.
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CHAPTER 7
THE RESISTANCE OF HYBRID WILLOWS TO

SPECIALIST AND GENERALIST HERBIVORES
AND PATHOGENS: THE POTENTIAL ROLE OF
SECONDARY CHEMISTRY AND PARENT HOST
PLANT STATUS
JOAKIM HJÄLTÉN AND PER HALLGREN
Department of Animal Ecology, Swedish University of Agricultural Sciences, S-901 83 Umeå,

Sweden. E-mail joakim.hjalten@szooek.slu.se
INTRODUCTION
Interspecific hybridisation has shown to be more common than assumed some
decades ago (Hewitt 1988, Harrison 1993, Arnold 1997). The novelty of the
genotypes resulting from hybridization makes them interesting organisms for
evolutionary studies. Recently, hybrids and hybrid zones have been used to address
ecological and evolutionary questions regarding plant resistance to pests and host
shift by herbivores (Whitham 1989, Strauss 1994).
Whitham (1989) found that the densities of aphids were much higher in the
hybrid zone between two cottonwood species than in the zones with pure individuals
(see also Floate et al. 1993). Based on this observation, he suggested that the genetic
re-arrangements, which occur during hybridization, will result in a break down in
plant resistance against herbivores. This hypothesis assumes that defensive traits in
plants are based on a delicately balanced arrangement of genes that have evolved as
a result of selective pressure by herbivory. However, more recent studies have
sometimes revealed contradictory results, ranging from reports of herbivore densities
being similar to one parental species or intermediate between the parental species
(Boecklen and Spellenberg 1990, Aguilar and Boecklen 1992, Fritz et al. 1994,
1996a, Gange 1995, Messina et al. 1996), or occasionally even lower on hybrids
compared with pure individuals (Boecklen and Spellenberg 1990). This lead to a
153
154 J. HJÄLTÉN and P. HALLGREN
question of whether the observed differences were due to genetic factors or

environmental variation, e.g. environmental gradient in the hybrids zone and
microsite differences (Boecklen and Spellenberg 1990, Strauss 1994). Consequently,
it has been stressed that experiments should be conducted under controlled
environmental conditions (Strauss 1994, Fritz 1999).
Of course, we should not expect all herbivores to respond in a similar way to
hybrid plants. For this to occur we would have to assume that all traits that influence
plant palatability to herbivore will show the same inheritance pattern in hybrid plants
and that all herbivores will respond in a similar way to these changes (for further
discussion see Orians et al. 1997). Knowing that herbivores often have adapted to
very specific traits in their host plants, the latter assumption seems unlikely. Thus,
rather than argue whether or not hybridization will result in a breakdown in
resistance or any other response, emphasis should be placed on explaining the
mechanism behind the intraspecific variation in herbivore response to hybrid plants
(Hjältén et al. 2000). To understand and predict the outcome of plant hybridization
with respect to the response of specific herbivores, we must consider factors that
influence host choice in these herbivores.
Interspecific hybridisation is a genetic process, and most genetic hypotheses of
how hybridization affect plant resistance to herbivores consider how resistant traits
are inherited (additive or dominant) and how herbivores respond to these changes
(linear or threshold response, see Fritz 1999 for further discussion).
The most important resistance characters in many plant groups are secondary
compounds. For example, insect distribution on willows (Salicaceae) is strongly
influenced by phenolic secondary metabolites (Rowell-Rahier 1984, Tahvanainen et
al. 1985b). In most cases, these compounds act as repellents for herbivores, but for
specialist herbivores, they could act as attractants (Pasteels et al. 1982, Tahvanainen
et al. 1985b, Kolehmainen et al. 1994). Changes in secondary chemistry following
hybridization might provide the pre-requisite for differences in palatability between
hybrids and parental species.
There are striking differences in the secondary chemistry of different willow
species and this affects their herbivores. One group of species, e.g. Salix caprea, S.
aurita and S. viminalis, contain high concentrations of condensed tannins (generally
known to reduce protein uptake in herbivores) in their leaves, but low levels of
phenolic glucosides (known to sometimes have toxic effects) (Julkunen-Tiitto 1989).
These species are generally relatively palatable to both mammals (Tahvanainen et al.
1985a, Hjältén 1991, 1992) and polyphagus insect herbivores, such as the
chrysomelids Phratora vulgatissima, Galerucella lineola and Lochmaea caprea
(Rowell-Rahier 1984, Price and Martinsen 1994, Hjältén 1997). The other group of
willows, e.g. S. repens, S. triandra and S. pentandra, contains high concentrations of
phenolic glucosides, but low concentrations of condensed tannins (Julkunen-Tiitto
1989). These willows are often less palatable to mammals (Tahvanainen et al.
1985b, Hjältén 1991) and many polyphagus insect herbivores, for example
Lochmaea caprea, Phratora vulgatissima and Galerucella lineola, but can be
utilised by more specialist insect herbivores, such as galling sawflies and specialist
HYBRID RESISTANCE TO HERBIVORES AND PATHOGENS 155
leaf-beetles such as Phratora vitellinae and Plagiodera versicolora (Hodkinson et

al. 1998, Kendal and Wiltshire 1998). In many cases, the larvae of these specialist
chrysomelid species use these substances to defend themselves against predators
(Rowell-Rahier 1984, Pasteels et al. 1982, Orians et al. 1997, Rank et al. 1996). In
addition, phenolic glucosides have been shown to attract and trigger oviposition by
galling sawflies (Soetens et al. 1991, Kolehmainen et al. 1994, Roininen et al. 1999)
The fact that secondary chemicals might act as attractants for some herbivores
(mainly specialists) and repellents for others (generalists) could indicate that we
might expect generalists and specialists to respond in different ways to hybrid plants.
Specialists, for which phenolic glucosides act as attractants, have been suggested to
respond to changes in phenolic glucosides in a threshold manner. That is, if the
concentration of phenolic glucosides or some other plant traits go below some
minimum threshold, the plant will no longer be recognised as a host plant
(Moorehead et al. 1993). By contrast, secondary compounds act as deterrents for
generalist herbivores and we might, therefore, expect these herbivores to respond in
a different way compared to specialists.
Thus, the response of specific herbivores to hybrid plants is likely to depend on
the secondary chemistry of the parental plants. However, as discussed above, the
inheritance patterns of secondary compounds in hybrids is also essential for hybrid
palatability. Few attempts have been made to determine the inheritance patterns of
secondary compounds in F1 hybrids of willows. Orians and Fritz (1995) reported an
additive inheritance pattern of condensed tannins and two phenolic glucosides in the
F1 hybrids between S. sericea and S. eriocephala, but see also Orians et al. 2000.
Häggström (1997) found a similar pattern for the phenolic glucosides in the F1
hybrids between S. viminalis and S. dasyclados but they also found indications of
hybrid heterosis, with concentrations of three unidentified phenolic glucosides
exceeding the sum of the concentration in the parental species.
Plant resistance to parasitic fungi seems to be less influenced by secondary
chemicals. Studies have shown no, or very weak correlations between the
concentration of secondary chemicals in willows and resistance against fungal
infection (Hakulinen 1998). Studies on rust fungi, Melampsora sp., on various
willow systems show that, in general, hybrids are more infected than the parents
(Fritz et al. 1994, Roche and Fritz 1998, Hjältén 1998). However, Gaylord et al.
(1996) and Fritz et al. (1996b) have reported intermediate densities of fungi on
hybrid plants.
Most studies on hybridisation and herbivores only consider hybridisation
between two plant taxa. Thus, no attempt has been made to compare the response of
specific herbivores or functional groups of herbivores to hybrids with closely related
or distantly related parent taxa. For example, no earlier studies have tried to evaluate
the importance of parent host status for hybrid susceptibility to herbivores.
The aim of this study was to detect general patterns in the response of different
groups of herbivores and parasitic Melampsora sp. fungi to hybrid plants. To
achieve this goal, we compiled the data from several studies of hybrids-herbivore
interactions in different willow hybrid systems. Furthermore, we determined the
inheritance pattern of resistant traits, e.g. secondary substances to evaluate if this, in

combination with parent host plant status, can explain herbivore response. The
following questions were addressed.
1) Do the patterns of herbivore response to hybrid plants differ among different

herbivore groups, i.e. specialist gallers and generalist leaf-beetles or parasitic
fungi (Melampsora sp.)
2) If patterns differ, can we explain these differences based on the inheritance

pattern of resistant traits and the response of gallers versus leaf-beetles to
changes in specific resistance characters?
METHODS
In this study we compile data from 21 tests of herbivore response to hybrid plants
and parental species. The study system and methods are described below.
STUDY SYSTEM
Hybridisation is very Common in boreal willows (Salix spp; Lid and Tande Lid
1994). In addition, willows play an important role as host for many species of insect
herbivores. This makes this system very suitable for studying the response of natural
enemies to hybrid plants.
The tree-forming S. caprea L., the bush forming S. aurita L. and the creeping S.
repens Sm. (L.) were used in this study. S. caprea and S. aurita are closely related
and are believed to hybridise quite commonly (Lid and Tande Lid 1994). Similarly,
S. caprea and S. phylicifolia are also relatively closely related and are believed to
hybridise relatively commonly. S. caprea and S. repens are more distantly related
and occasionally hybridise (both species flower from May to early June) with each
other as well as with other willow species (Lid and Tande Lid 1994). These species
differ in their habitat requirements: in the northern part of Sweden S. caprea occurs
in relatively wet, rich habitats, S. aurita occurs in bogs, whereas S. repens mainly
occurs on sandy shores and ditches (Lid and Tande Lid 1994, Mossberg et al. 1993).
Leaf-galling and leaf-folding sawflies of the sub-genera Pontania and
Phyllocolpa (Hymenoptera: Tenthredinidae) are common on many willow species
and are often monophagous (Kopelke 1991, Zinojev 1995). The adult females
emerge in spring, oviposite in developing leaves, and a gall is formed. The larvae
feed inside the gall until late autumn when they go into the ground to pupate. Most of
the species have only one generation per year (Pschorn-Walcher 1992). Leaf-galling
and bud-galling midges (Family Cecidiomyiidae) are also common on willows and
many species are highly specialised.
Willows serve as hosts for numerous species of leaf beetles (Chrysomelidae).
Many of them utilise more than one host plant, but some are monophagous (Jolivet
1988, Koch 1992). For the preference tests, two leaf beetle species were used,
Lochmaea caprea L. (Coleoptera: Chrysomelidae: Galerucinae) and Crepidodera

fulvicornis Fabr. (Chrysomelidae: Halticinae). Both of these species are commonly
observed on wild willows in this area (S. caprea, S. aurita, and S. phylicifolia), as
well as on our experimental willows in the common garden (pers. observation, see
plant material section). Crepidodera fulvicornis are oligophagus on the genera Salix
and Populus and Lochmaea caprea are oligophagus on the genera Salix, Populus
and Betula. Both species are phytophagous both as larvae and as adults (Koch 1992)
and only have one generation per year at this location. It should be noted that none
of these chrysomelid species are reported to prefer willow species with high
concentrations of phenolic glucosides (Tahvanainen et al. 1985b, Koch 1992).
Parasitic fungi (Melampsora spp.) are very common on willows and poplars.
Severe infections can have a very detrimental effect on plant growth and survival
(Royle and Ostry, 1995).
PLANT MATERIAL
To control the plant material used and minimise the influence of environmental
differences, F1 hybrids and parental species were produced by hand-pollination of
willows in the field. In addition, the plants were potted and kept in an experimental
field under controlled conditions. Four willow species were used. Salix caprea were
crossed with S. repens, S. aurita and S. phylicifolia. The plants used were all found
within a 20 km radius of the city of Umeå in northern Sweden (63°44’N; 20°18’E).
The hand-pollination was performed in 1995, 1996 and 1997. Three catkins on
each female willow clone were bagged, using nylon stockings. To test the reliability
of the method, one catkin received pollen from one male individual of the same
species, one received pollen from the other willow species, and the third catkin
received no pollen. However, the bag was removed from the latter for as long a
period of time as it took to pollinate the other catkins, i.e. approximately one minute.
In no case did the unpollinated catkins produce seed.
The seeds were collected in late June, germinated and planted in 5-litre pots
containing standard peat-soil. The pots were kept in the greenhouse with no
additional artificial light at 20°C until late July-early August, when they were moved
outdoors to an experimental field. During late summer they received water with
added nutrients twice a week (standard liquid fertiliser “SuperbaS”; 10ml/l; NPK
6,5-1.0-4,7) (for further details see Hjältén 1997, 1998, Hjältén et al. 2000).
PREFERENCE TESTS
The preference tests were conducted in 1995, 1996 and 1997, using seedlings
produced in the test year. Beetle preference was determined in multiple-choice tests,
conducted in late August and early September. To minimise the influence of leaf
phenology, which is known to influence leaf palatability (Raupp and Denno 1983,
Floate et al. 1993), the third (1995) or fourth (1996, 1997) leaf from the top of the
main shoot was used. The preference test was started immediately after leaf
collection. In 1995 and 1996 one leaf of each taxon was placed in a petri dish lined
with a moistened filter paper to reduce water loss. One leaf beetle was placed in the
dish and, after a specified duration, the amount of leaf area consumed from each of
the different taxa was measured (see Hjältén 1997 for a further description). In 1997,
we used the same method, except the leaf size was standardised by using leaf discs
one in size. In addition, the hybrids of S. caprea and S. aurita were separated
into two categories: one with S. caprea and one with S. aurita as the pollen donor.
Therefore, four leaf discs were presented to each leaf beetle. The aim here was to
examine maternal and paternal effects on plant resistance. However, we found no
indication of any such effects and a mean value for these two hybrid categories was
therefore used in all statistical analyses. The preference tests were performed under
natural light conditions, at 20°C. No individual beetle or individual plant was tested
more than once.
FIELD SURVEY
In late August 1995, 1996 and 1997, plant height, leaf number, and densities (total
number of insects per plant/total leaf number per plant) of the leaf-galling sawflies
Pontania pedunculi (A. Zinojev pers com.) and Pontania bridgmanii (H. Roininen
pers com.) were determined on the potted willows. These species commonly occur
on S. caprea (Coulianos 1991, Zinojev 1995). In addition, we determined the
densities of adult Crepidodera fulvicornis (Chrysomelidae), chrysomelid larvae, the
leaf-galling midge Iteomyia capreae, the bud-galling midge Dasineura rosaria, and
the parasitic fungus (Melampsora sp.) on the willows. Ten individuals (seven in the
case of S. caprea) from each plant category were randomly selected for determining
the degree of rust infection and leaf size (Lambda LI-3000 portable area meter). Ten
leaves were collected from each individual, giving a total of 100 leaves from S.
repens, 100 from the hybrids and 70 from S. caprea. The proportion of leaves
infected and the
degree of infection were used to
calculate a rust score (proportion of leaves infected*degree of score)
reflecting the impact of the rust infection on plant growth and general health (for
method, see Schreiner 1959). The method was slightly modified so that uninfected
plants could also be included. The score for these was set to zero.
CHEMICAL ANALYSIS
The material for chemical analysis was collected in 1996. To reduce the impact of
leaf phenology on leaf chemistry, we standardized the collection method. The fifth
and sixth leaves from the top of the main shoot were collected at the same time as we
collected the leaves for the preference tests. For S. caprea, S. repens and their F1
hybrids, the leaves were collected from 10 randomly selected individuals. For S.
caprea, S. aurita and their F1 hybrids, leaves were collected from 20 randomly
selected individuals of each parent species and from 30 F1 hybrids, half with S.
caprea and half with S. repens as the pollen donor. The leaves were freeze-dried
immediately and stored in the freezer prior to analysis. For the analysis of condensed
tannins, 0.1g plant material was extracted with 1ml 80% ethanol, in an ultrasonic
bath for 15 minutes. The aliquot was then analysed according to the
proanthocyanidin method (Waterman and Mole 1994). Due to the problem of finding
appropriate standards for condensed tannins, we chose to present our results as
absorbance values (Waterman and Mole 1994).
RESULTS
The results from all the field surveys, preference tests and chemical analyses are
presented in Table 1 and the patterns for gallers and leaf beetles are summarised in
Figure 1. The most common pattern (46% of all cases) for leaf beetles was that no
significant difference in utilization was found between any of the plant categories
(Table 1, Fig. 1). In 27% of the cases, hybrids were consumed to the same degree as
the most susceptible parent, and in 18% of the cases the leaf beetles consumed an
intermediate amount of biomass from hybrids compared to the parent species (Fig.
1). However, the pattern for gallers differed from that of leaf-beetles. The densities
of gallers on hybrid plants were generally consistent (60% of the cases) with the
densities on the most susceptible parent. In 20% of the cases, we found no difference
between the taxa, and in 10% of the cases we found an additive response. It should
be noted that in no case did our results support either the resistance or the
susceptibility hypotheses. The response of herbivores and the Melampsora rust did
not follow the same pattern. Hybridisation resulted in a breakdown in the resistance
of Fl hybrids to the Melampsora rust. However, a reconstitution of resistance
occurred in the back crosses, suggesting an additive inheritance of resistance traits
(Figure 2.).
The inheritance patterns of condensed tannins in the S. caprea x S. repens
crosses can best be described as additive; that is, hybrid plants had intermediate
concentrations of phenolics compared to the parental species (Table 1). We found no
significant differences in the concentration of condensed tannins between any of the
plant taxa in the S. caprea x S. aurita crosses, but there was an indication that
hybrids were intermediate between the parents.
DISCUSSION
Densities of herbivores and pathogens on plants can be influenced by both genetic
and environmental factors (Kearsley and Whitham 1989, Boecklen and Spellenberg
1990, Floate et al. 1993, Strauss 1994, Hjältén and Price 1996, Waltz and Whitham
1997). In the present study, the effects of confounding environmental variation
should have been minimised since all plants were of the same age, potted, and
growing under similar conditions in an experimental field. Thus, the results reported
should mainly reflect genetic differences between plant taxa.
The response to hybrid plants seemingly differed between gallers and leaf-
beetles. The most common pattern for gallers was dominance towards the most
susceptible parent, whereas the most common pattern for leaf beetles was that no
difference in utilisation was found between any of the taxa.
One possible explanation for this pattern is that gallers, compared with the leaf
beetles used in this study, have a much more narrow host range. Both Pontania
pedunculi and P. bridgmanii occur on S. caprea and a few closely related willow
species, S. aurita and S. cinera and, in the case of P. bridgmanii, also on S.
phylicifolia (Benes 1968, Vikberg 1970, Coulianos 1991, Zinojev 1995). Compared
to the gallers, the leaf beetles used in this study have a broader host range.
Crepidodera fulvicornis are oligophagus on the genera Salix and Populus, and
Lochmaea caprea are oligophagus on the genera Salix, Populus and Betula.
However, these species generally show less preference for willows species with high
concentrations of phenolic glucosides (Tahvanainen et al. 1985b). Thus, the high
percentage of cases where no difference in leaf-beetle consumption could be found
between any of the plant categories could simply be due to a wider host range of the
leaf beetles.
In contrast, the most common pattern for gallers, dominance towards the most
susceptible parent, can possibly be explained by the specific host selection
mechanisms in gallers. In gallers, specific plant phenolics seem to act as attractants
for galling sawflies, whereas they act as deterrents for the generalist leaf beetles used
in this study. Phenolic glucosides have been shown to trigger oviposition in galling
sawflies (Soetens et al. 1991, Roininen et al. 1999). If gallers respond to plant traits
at specific thresholds, as has been reported in earlier studies (Moorehead et al. 1993,
Fritz et al. 1994, Fritz et al. 1996a, Messina et al. 1996), this could potentially
explain our result. This is because if the concentration of secondary metabolites in
hybrids is sufficiently high for the sawfly to recognise it is at a host plant and thus to
trigger oviposition in sawfly females, we should expect a dominant response towards
the susceptible parent.
Moorehead et al. (1993) found that a cynipid gall-former recognised hybrids
exhibiting only 15% of the host plant characters. We found an additive inheritance of
secondary compounds, i.e. condensed tannins, and unpublished data from our S.
caprea*S. repens crosses also show an additive inheritance pattern of specific
phenolic glucosides in hybrid plants (Hallgren et al. in prep.). This indicates that the
hybrids might contain sufficient amounts of secondary metabolites to be accepted as
host plants.
These results are also consistent with earlier studies of hybrid chemistry in
willows. Although very few earlier studies have been conducted, the most common
pattern is additive inheritance; that is, hybrids generally contain intermediate
concentrations of phenolic compounds compared with the parent species (Orians and
Fritz 1995, but see also Häggström 1997). Orians and Fritz (1995) reported an
additive inheritance pattern of condensed tannins and two phenolic glucosides in the
F1 hybrids of Salix sericea and S. eriocephala. This situation is similar to that of our
S. caprea*S. repens system, since S. sericea has high concentrations of phenolic
glucosides and low concentrations of condensed tannins, and the reverse is the case
for S. eriocephala. However, Orians et al. (2000) found that the production of 2´-
cinnamoylsalicortin appeared to be controlled by one or more recessive alleles.
Thus, it is possible that the difference between gallers and leaf beetles is due to
the more limited host range in gallers, and that phenolic glucosides act as attractants
in gallers, but deterrents in leaf-beetles. However, it should be noted that there is
considerable variation within these herbivore groups. For example, P. bridgmanii
utilised S. caprea, S. phylicifolia and their hybrids to the same degree. Furthermore,
D. rosaria response to S. caprea, S. repens and hybrids was either additive, or
densities did not differ between the plant taxa. One other difficulty with these data is
that preference tests were generally used for leaf-beetles whereas field experiments
were used for gallers. This might have influenced the results and made comparisons
more difficult. Still, we hope that the results from this compilation of data will
provide some background for future studies.
Although we found no example of increased susceptibility to insects, the hybrids
between S. caprea and S. repens were highly susceptible to infection by the parasitic
fungi (Melampsora sp.) Other studies (Gaylord et al. (1996), Fritz et al. (1996b))
have reported intermediate densities of fungi on hybrid plants. However, several
studies have also reported an increased susceptibility of hybrid plants to parasitic
fungi, both for a smut (Ericson et al. 1993) and for an unidentified yellow spot
disease (Whitham et al. 1994). Studies of rust fungi, Melampsora sp., on various
willow systems, in general show that hybrids are more infected than the parents
(Fritz et al. 1994, Roche and Fritz 1998, Hjältén 1998 but see also Fritz et al.
1996b). However, Hjältén et al. (2000) found no difference in the resistance of S .
caprea, S. phylicifolia or their F1 hybrids for another type of parasitic fungus, the tar
spot disease Rhytisma salicinum. Still, a breakdown in rust resistance in hybrid
plants, as found in the present study, could reflect a severe disruption of the
resistance traits by the genetic re-arrangement in hybrids. Furthermore, fungal
pathogens can have a very strong negative affect on plant growth and survival, and
predispose plants to infections by secondary organisms (Royle and Ostry 1995).
Accordingly, there should be strong selection pressure for resistance against fungal
pathogens, which could place hybrids at a selective disadvantage.
ACKNOWLEDGEMENT
We thank Åke Nordström for assistance in the field. Financial support was provided
by the Swedish Council for Forestry and Agricultural Research (JH).
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CHAPTER 8
DEPLOYING PEST RESISTANCE IN

GENETICALLY-LIMITED FOREST PLANTATIONS:
DEVELOPING ECOLOGICALLY-BASED
STRATEGIES FOR MANAGING RISK
DANIEL J. ROBISON
Hardwood Research Cooperative

Department of Forestry, North Carolina State University
Raleigh, NC 27695 U.S.A.
1. INTRODUCTION
Genetically-based tree resistance to agents of stress, when purposefully deployed in
forestry operations is accomplished in plantations of limited genetic diversity, and
increased cultural inputs. Genetic diversity is limited due to, 1) the need to focus the
planting efforts on stock containing the desired growth and performance traits,
including resistance factors, and 2) as compared to natural stands or planted seedling
origin stands where there were no, or limited, selection criteria for resistance and
other traits. Cultural inputs are increased due to the need to secure the investment
made in developing and deploying resistance, and the likelihood that such
plantations will be on the best sites with fertilization, weed management and other
silvicultural activities. Both of these factors, genetic and cultural, can reduce the
resiliency of plants to stress, especially pest depravations (Heinrichs 1988; Panda
and Khush 1995).
These will also be plantations with high productivity (= shorter rotation lengths)
and product expectations. All of these factors tend to lower the economic injury
level, and necessitate economically viable means to manage biological risk. To do
so effectively and sustainably requires an ecologically-based approach (NRC 1996).
This is also true if such operational forest systems are to be environmentally
acceptable (in the socio-political sense) (Sedjo et al. 1998). The challenge is to
169
170 D. ROBISON
deploy highly productive forest trees that will sustainably resist and/or tolerate
attacks from known and future pests (and other stress agents), over multiple years
and rotations, on a relatively low value crop.
Worldwide there is significant environmental and ecological concern about the
use of exotic, genetically-limited (especially clonal) and -engineered, and intensive
plantation systems (Abrahamson et al. 1998; Cannell 1999; EPRI 1995; James et al.
1998; Powers 1999; Ranney and Mann 1994; Stelzer and Goldfarb 1997). To
answer these challenges will require ecologically-based approaches, which can
satisfy, 1) the need to create ecologically stable forest production systems, and 2)
environmental scrutiny (Binkley 1997; Boyle et al. 1999; Friedman and Foster
1997; James et al. 1998; Powers 1999; Tuskan 1998). These factors need not be
opposing. Forest plantation systems that are stable, productive and secure (protected
from agents of stress) are the goal of forest managers, for both silvicultural and
ecological-environmental reasons. Such systems, when properly defined and
substantiated, should satisfy environmental skeptics as well.
Deployment of tree resistance to pests is a relatively new silvicultural tool. It
requires an understanding of pest issues, and a proactive approach (Robison and
Raffa 1998; Smith and McSorley 2000; Wingfield et al. 1991; various authors in
this volume). It is only within the past several decades that wide-scale deployment
of resistance in forestry has been used, and almost entirely against diseases (Carson
and Carson 1989; Chou 1981; Gibson et al. 1982; Lo et al. 1995; Newcombe 1998;
Redmond and Anderson 1986; Zobel 1982). While there have been very successful
uses of this approach (Alfaro et al. 2000; Pei et al. 1997; Pye et al. 1997; Wingfield
et al. 1991; Zobel 1982; Zsuffa 1975), it is not clear that they have been based on
sufficient ecological information to provide continued confidence as forests become
increasingly intensively managed, more genetically-limited, and product values rise.
For insect pests, most operational activities are reactive, through the use of
insecticides, biocontrol or subsequent breeding for tree resistance. Deployment is
proactive, and while intuitively obvious, its ecological basis is not simplistic. The
nature of tree-pest interactions is fundamentally complex, involving many stochastic
elements, including genetic, environmental and multi-trophic interactions, and pest
life history characteristics (Altieri 1994; Berryman 1988; Kennedy et al. 1987;
Manion 1981; Riggin-Bucci and Gould 1997; Rao et al. 2000; Smith and McSorley
2000).
Genetic resistance to agents of stress is purposefully developed in tree species
through the iterative processes of tree selection, breeding and propagation (Zobel
and Talbert 1984). With each improvement cycle, the individuals propagated either
sexually or vegetatively, become increasingly genetically-limited as compared to the
initial natural and/or breeding population. In the most extreme form, cloning, all
individuals propagated from a single elite clone are genetically identical. With
either a seed based (sexual) or vegetative (clonal) propagation system, the goal is to
capture genetic gain (improvement), and as a consequence the variation among
individuals is narrowed. With a seed based system, each breeding cycle should
advance the mean response (productivity, resistance, etc.), and perhaps reduce the
amount of variation about the mean. In a clonal system, all propagules perform (for
DEPLOYMENT IN GENETICALLY-LIMITED PLANTATIONS 171
all practical purposes) exactly like the elite selection from which they were derived.
However, among a group of selected clones, there can be considerable variation of
many traits.
The effect of “improving” and narrowing the genetic base of trees in plantation
systems is to make production more efficient. This is a good thing. However, the
consequence is that the capacity of the forest system to withstand the vagaries of the
natural world, including biotic and abiotic stresses, may be compromised (Carson
and Carson 1991; Gibson and Jones 1977; Park et al. 1998b; Wilson 1977).
Landscape-level issues, such as the impact of these forests on biodiversity and
ecosystem health, are also of concern (Abrahamson et al. 1998; Cannell 1999;
Chapin et al. 1998; Greenberg and McGrane 1996; Powers 1999). These are the
challenges that confront the deployment of resistance. These challenges are
particularly evident in clonal systems, and when coupled with operational desires for
a limited number of genetic entities (clones or families) (Carson and Carson 1991).
Additionally, silviculturists often want genetic entities as individually robust as
possible, in order to use them in a variety of situations, thereby promoting the use of
fewer such entities and a narrower genetic base on the landscape.
2. CHARACTERIZATION OF STRESS FACTORS

The two fundamental types of stress agents, for which resistance may be deployed,
are abiotic and biotic. They differ fundamentally in the nature of their interactions
with trees, and how deploying resistance against them may be best accomplished.
Abiotic Stress – such as drought, flood, cold, wind, soil factors - -
While they can exert strong genetic selection pressures on trees, there is no
feedback from the trees to the stress.
Stable (ecologically-based) resistance against such stresses can be deployed by
selecting genetic entities which are robust in their tolerance and resistance.
The value of the resistance/tolerance should not change or erode with time (it is
stable), unless the stress becomes more severe.
Biotic Stress – such as insects and diseases - -
There can be strong genetic feedback/interaction between the biotic agents and
the trees, and vice versa.
Pest generation times are invariably shorter than trees, no matter how short tree
rotations are, thereby providing ample time for natural selection to affect pest
population genetics.
Durable tree resistance (stable, ecologically-based) requires genetic buffering,
and is based on the nature of the biological interactions between the trees and
the pests.
For a stable system, the type and diversity of resistance mechanisms (and
tolerance) must be known, and deployed in such as way as to maintain its
efficacy despite strong genetic interactions.
New biotic stresses, such as exotic pest arrivals, can emerge.
172 D. ROBISON
To manage abiotic stress through resistance deployment is therefore a

straightforward task - - select and deploy robust mechanisms of tolerance and
resistance. Managing biotic stress agents, however, requires careful consideration of
interactions between the trees and the pest populations (Carson and Carson 1991;
Gadgil and Bain 1999). The key features are:
1) Deployed resistance may be overcome by emerging pests not yet recognized.

2) Very intensive pest pressures may overwhelm the resistance.
3) Pest populations may evolve into new biotypes able to overcome the resistance.
4) the nature of the deployed resistance may have negative impacts on landscape-
level ecosystem functions.
The responsibility of those who manage biological risk in these systems is to

devise economically- and ecologically-viable means of dealing with these features.
All of these can at least be partly managed through the deployment of a diversity of
genetically-based resistance mechanisms. A key factor is to not deploy a single,
strong, uni-directional selective pressure (= resistance mechanism) that can through
selection move pest populations towards biotype evolution. This will hold equally
true for resistance mechanisms derived through breeding and selection for natural
traits (Carson and Carson 1991; Gould 199la; van Emdem 1991), as well as for
resistance traits acquired through genetic engineering (Gould 1998; Robison et al.
1994), as has been found for pesticide use (Mallet 1989; Metcalf 1994). These
needs must be managed within the context of multiple pests (Gadoury 1994;
Mattson et al. 1988; Robison and Raffa 1998), and tree productivity, for practical
purposes, cannot be sacrificed. When alternative means of pest control are available
(e.g., pesticide applications) there may be limited incentives (other than
ecological/environmental) to develop resistance-based approaches. When the
consequences of pest depravations or reduced productivity are economically severe,
forest managers may not want to rely on resistance alone.
To deal with these issues requires: 1) fundamental linkages between those
studying pest-tree interactions and tree genetic improvement programs; 2) the
development of ecologically-based approaches to risk management; and 3) the
development of efficient screening and testing methods for use within the context of
operational improvement and deployment. The basic concern is that genetically-
limited commercial forests, especially clonal, can be ecologically simple; and when
they are, risk is high. However, appropriate complexity can be imposed on these
systems, enhancing the likelihood of sustainability. To do this requires considerable
ecological and genetic understanding.
3. CURRENT STATE-OF-THE-ART
Through an informal worldwide email survey (July-August 2000) of selected
individuals (56 from 14 countries) involved in studying and developing pest
resistance in forest trees, and those involved in or knowledgeable of the operational
deployment of trees, the following points suggest the current state-of-the art:
- Most resistance selection and development is through generalized field screening

based on broad categories of symptoms.
- Some researchers are conducting resistance work directly with tree genetic
improvement programs; many do not follow this approach.
- There is more work with selection and development of disease resistance, than for
insect resistance.
- In some plantation systems, insects are not considered critically important, but in
nearly all, diseases are.
- Deployment of resistance is common for disease pests, but rare for insect pests.
- Most deployment of resistance is through family-level genetic mixtures, some
family-level blocks, and in some cases clonal plantings.
- Clonal deployments are increasing, but without any apparent ecological basis to
the number of clones being used.
There is no doubt that insects are of legitimate concern in forest plantation

systems. However, the relative lack of resistance development and deployment
activity for insect pests as compared to diseases, is worthy of consideration. Perhaps
disease pests have received more attention in resistance work due to: 1) the greater
apparency and persistence of their impact in time and space when they are a
problem; 2) disease resistance is perhaps easier to screen for in the field and
laboratory; 3) diseases tend to be more specialized on particular hosts than are
insects as a general rule, and therefore are more likely to be controlled by selectable
genetic resistance; and 4) there are fewer ecologically or environmentally viable
alternative controls. Whereas, insect pests are often cyclical, bioassays are more
difficult to develop due to “behavior,” life stages may differ widely in behavior and
host utilization, there is a traditional interest in biocontrol, and insecticide
approaches have been readily adopted. However, as a proactive tool in forestry, the
development and deployment of insect resistance should be an important goal.
4. RISK CONSIDERATIONS
The relationship between genetic diversity and risk is often oversimplified, through
the question, ‘how many clones (or families) are required to reduce risk?’ The
question implies that something inherent in the number of genetic entities, without
specific consideration for ecological mechanisms, can reduce biological risk. A
number of authors have written about ecological stability in genetically-limited
forest plantation systems, with and without mention of biological-mechanistic
factors (Ahuja and Libby 1993; Bain 1981; Bashir and Roberds 1999; Carson and
Carson 1991; Chou 1981; DeBell and Harrington 1993; Lambeth and McCullough
1997; Libby 1982; Park et al. 1998a, 1998b; Pei et al. 1997; Roberds and Bashir
1997; Stelzer 1997; Zobel 1993). In fact it is neither the number of clones, nor the
diversity of parentage, which is likely important. It is much more specifically, the
number of ecologically relevant mechanisms within the plantation and across the
174 D. ROBISON
relevant landscape. This should be true whether the plantation consists of two or
many clones or families.
The notion that some general number of clones or parental lines is sufficient to
manage biotype evolution of known pests, and also the emergence of new pests, is
not founded on an ecological basis. It is at the mechanistic level that pests interact
with trees, and pest populations are affected through the selection of the most fit
individuals. Stable, durable resistance, within and across rotations, in genotypic
mixtures or blocks, even when spatially and/or temporally comprised of different
clones, can only be attained with an array of resistance mechanisms (and/or
susceptibility, see below) designed to prevent strong uni-directional selective
pressures. Such an array may also reduce the probability of emergent pests (exotic
or indigenous)(Wingfield 1999) and negative impacts on the broader ecosystem, by
challenging potential pests with a diverse set of factors to overcome or adapt to, and
by maintaining genetic stability in existing insect populations which range
landscape-wide. However, the current operational question, of, ‘how many
clones?’, remains difficult to answer given our current level of understanding
(Carson and Carson 1991; Park et al. 1998b; Tuskan 1998; Zobel 1993).
The question of using blocks or more intimate mixtures of pest-resistant genetic
entities also remains difficult to answer with certainty. There are obvious
operational advantages to using blocks of moderate size, including the ability to
respond to pest problems (Zobel 1993). However, there is also considerable
evidence that intimate mixtures, when fully understood, can lead to reductions in
pest pressures for a variety of reasons, and may also reduce the likelihood of pest
depravations, emergence and biotype evolution (Altieri 1994; Carson and Carson
1991; DeBell and Harrington 1993; Nordman 1998; Rao et al. 2000; Robison and
Raffa 1997; Tuskan 1998). Recent work with short-rotation willow (Salix spp.)
biomass systems has revealed that for the management of Melampsora spp. rust,
intimate mixtures can have great benefit if the clones and pathotypes are very well
studied (Pei et al. 1997); and there may be benefits in the management of insect
pests as well (Peacock and Herrick 2000), similar to multilining in agricultural
crops. This work is worth considering as clonal forest systems expand, with regard
to insect and disease pests (McCracken and Dawson 1998; Parker et al. 1996).
Clonal systems in nature reveal a variety of spatial patterns, perhaps instructive in
making deployment decisions (see below), ranging from very large (tens-to-
hundreds of hectares) single-clone blocks (e.g., Populus tremuloides (quaking or
trembling aspen) in the western U.S.A.), to very small (thousandths of hectares)
mosaics of many clones (e.g., Vaccimium angustifolium in Maine, U.S.A.).
The problem with managing risk through the deployment of some number of
genetic entities, without knowledge of their ecologically relevant mechanisms, is
that they all may contain the very same resistance mechanism, or a suite of closely
related mechanisms. This is especially of concern across the continuum of pests as
they tend toward polyphagy. This is true even when they are selected based on field
surveys of resistance/tolerance. In trees, by species groups, generally the diversity
of resistance mechanisms is fairly conserved. The fact that plant taxonomy can be
accomplished through chemical profiling attests to the relative lack of diversity in
secondary compounds within taxonomic groups (Harborne and Turner 1984).

However, there can be considerable variation within taxonomic families of similar
compounds (Harborne and Turner 1984), such as the phenolic glycosides (Palo
1984). Thus when selecting genetic entities based on crude screens for resistance,
and then deploying some arbitrary number of those entities, they may in fact present
the pest populations with strong uni-directional selective pressures. This may lead
to pest biotype evolution, and the loss of resistance efficacy. Further, since
secondary compounds are conserved within species (Harborne and Turner 1984),
once a pest overcomes resistance through biotype formation, it may prove difficult
to return to the base population of the tree, and find novel resistance mechanisms
which can again control the pest. Even where there exists a diversity of resistance
mechanisms within a species or family, if they all have similar structure-function
relationships, cross resistance may develop, as happens with pesticide formulations
(Metcalf 1994). This may render new genetically-based resistance more difficult to
develop through traditional breeding and selection from within a base population.
Additionally, newly emergent pests, especially exotics, may more readily impact
forests having a uniform or similar set of resistance mechanisms, than if a diversity
of mechanisms has been deployed. These points suggest that stable resistance
should be deployed from the onset, to reduce the probability of damage and loss, to
maintain that low probability through many rotations and improvement cycles, and
to retain the utility of as many resistance mechanisms in a population as possible.
Therefore, the key question is not, ‘how many clones or families to deploy?’
rather it is, ‘how many ecologically active mechanisms are required to reduce risk
across generations (tree rotations and pest population cycles)?’ To answer this
requires understanding pest-tree interactions at the ecological level (at least) (Alfaro
1996; Carson and Carson 1991; Gould 1991b; Robison and Raffa 1994, 1997; Van
Zyl and Wingfield 1999; Wagner 1988), and the development of efficient screening
methods for selecting among productive genotypes. These screening methods must
be able to differentiate among resistance mechanisms, with greater discretion than
crude field screening typically allows. Understanding the biochemical and
molecular basis of resistance would provide obvious screening tools for selecting
mechanisms that would not translate into a strong uni-directional selective pressure
(Lande and Thompson 1990; McKeand et al. 1999; Wilcox et al. 1996; Williams
and Byram 2001). However, specific bioassays and symptomology may also
provide sufficient evidence for identifying an adequate array of resistance
mechanisms.
5. SELECTING AND SCREENING FOR RESISTANCE

Recalling Painter’s (1941) triangle, insects express behavioral and developmental
responses to plants, and each trait may offer a distinct opportunity to identify
specific resistance mechanisms. Tree tolerance to pest impacts should always be
considered as well. Landscape spatial and temporal patterns of resistance
deployment are superimposed on these factors. Within resistance for insects, it may
be possible to screen various life stages for behavioral and developmental responses
176 D. ROBISON
(Kennedy et al. 1987), in order to capture a diversity of resistance mechanisms. For

example, among genetic entities, families or clones, one that elicits a behavioral
aversion, and one that elicits a developmental but not a behavioral aversion, together
would represent two entities with different ecologically active mechanisms. The
likelihood that they would drive the pest population in a strong uni-directional
manner is far less than if both elicited the same response. Ideally, in the deployment
of diverse ecologically active mechanisms, adaptation to one mechanism should
reduce adaptation to another, furthering stability. There is some evidence to indicate
that such differential mechanisms (or at least a breakdown in the typical positive
correlation between insect behavioral preference and developmental performance)
may exist within tree populations for various insects (Bingaman and Hart 1992;
Jetton 2001; Leyva et al. 2000; Robison and Raffa 1994). Selection criteria based
on this approach could be worthwhile.
Field screening alone would not likely provide sufficient detail to select
differential resistance mechanisms, unless accompanied by more detailed
evaluations. These could be in the field, or in laboratory/greenhouse bioassays,
meant to differentiate behavioral and developmental resistance factors (by life
stage), among productive and field resistant trees. An analogous approach may be
feasible with disease pests, by searching for specific aspects of their disease
symptomology and/or response morphology which reveal differential resistance
mechanisms among families or clones. The relative efficiency of field screening
followed by in-vitro screening, or vice versa, has not been investigated, nor has the
probability that one or the other is more likely to accurately differentiate among
resistance mechanisms.
Given that there are multiple pests to consider (including those unrecognized),
screening techniques must be robust (Smith et al. 1994). Similar issues are found
within the pesticide industry, where initial compound screens are accomplished on a
few organisms, and when efficacy is found, more detailed screens are undertaken.
Among insects, there is some evidence to suggest that tree resistance to generalist
insects is correlated, whereas among specialized insects the search for such
correlations is often frustrated (Mattson et al. 1988; Robison and Raffa 1998;
Nordman 1998; Robison unpubl. data). It may be possible to select one or a few
robust generalists, perhaps one from each major feeding guild, and develop a screen
based on their responses. Among specialists, more individual screening is likely
necessary. For either generalist or specialist insects, when they occur in high
numbers in the field, it might be possible to observe their behavioral and
developmental interactions with the genetic entities, and select those entities which
elicit different responses in the field. When screening is to be done without high
field populations, specific bioassays with test (“model”) insects should be able to
accomplish this. Such screens may also include likely pests in native environments
that have not yet reached the location of exotic plantings. The screens could be
done under controlled conditions locally, or the tree germplasm sent to the
environment where the pest is native and screened there.
By prioritizing and generalizing among pests, operational screens can be more
readily developed. This is necessary to facilitate the efficient screening of very
many genetic entities from tree genetic improvement programs, on a

continuous/ongoing basis, and provide results which improvement programs and
silviculturists can utilize. The lack of efficient/operational screening techniques
may be one reason why insect resistance has not often been incorporated into
breeding programs. It seems fair to say that tree pathologists have worked more
closely with tree breeders than have entomologists, and therefore insect-based
resistance screens have not been adopted. The development and deployment of
resistance is in many ways a point at which genetics and silviculture merge. Screens
could be used on genetic material in the breeding populations in advance of
controlled crosses by tree breeders, to help guide their decision making, and
during/after field testing in progeny or clone trials (Zobel and Talbert 1984). It will
be essential to develop screening tools that can be efficiently used and conducted in
concert with genetic improvement efforts, otherwise they will not be well utilized.
Excellent examples of this are the United States Forest Service fusiform rust
(Cronartium quercuum (Berk.)) resistance screening program (USFS 2001), and the
eucalypt disease screening program of the Tree Pathology Cooperative Programe at
University of Pretoria, South Africa (TPCP 2001). These types of services provide
support for tree improvement efforts, outside of the context of research activities.
There are many examples of insect resistance screening programs for
agricultural/horticultural crop plants, by public agencies and private industry
worldwide, and these provide examples for extending this approach to forest trees.
Other chapters in this volume discuss resistance screening and deployment in
forestry worldwide.
6. DEPLOYMENT DECISION-MAKING
When at least two ecologically active mechanisms are identified that will not drive
the pest population towards biotype development, then, for that pest organism, a
stable system can be deployed (Figure 1). Thus two mechanisms, with non-
complimentary selective pressures, can constitute a stable, durable system.
However, this information is best coupled (most sustainably) when there is also
knowledge of gene flow within the pest population from local and adjacent areas,
and knowledge of the impact of the intensity of resistance on genetic selection and
gene frequency within the affected population (Gould 1998). This information is
rarely known, and difficult to acquire, and for practical and research purposes wise
deployment decisions including at least two opposing selective pressures is a
reasonable approach. This could translate into deploying only two families or
clones, for that pest, or group of pests (e.g., generalist folivores). This “solution” is
distant from the current standard approach, calling for some number of clones,
typically 10-30, regardless of the number of recognized pest threats.
The number of clones to be deployed, with respect to pest issues, should be
determined based upon specific tree-pest interactions, and not solely with regard to
percent loss expectations as if deploying a large number of entities guarantees
anything about their group resiliency. Deploying, for example, 20 clones from at
least five parental lineages, may result in actually less ecological stability, then
178 D. ROBISON
deploying two clones, perhaps even with the same parental lineage, known to
differentially effect one or several pests. When considering multiple pests, it will be
necessary to stack and sort resistance (at least two mechanisms per pest) among
available clones (Robison et al. 1994). The final number of clones to use will
depend on an analysis of known pests, and some accounting for the probability of
emergent pests.
For known pests, when at least two mechanisms of resistance cannot be found,
alternative strategies are genetic engineering to add a novel mechanism, and the
inclusion of susceptibility (Gould 1998; Raffa 1989). Either situation will prevent a
segment of the pest population from being driven toward the same biotype condition
as the known/existing resistance mechanism. Then, through panmixis, the pest
population will not efficiently evolve into a biotype able to overcome the desired
resistance. When no resistance can be found, then several genetically engineered
traits with different mechanisms may be a solution, or two entities - - one with the
genetically engineered trait(s) and the other without (susceptible) may be utilized.
All of these solutions should reduce the likelihood and rate of biotype evolution for
a specific pest or groups of pests, and delay emergent pests from reaching outbreak
status. The specific nature of the insect-tree ecological-genetics interactions will

provide guidance as to the relative strength of required resistance mechanisms and
the amount of susceptibility needed to devise a durable strategy (Gould 1998).
When considering the addition of an engineered trait, it could be added to an
otherwise susceptible clone, or layered on top of an already resistant clone, but
overwhelming the natural resistance, effectively making it a different clone with
respect to resistance mechanisms. In this fashion, a single exceptional clone or
family could be deployed as a set or suite of subclones/families each containing a
different array of novel and native properties, including susceptibility (Caprio 1994;
Robison et al. 1994; Tabashnik 1994; Sachs et al. 1996; Roush 1998).
Susceptibility, being the opposite of a resistance mechanism, serves pest
management through the relaxation of selective pressures which might otherwise
drive a pest population toward biotype development and loss of resistance efficacy.
In this regard, it can be an important practical aspect of preserving pest management
through deployment of resistance. Such susceptibility has also been termed refugia.
Refugia are host locations where the pest can develop without an intense selective
pressure, and coincidentally, where natural enemies of the pest can find hosts to
maintain their populations. Susceptibility / refugia have been the subject of
considerable thinking with regard to the use of genetically engineered plant systems
(Gould 1998; Raffa 1989). Here the concept is expanded to include it with a role in
managing pests in genetically-limited tree systems, even without genetic
engineering. The important feature, without regard to the origin of resistance, is the
intensity of the selective pressure and the role susceptible hosts can play in
mitigating biotype evolution. Of course the negative aspect of susceptibility is the
potential loss of the susceptible individuals. When plantation stocking issues
dominate due to such losses, then searching for two or more mechanisms of
resistance may be more rewarding than using susceptibility as a means to minimize
biotype development.
Whether the plantation system is of native or exotic species, emergent pests,
especially exotic ones, are ultimately more likely to prosper when the tree system
presents a lack of resistance diversity. While there has been great success with
exotic forests (Gadgil and Bain 1999), there is enormous potential for devastating
pest arrivals (Kliejunas et al. 2001; Niemela and Mattson 1996). These could
include tree killers like insects in the Scolytidae (especially Dendroctunus spp. bark
beetles), and various Adelgidae, and Lymantriidae, among others, and a variety of
disease organisms. A proactive approach to resistance development, while not a
guarantee, seems most certainly a reasonable approach to secure forest systems
against the seemingly inexorable globalization of pests. Finally, the most successful
strategy to develop and deploy pest resistance mechanisms in forests will include
factors such as expected rotation length, family/clone replacement rate (speed of
genetic improvement, and use of coppice regeneration), and in an economic sense,
anticipated tree value/supply vulnerability issues. Relying on family/clonal
substitution alone, without knowledge of resistance mechanisms, may not provide
much long-term stability.
180 D. ROBISON
7. ISSUES OF REFUGIA AND SCALE

Refugia can be deployed within a plantation (among individual trees or blocks), or
used wherever they occur adjacent to (naturally or planted), but outside of the
plantation system. In locations where plantation systems are established with native
species, there are often considerable refugia among the native forests. If these are of
sufficient scale (Figure 2), whereby through panmixis individual pests emerging
from the refugia can find and mate with those individual pests which were able to
develop on the resistant trees, then biotype development may be minimized through
this approach. The same is true for the use of refugia within the plantation system.
The opposing force is the scale of the resistant planting. These issues have not been
quantitatively assessed for insect-tree systems, but have been addressed in some
agricultural systems, especially with regard to genetically-engineered insect
resistance (Dillon et al. 1998; Gould 1998; Fitt and Wilson 2000). When the tree is
an exotic species, then it may represent all potential host plants. When it is a native
tree species, then it will depend on the scale of the plantations relative to the scale of
the refugia. However, even in exotic environments, if the tree species has long
escaped and naturalized, then it will have some refugia with respect to the
improved-resistant plantations (i.e., loblolly pine (Pinus taeda L.) in Brazil,
eucalytps in South Africa, others). But, when the scale of resistant planting
becomes such that pollen and seed from the resistant plantings dominate
reproduction in natural forests (either as an exotic or native species), then slowly the
value of apparent refugia may diminish as it too acquires the resistance traits.
Regardless of the origin of the tree species, when the pest is exotic, specific studies
are required to determine the pest’s effective refugia on various plant species, and if
the newly arrived pest population has sufficient genetic diversity to efficiently adapt.
The importance of scale with regard to biotype development / refugia is
dependent upon the intensity and uniformity of the selective pressure (resistance
mechanism), and the capacity of the pest population to move and interbreed with
individuals emerging from non-resistant (refuge) areas (Gould 1998). Examples of
this come from a number of systems. With the advent of commercially planted
agricultural crops genetically engineered to express the Bt d-endotoxin (e.g., in
cotton and maize), operational decision-making criteria have been developed to use
refugia as a means to delay biotype formation, reduce instability in crop production,
and preserve the utility of this important pest management mechanism (Gould
1998). From the use of pesticides there are many examples of biotypes developing
in response to strong uni-directional selective pressures, especially when the scale of
pesticide use overwhelmed the influence of refugia, and particularly against exotic
pests and pests on exotic plants (Metcalf 1994). An important example of this in
forestry was resistance to DDT formed in spruce budworm (Choristoneura
fumiferana (Clem.)) through intensive repeated spraying in New Brunswick Canada
in the 1950s and 1960s (Randall 1965). In this field situation, nearly 1 million
hectares of native forest were sprayed, and despite larger areas of refugia (unsprayed
areas) not far away, and a native insect with two mobile life stages, significant
resistance evolved. This spruce budworm – DDT example demonstrates the
potential for biotype evolution when scales are large, even where refugia is
extensive and the insect highly mobile. The stability of a resistant pest biotype,
when substantial refugia exists, and the selective pressure is later relaxed (e.g.,
cessation or change of insecticide spraying, or deployment of hew host resistance
mechanisms), is unknown.
By inference then, when a tree plantation system is widely deployed containing

strong uni-directional selective resistance characters, it potentially could result in
pest biotype development, and loss of resistance efficacy. This should be of
increasing concern in many parts of the world where exotic trees are extensively
planted, harvest and breeding cycles are increasingly short, and little is known about
the diversity of resistance mechanisms being utilized (i.e., loblolly and radiata
(Pinus radiata D. Don) pine grown outside of the U.S.A., Eucalyptus spp. grown
outside of its native range in Australia, others). In these situations, the plantations
represent the only host material, all of which may be contributing towards biotype
selection, slowly or rapidly. In some instances there are unimproved land races of
182 D. ROBISON
these types of exotic trees that have developed, thereby offering some, generally
limited, refugia. However, as discussed previously, the value of these trees as
refugia may decline over time, and increasingly such land races are viewed as
invasive weeds and discouraged. Even when planting native trees, the scale of
planting can become an important factor. Perhaps the best example of this is the use
of improved loblolly pine in the southern U.S.A. In this region such plantations
cover about 12 million hectares, or about 40% of the commercial pine forest in the
region, and this percentage is expected to increase to about 70% by 2040 (Wear
1993). While tremendous areas of natural pine refugia still exist, the scale of
planting suggests that within these areas biotypes may develop, and over time pollen
and seed from improved plantations will gradually become more represented in the
natural stands as well, thereby diluting the refugia.
8. SOURCES OF RESISTANCE
A significant base for inference about constructing stable forest systems with limited
genetic diversity, may be derived from naturally occurring clonal systems. Such
systems are common in nature, and are generally long-lived, stable, productive and
adaptive (Jackson et al. 1985). The socio-political/environmental notion that clonal
systems are alien is incorrect. These natural systems, many of extreme scale,
stability and ecological importance, beg for an explanation. Such perennial, tree and
tree-like, systems include various species within the genera Populus / Salix
(poplar/willow), Acacia, Pseudoacacia, Eucalyptus, Phyllostachys (bamboo),
Vaccinium / Gaylussacia (blue/huckle-berries), Rhizophora (mangrove),
Liquidambar (sweetgum), Ulmus (elm), and Paulownia, among others. It may be
possible to study these systems (Ellstrand and Roose 1987; Tuskan et al. 1996) and
derive information / guidance on the relative diversity of pest resistance mechanisms
necessary for stable and productive systems. Such knowledge, when applied to
commercial production systems, will provide a sound ecological basis for
deployment decisions.
The diversity of pest resistance (susceptibility) mechanisms within these natural
systems could be used as a guide and basis for inference for making decisions about
how to manage genetically-limited forest plantations. For example, while it might
be expected that among clonal groups within a wide-ranging species (i.e., Populus
tremuloides in the western U.S.A.) there will be a continuum of resistance factors of
varying efficacy, it would be instructive to assess these mechanisms, and using
information on their range of efficacy and modes-of-action, select or develop a suite
(at least two) of desired resistance factors. Then through ideotypic tree
improvement and clonal/family selection (Dickmann 1985; Park et al. 1988a; Martin
et al. 2001; Tharakan et al. 2001), plantations could be deployed with similar multi-
directional (durable) resistance factors, and ecological stability. Clues from these
systems will not only serve the purpose of guiding resistance development and
deployment strategies, but also provide a strong basis to satisfy environmental
skepticism about the nature and legitimacy of commercial clonal systems. Other
examples can be readily found among a wide variety of clonally propagated
agricultural and horticultural crops, some which have required intensive efforts to
manage pest problems, and others that have been very stable for many years
(Metcalf and Luckmann 1994; Panda and Khush 1995).
Interspecific tree hybridization also offers good possibilities for developing
productive and pest resistant genetic entities that can contribute toward providing
stable resistance. Through the process of hybridization, novel resistance
mechanisms can be added to existing species. This is the case in the development of
resistance to Dutch elm disease (Ophiostoma novo-ulmi) in American elm (Ulmus
americana L.) (Smalley and Guries 1993), and Eucalyptus canker (Cryphonectria
cubensis) worldwide (Alfenas et al. 1983), among others. While there are examples
of breeding and hybridization for the enhancement of insect resistance in
agricultural/horticultural crops (Metcalf and Luckmann 1994; Panda and Khush
1995), similar examples are not readily apparent for forest tree insect resistance.
Hybridization can provide a new diversity of resistance mechanisms to manage
biotype evolution, and be a source of new mechanisms when resistance breaks down
or is lacking. For example, resistance may be more readily derived from hybrid tree
development than from screening native populations for resistance to aggressive tree
killing pests. Such pests might include the southern pine bark beetle (Dendroctonus
frontalis) (native to North America; but potentially relevant wherever loblolly pine
is planted), and balsam woolly (Adelges piceae) or hemlock woolly (A. tsugae)
adelgids (exotic tree killers in North America), and the diseases mentioned
previously. There is also a need for care in developing/screening hybrids for growth
potential, as some may have poorer traits than either parent with regard to pest
resistance (Floate et al. 1997). Additionally, hybrids combining species long
separated evolutionarily may exhibit characteristics which violate standard
observations of plant defense and resource allocation strategies (Bazzaz et al. 1987;
Bryant et al. 1987; Coley et al. 1985; Mattson et al. 1988; Tuomi et al. 1988),
enabling genetic entities to be identified that are tolerant, resistant and productive
(Robison and Raffa 1994; Dvorak and Hodge 1998).
9. CONCLUSIONS
Deployment of genetically-based insect pest resistance in large-scale and intensively
managed forest plantations requires ecological understanding to achieve
sustainability. The problems of pest depravation and biotype evolution, and the
emergence of new pests can be managed through the use of a well-designed variety
of resistance and susceptibility factors. These must be selected based upon their
ecological and genetic interaction with the pests of concern, and not merely through
the use of a probability assessment of intolerable pest damage. The deployment of
pest resistance mechanisms that do not foster uni-directional genetic selection is
especially important. There must be greater coordination of pest-tree studies with
tree genetic improvement programs, and the development of operational resistance
screening methods, for insect resistance to be widely used in forest management
activities.
184 D. ROBISON
ACKNOWLEDGEMENTS
The invitation, patience and confidence of Mike Wagner (Northern Arizona University, USA)
are most gratefully recognized. Assistance from the book’s other editors is also gratefully
acknowledged, as well as that from many colleagues at North Carolina State University, and
others consulted during the process of developing this work, including the 56 people who
responded to the email survey. Fred Gould (North Carolina State University, USA), E.A.
“Short” Heinrichs (University of Nebraska-Lincoln, USA), Gerald Tuskan (Oak Ridge
National Laboratory, USA) and Mike Wingfield (University of Pretoria, RSA) provided
additional critical reviews and input.
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CHAPTER 9
DEPLOYMENT OF TREE RESISTANCE TO

INSECTS IN SHORT-ROTATION POPULUS
PLANTATIONS
DAVID R. COYLE1, JOEL D. MCMILLIN2, RICHARD B. HALL3 &

ELWOOD R. HART3,4
1
USDA Forest Service, Savannah River, New Ellenton, SC 29809, USA. 2USDA Forest
Service, Flagstaff, AZ 86001, USA. 3Department of Forestry, Iowa State University, Ames, IA
50011, USA. 4Department of Entomology, Iowa State University, Ames, IA 50011, USA.
1. INTRODUCTION
Host plant resistance has been identified as a key component of integrated pest
management (IPM) in agriculture and forestry. The topic of deploying and
conserving host plant resistance to minimize economic damage caused by insect
herbivores is not a new problem. For example, deployment strategies have been
addressed in depth in traditional agricultural systems for several decades (see review
by Gould 1998). In forestry, however, while the issues are recognized, little
rigorous experimental work has been completed. Although theoretical models have
been developed to predict the number of clones that are needed to minimize damage
and to conserve resistant genes (Libby 1982), actual field tests of these conceptual
models are lacking.
To maintain the usefulness of host plant resistance mechanisms as a management
tool while at the same time minimizing environmental risk, there are several critical
factors to consider: 1) determining and isolating multiple resistance mechanisms to
insects, 2) maintaining the effectiveness of host plant resistance in plantation
settings over time through adequate lines of resistance and planting designs, and 3)
developing resistance to a complex of pests. These factors have even more
importance when woody plant species are grown in systems similar to traditional
189
190 D. COYLE et al.
agricultural crops. At the same time, however, there is the potential to overcome
some of the limitations associated with traditional forestry.
The objective of this chapter is to review short-rotation woody crop (SRWC)
systems, attempts to incorporate resistance as part of an IPM program, and research
and theoretical tests designed to evaluate the effectiveness of host plant resistance
deployment strategies. In addition, we compare traditional tree selection and
breeding programs for developing tree resistance with genetic engineering
approaches. We then provide a detailed review focused on defoliators of short
rotation Populus plantations, as they have had the greatest insect impact on these
systems. However, a review of host plant resistance to other organisms also is
discussed, because all potential pests must be considered when developing IPM
systems. As SRWC systems are relatively new, but increasing in acreage
worldwide, we may see a new complex of organisms emerging that could be even
more economically important.
1.1 SHORT-ROTATION WOODY CROP SYSTEMS

SRWC systems are essentially tree plantations that combine traditional agricultural
and forestry practices. Most tree plantings usually are done with minimal site
preparation following a timber harvest; however, intensive site preparation occurs
prior to planting SRWC systems. Site preparation includes tillage to break up the
soil, herbicide applications to reduce existing weeds, pre-emergent herbicides to
reduce weeds during tree establishment, and the addition of lime or granular
fertilizer to increase the pH or nutrient availability of the soil (Dickmann and Stuart
1983). Irrigation or fertigation is often provided, allowing SRWC systems to be
grown on less than optimal soils. Typically, trees are planted in a grid pattern;
spacing depends on the desired product. Narrow spacing often is
used in coppice plantations, where the end product can be used for pulp or energy
(Kenney et al. 1993, Peterson et al. 1996, Hughes 1997). Wider spacing
is used for pulp production and for saw timber where rotation ages are greater
(Peterson et al. 1996, Zsuffa et al. 1996, Eaton 2000b). As the phrase implies,
harvest intervals in SRWC systems are much shorter than in traditional forestry and
usually range between 1 and 15 years.
Tree species commonly used in SRWC systems are fast growing, early
successional species such as Populus, Salix, Platanus, Liquidambar, Eucalyptus,
and Pinus. These genera provide species and hybrids that are very shade intolerant;
weeds must be kept to a minimum throughout the establishment period by tilling or
herbicide applications. Weeds have been shown to have a major negative impact on
Populus growth in SRWC systems (Hansen et al. 1984, Schuette 2000). Most of the
species used in SRWC systems are quite susceptible to insect and disease pests.
This is common in fast growing tree species, as the majority of the available
resources are invested in growth rather than defense (Kozlowski et al. 1991).
Currently, the most common solution for pest problems in SRWC systems is
pesticides. This chapter examines alternative pest management strategies, primarily
host plant resistance, that can be used in SRWC systems. Our review is primarily
limited to research conducted on Populus and Salix species in temperate zones;
RESISTANCE DEPLOYMENT IN POPULUS PLANTATIONS 191
selections and hybrids from these two genera are the most widely planted trees in
temperate SRWC systems.
1.2 SRWC PLANTATION STRATEGIES

Even though no field tests have been conducted on the effect of field size, number of
clones needed, or separation distances required between plantings of the same clone
(Hall 1993), there is general agreement that there are several plantation strategies
that could be used in SRWC systems (Zsuffa et al. 1993; Figure 1). Each strategy
has positive and negative attributes that might determine which plantation strategy is
used in a particular situation. Monoclonal stands, as the name suggests, consist of
large, single clone plots. These plots can be up to 20 hectares in size (Hall 1993).
Of the four strategies mentioned, monoclonal plantations are the most cost and labor
efficient and generally most used by industry (Eaton 2000a). Monoclonal stands are
treated much like traditional agricultural crops. The plantations are planted with a
single clone, receive the same cultural and chemical treatment, and can be harvested
at the same time. However, large monoclonal blocks increase susceptibility to pest
problems through resource concentration and ecosystem simplification (sensu Root
1973). As a consequence, once a pest becomes established it can continue to
proliferate throughout the entire plantation.
Several additional studies have reviewed the monoclonal block mosaic

plantation strategy (Libby 1987, DeBell and Harrington 1993). This consists of
several clones, each planted in relatively small monoclonal blocks. These blocks are
192 D. COYLE et al.
planted in a way that no two like clonal blocks are adjacent, creating a checkerboard
pattern. This system allows poor performing clones to be continually removed and
replaced, if necessary, thus keeping a fully-stocked plantation and constant supply of
wood. From a pest management perspective, the monoclonal block mosaic planting
pattern is more desirable than pure monoclonal blocks. In the event that one of the
clones becomes infested with an insect or pathogen, individual clonal blocks can be
managed separately. Diseased or damaged clones can be removed and replanted
without disturbing the other clones in the plantation. However, as clone use
increases, the logistics of plantation management generally become more difficult.
Clonal rows are another plantation strategy generally used in clonal selection
trials and cutting orchards. Clones are planted in several single rows adjacent to one
another. This planting method allows the assessment of various growth parameters
and pest susceptibility on many clones at one time. Research at Long Ashton, U.K.
suggested that mixing rows of susceptible and resistant willow clones may both
delay the onset of rust epidemics and reduce the movement and subsequent damage
caused by chrysomelid beetles (Royle et al. 1998, Peacock et al. 1999).
In terms of pest resistance, the safest planting method entails single tree mosaics
and small groups of trees. This method is by far the most time and labor intensive to
establish (if tree identities are to be maintained), but provides the greatest protection
from pests. Single-tree or polyclonal plots also are subject to more inter-plot
competition and therefore can result in overall reduced biomass production
compared with monoclonal plots (DeBell and Harrington 1997). Libby and
Cockerham (1980) also state that single-tree plots can be beneficial for research
activities, primarily because they eliminate environmental variances that can occur
within plots. However, single-tree plot studies are subject to missing data caused by
tree mortality. Also, should a single clone planted in this regime become infested, it
is much more difficult to remove the infested plants without harming the other trees.
Based on the above information, it becomes apparent that determining the
optimal number of clones necessary to maintain the effectiveness of resistance and
prevent plantation failure, while still maintaining plantation efficiency, is a
fundamental question that needs to be addressed. (See Robison this volume for an
alternative view on clone deployment). Theoretical models suggest that a minimum
of seven and perhaps as many as 20 (Libby 1982) or even more than 30 (Roberds
and Bisher 1997) unrelated clones are needed. However, using more than 20 clones
may create new problems, as it would be difficult to have >20 high-quality clones
that do not have some relatedness and therefore a genetic bridge for insect resistance
to develop (Libby 1982). Until the early 1990s, clonal diversity had been more
apparent than real. For example, although probably several hundred clones have
been developed in the U.S., only 3-9 were recommended for nursery production in
the Lake States (Hansen et al. 1994). Realizing the potential for plantation disaster,
most countries and industries have been working to scale up the number of clones
available for deployment. In Ontario, the goal was to have more than 50 clones
available at any one time with an annual replacement of 5-10% of the clones
recommended for planting as problems arose with older clones and/or much more
productive clones became available (Hall 1993). Also, clones being deployed are
specifically suited to each soil type and planted in monoclonal blocks no larger than
5 ha in size. In Oregon and Washington, U.S.A., only one clone from any full-sib
family is taken into production (Hall 1993).
To date, few experiments have attempted to evaluate the effect of multiple-clone
deployment strategies on pest populations and damage levels. Nordman (1998)
evaluated three clonal deployment strategies on larval gypsy moth, Lymantria dispar
L. (Lepidoptera: Lymantriidae). Two Salix clones were used: SV1 (S. dasyclados,
not resistant to L. dispar) and SH3 (S. purpurea, resistant to L. dispar). These
clones were arranged in three deployment patterns in the greenhouse: monoclonal
blocks, monoclonal mosaics, or clonal rows. Gypsy moth larvae were released in
the center of each pattern and allowed to disperse and feed for 10 days. Significant
defoliation differences occurred as a result of the clonal deployment pattern. As
expected, the least damage occurred on the monoclonal block of the resistant clone
SH3. Clonal rows provided better levels of pest resistance than did monoclonal
mosaics or the monoclonal block of the non-resistant clone SV1. Presumably, this
occurred because larvae spent more time searching for a suitable food source and
less time eating. In nature, additional time spent searching for food is detrimental to
pests, as their exposure to natural enemies and abiotic hazards is increased.
Peacock et al. (1999) demonstrated the spatio-temporal dynamics of a
chrysomelid beetle on short-rotation willow in the United Kingdom. Three willow
clones (one highly-, one moderately-, and one non-preferred for feeding) were
planted as monoclonal blocks or clonal rows. Adult Phratora vulgatissima L.
(Coleoptera: Chrysomelidae) were shown to aggregate on the preferred clone in
both deployment strategies. However, much more time was needed for the beetles
to find the preferred clone when in the clonal row pattern, potentially increasing
their exposure to natural enemies as well as delaying development.
Another group of strategies related to plantation management includes those
borrowed from traditional agricultural systems. These also may work in short-
rotation forestry systems. Crop rotation is a common pest management tactic used
in agriculture. The same crop or variety is seldom planted in the same field in
repeated years, as many pests overwinter in duff or soil within the field or in nearby
ground cover or litter. This strategy prevents the pest buildup over several years, as
each spring the previous year’s food source is not present, causing them to move on
or make use of the new crop. This strategy may work in SRWC systems; however,
it is not nearly as applicable. For instance, by the end of a Populus rotation (8-12
years) new clones are available that are superior to the clones previously planted.
Perhaps a more appropriate cultural method would be to leave an area fallow for a
year before replanting a SRWC system. Chrysomela scripta F. (Coleoptera:
Chrysomelidae) are believed to overwinter in leaf litter near their summer food
source. By leaving a plantation fallow after harvest, emerging adults would be
forced to find a new food source the following spring.
Sage et al. (1999) showed that three chrysomelid beetle species overwinter
outside Salix biomass plantations and re-infested them each spring. Planting a
clonal buffer around the desired clones may be a way to control these pests. The
buffer rows could be chemically treated or genetically modified with an insect
resistant gene while the interior of the plantation could be left untreated, thus
creating an insecticidal border around the plantation. This would reduce or
194 D. COYLE et al.
eliminate the beetle population that reached the interior untreated area of the
plantation.
Additional clonal deployment strategies with respect to genetically engineered
plants will be discussed in section 2.1.4.
1.3 GENETIC ENGINEERING VERSUS TRADITIONAL TREE BREEDING

If the use of host genetics in forest pest management was easily achieved it would
probably be more widely used. Research in the use of host genetics to disrupt pest
populations has traditionally proceeded through selection and breeding programs.
More recently, biotechnology has begun to play an increasingly important role
combining the two approaches into a single program (Hart et al. 1992). Genetically
modified (GM) trees have the potential to substantially increase wood production in
the U.S. (Pullman et al. 1998). From a pest management perspective, genetically
engineering toxic genes into trees seems to be an excellent means of pest control.
However, changes created by genetic engineering are very different than those
brought on by natural evolution or traditional tree breeding and selection. This
tactic introduces organisms into the environment that would not otherwise exist
there, providing a potential risk to native flora and fauna. Yet, if properly managed,
GM trees have the potential to cause little or no damage to the current state of the
environment. Several authors have provided excellent reviews on the benefits and
risks of GM trees (Raffa 1989, Boulter et al. 1990, McGaughey and Whalon 1992,
James 1997, Raffa et al. 1997, James et al. 1998, Jouanin et al. 1998, Pullman et al.
1998).
Summarized below are some of the benefits and risks associated with GM trees:
Benefits:
1. Pesticide replacement. The use of GM trees in SRWC systems would reduce
the amount of pesticides applied to plantations and subsequently lost into the
environment via drift, leaching, etc. (Raffa 1989, James 1997). It has been
estimated that only 0.1% of the average pesticide application actually reaches the
target pest (Pimental 1995). Trees possessing genetic toxicity to insects would
eliminate the pesticide lost (an estimated 99.9%) in the environment while
simultaneously providing much more efficient insect control. Furthermore, by not
investing the time, effort, and physical resources needed for large-scale pesticide
applications, great economic savings could be achieved. GM trees also would
provide equal pest protection for the entire growing season regardless of weather
(Boulter et al. 1990), a luxury rarely attained using chemical sprays, and especially
important in managing multivoltine pests.
2. Increased productivity. Trees genetically engineered for pest resistance may

not only reduce pesticide cost and input into the environment, but also greatly
improve tree productivity by reducing defoliation-related losses. Coyle et al.
(2002b) showed the negative effect C. scripta defoliation had on Populus above-
ground volume accumulation. Volume was more than 70% greater in chemically
protected trees compared to controls. Also, fast growing trees contribute more
carbon sequestration activity than do slower growing trees. The increased
productivity potential associated with transgenic trees could help make SRWC
Populus an effective source of wood and wood-based products.
3. Source of the toxic gene. Most GM Populus contain either a Bacillus

thuringiensis (Bt) gene or a proteinase inhibitor, both of which are naturally-
occurring and have relatively well-defined target specificity. Furthermore, these
genes are biodegradable and usually non-toxic to mammals, birds, and other
vertebrates (Boulter et al. 1990). However, because GM trees do not occur naturally
in nature, they are not considered true biological control pest management methods
even though the pest control tactic they employ occurs naturally.
4. If clonal sublines can be developed with different transgenes for resistance to

a particular pest, then plantations could be established as single tree mosaics at the
subline resistance level, but as monoclonal blocks from the standpoint of the other
commercial traits of a clone (Klopfenstein et al. 1993b). This approach would
combine the pest management benefits of single-tree mosaics with the logistical and
commercial benefits of monoclonal block plantations.
Risks:
1. Biotype evolution. This is defined as the selection for pest populations able to
tolerate the new resistance mechanism (Gould 1988). Evolution of new biotypes is
the most important risk associated with the deployment of GM plants, and creates an
ineffective system in which the GM plant is no longer toxic to the target organism
(Raffa 1989, James 1997, Klopfenstein and Hart 1997, Raffa et al. 1997). This is
particularly problematic when dealing with trees because of their long life cycle. A
single SRWC rotation of 8-12 years can encompass enough insect generations to
allow new biotypes to develop (James 1997). Also, the transgene is expressed
continually in the plant, thus constantly exposing insects to the toxin, a process that
accelerates resistance. Bauer (1995) reported on 13 species (including C. scripta)
that have already developed resistance to Bt in the laboratory.
2. Effects on non-target organisms. The potential for GM plants to adversely

affect non-target organisms is of great concern. Perhaps the most well-known and
controversial example is the recent finding that corn pollen containing a Bt toxin has
the potential to negatively affect monarch butterfly, Danaus plexippus L.,
(Lepidoptera: Danaidae) larval survival and development (Losey et al. 1999,
Hansen-Jesse and Obrycki 2000). These studies have initiated an intense
controversy and increased the number of studies into the non-target effects of
transgenic plants. Other studies also have found Bt toxins to negatively affect
beneficial organisms (James et al. 1993). There also is a risk of predatory insects
acquiring toxins through the consumption of contaminated prey. Reducing predator
populations this way would not benefit transgenically gained protection, as predator
complexes often compliment transgene pest control. Overall, much less research
has been conducted on the effects of GM trees on non-target organisms.
196 D. COYLE et al.
3. Transgene escape. Substantial environmental damage could occur if the

transgene increases the fitness of the host tree under wild conditions (Raffa 1989,
James 1997, Raffa et al. 1997, DiFazio et al. 1999). The longevity of the escaped
GM tree may be greater than that of the original non-GM tree, resulting in increased
probability that GM trees could establish in the wild or interbreed with non-GM
trees. Hypothetically, GM trees could be more invasive than non-GM trees, thus
outcompeting native host trees for available resources. This also could happen if
GM trees exhibited an increased growth rate, reaching reproductive maturity earlier
than non-GM trees. One way to combat this might be to genetically engineer
reproductive sterility. The research group led by Dr. S. H. Strauss at Oregon State
University is working on this issue, and has inserted some transgenes that may give
sterility (Strauss et al. 1995). This could solve many of the risks associated with the
deployment of GM trees.
Adequate risk assessment of GM Populus is necessary if these plants are to be
used in SRWC systems safely and effectively (Raffa et al. 1997). Relying on the
pest resistance of the transgenic plant alone will almost certainly result in increased
biotype formation, thus negating the insecticidal effects of the transgene.
Supplemental pest control with pesticide applications, utilizing clonal deployment
strategies, and GM crop rotation are effective ways for managing insect resistance.
2. REVIEW OF HOST PLANT RESISTANCE IN POPULUS AND SRWC

SYSTEMS
2.1 RESISTANCE TO CHRYSOMELID BEETLES
2.1.1 Clonal variation

Developing and selecting insect and disease resistant clones should be emphasized
as the primary defensive strategy against pests in short-rotation Populus. A great
deal of information has already been learned about this group of pests.
Chrysomela scripta is the most important defoliator of Populus in the eastern
U.S. (Burkot and Benjamin 1979). Both adults and larvae of this multivoltine insect
can severely damage branch terminals, and its ability to rapidly increase populations
can lead to widespread economic damage in young plantation Populus (Harrell et al.
1981, Coyle et al. 2002b). While synthetic (Abrahamson et al. 1977) and
biorational (Coyle et al. 2000) chemical controls have proven effective in
controlling C. scripta in plantation Populus, these methods are neither
environmentally-friendly nor provide a long-term solution to the pest management
problem, respectively.
Through the process of selective tree breeding, favorable traits can be combined
in superior tree cultivars. This process is ongoing and new clones are continually
being developed. Because of the large number of clones potentially available for
large-scale clonal deployment, careful screening must be completed to ensure that
only clones with positive attributes are chosen. Several general principles have been
established regarding C. scripta as a result of clonal screening trials, particularly in

the areas of oviposition and feeding preference as well as performance.
Caldbeck et al. (1978) examined C. scripta feeding preference on 33 Populus
clones. Both adult and larval C. scripta defoliated trees. Visual damage estimates
were used to assess beetle preferences. Clonal preferences were observed, and
followed lines of sectional parentage. Clones in the section Populus ( = Leuce) (e.g.
containing P. alba parentage) showed minimal damage, whereas clones in the
Aigeiros (e.g. P. deltoides) and Tacamahaca (e.g. P. trichocarpa) sections had a 22
to 78% reduction in leaf area.
Haugen (1985) evaluated adult C. scripta feeding and oviposition preference on
12 Populus clones. A multiple choice greenhouse experiment confirmed that adult
C. scripta did not prefer Populus section clones for oviposition. Pure species clones
in the sections Aigeiros and Tacamahaca were both highly preferred for oviposition,
and there was a relationship between Aigeiros parentage and oviposition preference.
Clones with a greater amount of Aigeiros parentage were more preferred for C.
scripta oviposition than those with greater Tacamahaca parentage.
A study by Bingaman and Hart (1992) showed C. scripta’s preference to
oviposit on section Aigeiros clones compared to section Tacamahaca clones. Six
clones were examined in this study, and two of the top three highest oviposition
rates were on clones with section Aigeiros parentage; a section Tacamahaca hybrid
was used the least for oviposition. These findings contrast somewhat with those of
Haugen (1985), as he found the same section Tacamahaca clone preferred for C.
scripta oviposition. Furthermore, oviposition was preferred on pure species in
sections Aigeiros and Tacamahaca over intersectional hybrids (Bingaman and Hart
1992). Adult C. scripta feeding preference also was examined in this study.
Increased adult C. scripta feeding occurred on clones with a greater percentage of
section Aigeiros parentage when compared to clones with section Tacamahaca
parentage. However, increased adult feeding was shown on clones in the Aigeiros
and Tacamahaca sections when compared in multiple-choice bioassays. A P.
deltoides P. nigra clone was the most preferred in adult feeding trials; this agreed
with Caldbeck et al. (1978). Bingaman and Hart (1992) suggested that oviposition
preferences followed feeding preferences because adult C. scripta spent more time
on these clones, thus having a greater opportunity for oviposition.
Previous research showed that C. scripta adult feeding preferences did not
correspond with larval performance on Salix host plants (Orians et al. 1997). A
study was conducted to determine if adult C. scripta preferentially oviposit on
clones that increase larval performance. Larval C. scripta performance was
examined on eight Populus clones by measuring larval mortality, pupal weight,
adult emergence, and total mortality (Coyle et al. 2001). Larvae generally
performed better on section Aigeiros Tacamahaca hybrids as opposed to pure P.
deltoides or P. trichocarpa clones. However, environmental factors may play a
more important factor in larval C. scripta performance than originally thought, as a
seasonal decline in larval performance was evident.
Species in the section Populus are not preferred for feeding or oviposition,
whether they are pure species or hybrids. Aspens are not natural host plants for C.
scripta (Baker 1972), and this antixenotic relationship might be exploited by using
198 D. COYLE et al.
selections from the Populus section in mixed planting designs. However, section
Populus clones are quite difficult to cross with clones in other sections, and it is not
clear that anything could efficiently come out of a hybridization strategy.
2.1.2 Foliar chemistry

Phytophagous insects usually consider combinations of olfactory, visual, and
physical factors when selecting a host plant. Chemical interactions seem to be quite
influential in C. scripta host plant selection. Trees in the genus Populus have a suite
of secondary compounds throughout their tissues; most notable are the phenolic
glycosides (Palo 1984, Picard et al. 1994b, Lindroth and Hwang 1996a). Aspens (P.
tremuloides) have at least four phenolic glycosides present in their leaf tissues
(salicin, salicortin, tremuloidin, and tremulacin), whereas P. deltoides seems to lack
tremulacin (Lindroth et al. 1987). Extensive research on aspen phenolic glycosides
has come, from Dr. R. L. Lindroth and his research group at the University of
Wisconsin. Lindroth and Hwang (1996b) have written a comprehensive review of
this subject.
Seasonal fluctuations in the amounts of phenolic glycosides and nitrogen content
occur in several Populus species and clones (Dickson and Larson 1976, Lindroth et
al. 1987, Osier et al. 2000b). Generally, these chemicals decline over the course of
a growing season. However, younger leaves had significantly higher concentrations
of phenolic glycosides than did older leaves (Lindroth et al. 1987). Seasonal decline
also was found in leaf surface long-chain alcohol and alpha-tocopherylquinone
concentrations (Coyle 2000).
Herbivory by chrysomelid beetles also influenced Populus foliar chemistry.
Populus tremula P. tremuloides clones showed an increase in phenolic glycoside
production in response to C. scripta defoliation (Picard et al. 1994a). This resulted
in decreased herbivory by the beetle. Bingaman and Hart (1993) examined this
relationship with C. scripta and hybrid Populus. Phenolic glycoside (salicin,
salicortin, and tremulacin) content was measured on seven hybrid Populus clones.
Chemical amounts varied among clone and leaf age class (younger leaves had
higher phenolic glycoside concentrations). Tremulacin amounts in hybrid Populus
were negatively correlated with C. scripta feeding and oviposition preferences,
whereas salicin and salicortin amounts were not.
Matsuda and Matsuo (1985) showed that some phenolic glycosides in Salix
gracilistyla leaves act as chrysomelid beetle feeding stimulants. Long-chain
alcohols on the leaf surface also can serve as phagostimulants to chrysomelid beetles
(Adati and Matsuda 1993). Recently, Lin et al. (1998a) discovered a suite of
Populus leaf surface chemicals that act as adult C. scripta phagostimulants. Long-
chain alcohols and were isolated from the P. deltoides P. nigra
clone ‘Eugenei’. Artificial leaf disc bioassays were used to examine the effects of
these chemicals on adult C. scripta feeding. Alcohols or alone did not
stimulate intense feeding behavior, but when used in specific ratios these chemicals
induced C. scripta to bite. A subsequent study (Lin et al. 1998b) investigated the
interactions between Populus leaf surface phagostimulants from field-grown trees
and adult C. scripta. Adult C. scripta feeding preferences were examined for 91
Populus clones from a University of Washington pedigree line. Feeding preferences

were then correlated to the aforementioned phagostimulants and to the phenolic
glycosides tremulacin and salicortin. Leaf surface chemical amounts of long-chain
alcohols and the phenolic glycosides did not explain C. scripta feeding preferences.
However, feeding preference was linked to content. Leaf area consumption
increased as concentrations reached , but feeding decreased when
levels increased further. This study linked the content on the Populus
leaf surface to adult C. scripta feeding preference.
It is unknown if Populus trees are able to alter their leaf surface phagostimulant
concentrations in response to C. scripta feeding. A study was conducted to examine
the effects of larval C. scripta defoliation on the leaf surface phagostimulant
concentrations of eight Populus clones. Coyle (2000) found that amounts of these
chemicals were not significantly altered by larval C. scripta defoliation. Larval
performance did not correlate with leaf surface phagostimulant concentrations;
however, both larval performance and leaf surface chemical amounts declined over
the course of a growing season.
There are many implications and applications from this research. Adult C.
scripta Populus clonal preference is mediated by amounts on the leaf surface;
however, it is unknown if Populus clones preferred by adult C. scripta for feeding
and oviposition are more suitable for larval growth and development. If this proves
true, clones less preferred by adult C. scripta could be used in Populus breeding and
clonal selection programs. This could, theoretically, produce clones less suitable for
larval C. scripta growth and development. Also, the identification of C. scripta
phagostimulants can be used in many ways. Efforts have been made to develop an
artificial diet for C. scripta (Bauer 1990) as maintaining a laboratory colony is labor
intensive and requires much greenhouse space for food trees. The diet developed by
Bauer (1990) was nutritionally adequate, but resulted in decreased colony health.
Attempts to incorporate Populus leaf surface phagostimulants into the diet to
increase C. scripta consumption have been unsuccessful (Coyle and Hart,
unpublished data).
2.1.3 Proteinase inhibitor genes

Genetic engineering of woody plants is a relatively new technology. Currently, the
primary focus is on incorporating genes for pest resistance (Heuchelin et al. 1997,
Klopfenstein and Hart 1997). Populus trees are easily manipulated through various
genetic engineering methods (Klopfenstein et al. 1997b). Effective procedures have
been developed for vegetative propagation of Populus (Faltonson et al. 1983). The
ability to genetically manipulate a rapidly growing woody plant with the possibility
of quickly increasing plant numbers opens doors to new pest management strategies.
Scientists at Iowa State University successfully transformed a hybrid poplar clone,
P. alba P. grandidentata, with a wound-inducible proteinase inhibitor II (pin2)
gene from a potato (Klopfenstein et al. 1991). Field data showed that transgenic
plants did not statistically differ in height or diameter compared to non-transformed
controls (Klopfenstein et al. 1993a). This study showed that pest resistance genes
can be incorporated into Populus clones without compromising growth.
200 D. COYLE et al.
Several studies have shown successful incorporation and application of the pin2
gene in hybrid poplar. Reduced leaf area consumption and growth rates occurred
when larval Plagiodera versicolora Laicharting (Coleoptera: Chrysomelidae) were
fed Populus leaves from clones transformed with the pin2 gene (Klopfenstein et al.
1994, 1997a). Kang et al. (1997) examined transgenic Populus resistance to C.
scripta on tissue-culture plantlets of the Belgian clone Ogy (P. deltoides P. nigra)
and three sublines transformed with the pin2 gene. Leaf area consumption was
reduced by as much as 45% and larval C. scripta weight was up to 16% less on the
transformed lines compared with Ogy.
Chrysomela scripta resistance on these clones was evaluated in a greenhouse
experiment (Coyle et al. 2002a) to determine if the resistance exhibited in plantlets
was maintained in young trees. Leaf area consumption and larval C. scripta growth
and development were not affected by the presence of the pin2 gene. We can
provide several explanations for these results, with environmental differences posing
as the main concern when comparing these two studies. Kang et al. (1997) placed
larvae in test tubes with the plantlets, whereas Coyle et al. (2002a) conducted their
study in the greenhouse. There are many differences between these two
environments, including sterility, air composition, and their effects on plant tissue
growth. Large increases in plant size accompany the laboratory – greenhouse – field
study experimental sequence; this may have had an effect on the efficacy of the pin2
gene. It is not known if a field study would produce results similar to either of the
previous studies.
European scientists also have had success incorporating proteinase inhibitor
genes into Populus for chrysomelid resistance. Leple et al. (1995) showed high
levels of gene expression in P. tremulae P. tremuloides clones transformed with a
proteinase inhibitor. Transformed clones were toxic to Chrysomela tremulae F.
larvae, an important pest of poplars in Europe. This was the first study to
successfully transform Populus with a proteinase inhibitor and demonstrate toxicity
to chrysomelid larvae. Recently, a proteinase inhibitor gene was incorporated into
P. alba (Delledonne et al. 2001) and high levels of resistance to Chrysomela populi
L. were obtained.
While this technology seems promising, there are still several cases of plants
transformed with proteinase inhibitor genes not showing resistance to insect
herbivores (Confalonieri et al. 1998, Girard et al. 1998, Coyle et al. 2002a). Insects
do possess the ability to adapt to proteinase inhibitor genes just as any other
transgenic control method (Jongsma and Bolter 1997).
2.1.4 Transgenic Bt trees

Technology has advanced to the point that select Bt toxin genes can be inserted
directly into plants for insect control. This pest management tactic is not new to
traditional agricultural crops; Bt corn has been commercially sold and field planted
since 1995 (Carozzi and Koziel 1997). Currently, cultivars of soybean, cotton,
potato, and a host of other crop species have been developed and are registered for
use.
The use of transgenic Bt-expressing plants in forestry systems is still a novel

approach to pest management. While the application of Bt formulations to
plantation Populus is an effective way to combat pests (Coyle et al. 2000), the use of
transgenic trees can be more favorable for a number of reasons (Meilan et al. 2000).
Spray drift is reduced, as the Bt toxin is produced in the plant tissues, and the toxin
will not degrade as will a sprayed formulation. Also, Bt plants only expose the toxic
gene to insects feeding on the plant. Bt toxins differ from proteinase inhibitors in
that Bt generally causes direct mortality of the target pest. Proteinase inhibitors
have a more subtle mode of action, reducing fecundity, extending the life cycle, and
causing reduced weight and changes in insect behavior (Ryan 1981, 1990).
Populus was the first woody plant species to be transformed with the Bt gene
(McCown et al. 1991). Researchers at Oregon State University have since produced
over 1,700 transgenic Populus lines (Strauss et al. 1998). Resistance to C. scripta
was evaluated on 51 lines of Bt Populus transformed with an Agrobacterium
tumefaciens vector (Meilan et al. 2000). Every transformed strain evaluated showed
significantly reduced defoliation and increased growth at the end of one growing
season. Robison et al. (1994) and Wang et al. (1996) observed insecticidal effects
in poplars with a lepidopteran-specific Bt gene. Large-scale field trials are currently
being initiated by Meilan et al. (2000) in the Pacific Northwest and by Wang et al.
(1996) in China.
202 D. COYLE et al.
Reviews by Tabashnik (1994) and Gould (1998) provide excellent summaries of

insect resistance management with respect to transgenic crops. These reviews
emphasise several resistance management tactics, including mixtures of toxins,
refugia strategy, high dose strategy, synergists, and spatial and temporal expression
of toxins. The refuge strategy may be the best way to slow the development of
insect resistance in transgenic crops (Tabashnik 1994). This strategy employs a
refuge of non-transgenic plants planted with transgenic ones. Non-resistant pests
are allowed to reproduce without receiving sublethal doses of the toxin, and
subsequently breed with resistant pests. This diffuses the gene for insect resistance,
thus delaying the species’ or population’s development of resistance. Gould (1998)
focuses on the high dose/refuge approach for management of insect resistance to Bt
crops (Figure 2). This differs only in that the transgenic plants present with the
refuge carry a level of toxicity much greater than needed to kill the pest. If the level
is sufficiently high enough, even resistant individuals will be killed by the toxin, and
will not be able to pass the resistant gene to future generations. While refuges can
be within or adjacent to transgenic plots, adjacent refuges have been shown to be
more effective in some systems (Tang et al. 2001).
2.2 RESISTANCE TO OTHER DAMAGING AGENTS

There is considerable interclonal variation in secondary chemical amounts present in
Populus foliage (Lindroth and Hwang 1996a, 1996b, Hwang and Lindroth 1997, Lin
et al. 1998b, Osier et al. 2000b). Insect survival, larval stadium duration, and body
weight varied greatly for two larval lepidopterans, L. dispar and Malacasoma
disstria Hübner (Lepidoptera: Lasiocampidae), when reared on 13 different aspen
clones (Hwang and Lindroth 1997). These differences were more pronounced in L.
dispar, where larval survival ranged from 0 to 100% in fourth instar larvae. Fourth
instar M. disstria survival ranged from 60 to 100% on the same clones. Lymantria
dispar performance was reduced when higher phenolic glycoside concentrations
were present in P. tremuloides foliage (Osier et al. 2000a). However, foliar
consumption was positively correlated with tannin concentration.
Atmospheric and light intensity also may influence larval performance and
foliar chemistry. Increased and light levels induced increases in aspen foliar
phenolic glycoside content (Lindroth and Kinney 1998, Roth et al. 1998, McDonald
et al. 1999). Furthermore, L. dispar larvae had reduced growth rates when fed aspen
leaves exposed to increased levels (Lindroth and Kinney 1998, McDonald et al.
1999). Overall, these larval performance reductions were not great, and were not
apparent in one study using M. disstria (Roth et al. 1998).
Many studies have shown that insect defoliation can induce chemical changes in
foliage. Often these are specific damage-induced chemical changes that provide the
plant protection (Lindroth and Hwang 1996b). Aspen trees have a well-documented
wound-induced chemical protection system. For instance, defoliation by
Choristoneura conflictana (Walker) (Lepidoptra: Tortricidae) induces increases in
phenolic glycoside content (Clausen et al. 1989). These chemicals are toxic to C.
conflictana, and result in reduced larval performance. Larval L. dispar and M.
disstria defoliation induced increases in aspen phenolic glycoside content (Lindroth
and Kinney 1998, Roth et al. 1998). However, only L. dispar performance was
correlated negatively with phenolic glycoside content in aspen. Therefore, wound-
induced increases in foliar phenolic glycosides are an effective but species-specific
natural defense mechanism.
Several additional insect pests, including root and shoot borers, sawflies,
lepidopterans, and leaf miners, attack Populus plantations (Solomon and
Abrahamson 1972, Thomas and Rose 1979, Wilson 1979, Solomon 1988, Sage and
Tucker 1997). However, their populations generally do not reach the economically
damaging levels of C. scripta, M. disstria, or L. dispar. However, the cottonwood
twig borer, Gypsonoma hiambachiana (Kearfott) (Lepidoptera: Tortricidae), can
have an economic impact on SRWC systems. Morris (1967) identified this insect as
a potentially damaging pest of plantation Populus. High populations have been
shown to cause nearly 100% terminal shoot mortality (Stewart and Payne 1975).
Current controls include synthetic chemicals (Morris 1960, Coster et al. 1972) and
possibly natural biological controls (Morris 1967). Two studies have evaluated P.
deltoides clonal resistance to G. hiambachiana (Woessner and Payne 1971, Payne et
al. 1972). Pure P. deltoides clones in both studies were more heavily attacked than
a hybrid clone. These results imply that Populus hybridization may be required in
order to attain resistance to G. hiambachiana, a phenomenon observed in other
herbivory studies and reviewed by Fritz et al. (1999). However, McMillin et al.
(unpublished data) found varying damage levels among four hybrid Populus clones
and across three locations in Iowa (Figure 3), indicating that not all hybrid poplars
are resistant to G. hiambachiana damage.
204 D. COYLE et al.
Recently, McMillin et al. (1998) suggested that increasing the number of

actively-growing Populus terminals in a plantation can result in G. hiambachiana
population increases. Hence, alternate controls must be attained for this pest, as
plantation size will most likely increase as short-rotation forestry gains acceptance
and industrial implementation.
Disease also is a major issue in short-rotation Populus plantations, and the
resulting damage can be equal to or greater than that caused by insects, particularly
in the establishment years (Ostry and McNabb 1985). Disease can be managed
much the same as insect pests by incorporating host-plant resistance mechanisms
and utilizing proper plantation planting and management strategies. Many diseases
can damage Populus (Berbee 1964, Shea 1971, Ostry and McNabb 1985,
Newcombe 1996). However, only a few are of great economic significance.
Melampsora medusae Thuem. (Uredinales: Melampsoraceae) leaf rust is one of
the most damaging and widely studied diseases of Populus in North America
(Newcombe 1996). This disease can result in premature leaf abscission, reduced
growth, increased lateral branching, and early mortality (Newcombe and Chastagner
1993, Newcombe et al. 1996, Callan 1998). Previous studies have shown wide
variation in Populus resistance to Melampsora rust (Ostry and McNabb 1985,
Newcombe et al. 1994). However, it is becoming clear that selection for complete
resistance and the deployment of resistant clones has led to the development of
many new rust biotypes that may overcome host resistance.
Septoria musiva Peck (Dothideales: Sphaerioidaceae) leaf spot and stem canker
is an important cosmopolitan disease of Populus. This fungus generally occurs as
leaf spot on native Populus with cankers predominately reported on clones
containing Tacamahaca parentage (Bier 1939, Waterman 1946). Stem breakage
often occurs well before harvest age, and susceptible clones are generally not
utilized in plantations (Ostry et al. 1989). Selecting Populus clones resistant to
Septoria through clonal screening is the only way to combat this pest. Clones with
Tacamahaca parentage have been shown to be more susceptible than clones with
Aigeiros parentage (Ostry and Berguson 1993). This study also showed that
selecting canker resistant clones can result in reduced biomass accumulation.
However, recent clone selection work with pure P. deltoides germplasm indicates
that high yields can be combined with Septoria canker resistance (Hall, unpublished
data).
Increased growth is often sought by hybridizing Populus rather than planting a
single species (Stettler et al. 1996). However, hybridization may sacrifice any
natural disease resistance occurring in native species (Fritz et al. 1999). Presently,
the only effective way to combat pathogens is by utilizing host plant resistance
mechanisms in breeding and selecting resistant clones (Callan 1998). Genes
conferring resistance to Melampsora have been discovered in hybrid and pure
species Populus (Newcombe et al. 1996, Tabor et al. 2000). Selective breeding
and/or genetic engineering may facilitate the incorporation of these genes into new
Populus clones. Exapted resistance (that conferred by a non-native species) may
play a much larger role in future Populus plantation management (Newcombe
1998). This type of resistance will need to be used in concurrence with other
resistance mechanisms to effectively combat many of the pathogens occurring on

Populus.
2.3 MULTIPLE PEST SCREENING

All woody crop species have a varied complex of organisms that have the ability to
limit the economic viability of these systems. For example, Populus has at least 24
insect defoliators as well as several pathogens in North America (Dickmann and
Stuart 1983). Further complicating the development of deployment strategies for
Populus resistance is the fact that different insect species seem to prefer different
clones; a resistant clone to one insect is susceptible to a complex of other insects.
Thus, screening of advanced clones or selections must include tests across a variety
of taxa.
Several studies have screened clones for resistance and/or susceptibility to two
or more defoliating insects and pathogens. Researchers at the University of
Wisconsin screened three Populus clones to C. scripta and M. disstria (Raffa et al.
1991, Ramachandran 1993). Two clones were highly susceptible to C. scripta, but
resistant to M. disstria, whereas the opposite was true in the third clone. This trade-
off was caused by the high phenolic glycoside content in M. disstria resistant clones,
which positively influences C. scripta, and the low concentration in the M. disstria
susceptible clone. This research suggests that the M. disstria resistant clone could
be engineered with the coleopteran-toxic Bt gene to create resistance across two taxa
(Raffa et al. 1991, Ramachandran 1993).
Nordman (1998) screened 19 Salix and six Populus clones for resistance to seven
defoliating insects. Two primary results were obtained: a wide range of
susceptibility occurred among clones to a particular defoliator, as well as in
individual clones to all seven defoliators. Clones resistant to one species often were
not resistant to others. This study demonstrates the need for multiple pest resistance
screening when preparing clones for commercial use.
3. DEVELOPMENT OF AN IPM PLAN FOR C. SCRIPTA

The majority of SRWC commercial hardwood operations have been developed in
the Pacific Northwest region of the U.S. and in Europe, but more recently are being
established throughout several other locations in the U.S. and Canada (van Oosten
2000). Present management methods for insect pests, such as C. scripta, in
commercial plantations are currently quite dependent upon applications of broad-
spectrum organic or biorational insecticides. Often, this is still done on a calendar
schedule, but commercial growers are beginning to recognize the desirability of
monitoring for pest activity and levels and timing applications to increase efficacy
and reduce losses. They are becoming aware that repeated applications of a single
pesticide may contribute to the development of insect resistance to that material.
The development and initiation of an IPM program is the next step in Populus pest
management. IPM is designed to be more environmentally-friendly and incorporate
many different control measures into a pest management strategy. IPM also may
help reduce the development of insect biotypes and thus prolong the effective
206 D. COYLE et al.
commercial life of desirable clones. With some expansion and fine tuning of the
existing base of knowledge, we seem to be poised to develop and implement an IPM
plan for plantation Populus, particularly for managing C. scripta.
Plantations should contain resistant clones, as this will serve as the foundation
for C. scripta control. By selecting clones that are less preferred for adult feeding
and oviposition we can reduce the amount of time adult beetles spend on the clones,
therefore, reducing their tendency to oviposit (Bingaman and Hart 1992). Also,
clones that cause poor larval performance and delayed development can be planted
to reduce the number of adults present. As stated earlier, multiple lines of resistance
are needed to prevent biotype evolution. However, the number of lines needed is
still under debate. Unless clones can be developed that are completely resistant to
C. scripta, other pest management strategies will also need to be utilized.
Biorational sprays are a chemical control method capable of providing excellent
C. scripta control. Unlike their synthetic chemical counterparts, biorational sprays
containing Bt are environmentally-friendly and non-toxic to vertebrates and most
non-target organisms (Tabashnik 1994). Several studies have shown Bt toxins to be
extremely effective in controlling C. scripta populations in the laboratory (Bauer
1990, James et al. 1999). Coyle et al. (2000) achieved excellent C. scripta control
in the laboratory using two commercially available Bt formulations. These
formulations were then applied to a Populus plantation and similar results were
attained. Results from Coyle et al. (2000) agreed with previous laboratory studies
(Bauer 1990, James et al. 1999) in that susceptibility to Bt was negatively correlated
with beetle age and size. Adult C. scripta are far less susceptible to Bt than are
larvae, especially the first two instars. Hence, the timing of Bt application is of
great importance. Bt formulations will achieve the greatest level of control early in
the C. scripta generation, and should be applied when eggs and first instars are the
predominant life stages. Coyle et al. (2000) made their applications when there
were equal numbers of unhatched and freshly hatched egg masses. After three
seasons, Populus trees protected by Bt sprays had produced between 50 and 73%
more above-ground volume than their unprotected counterparts (Coyle et al. 2002b).
Because the early life stages are the most vulnerable, population monitoring is an
essential aspect of C. scripta management. Coyle et al. (2000) visually determined
C. scripta life stages; however, this was time consuming and required experienced
personnel able to recognize the various life stages. Nebeker et al. (2001) used boll
weevil traps to monitor adult C. scripta field populations. Traps provided
information on population levels and the current life stage in the field. This
information could be used in conjunction with biorational sprays. C. scripta
emergence was easily detectable, as extremely large numbers were caught within 1-
2 days. After emergence, adult C. scripta undergo a 5-7 day feeding period during
which they become sexually mature (Burkot and Benjamin 1979). Traps can
indicate when each beetle generation emerges, and plantation managers can use this
information, along with the knowledge of the maturation feeding period, to best
predict the most optimal time to apply treatment.
Degree-day (DD) calculations also can be used to predict appropriate spraying
times. Burkot and Benjamin (1979) found that C. scripta generations required
between 222 and 273 DD depending on the generation and temperature. Similarly,
Jarrard (1997) examined the DD requirements on C. scripta in Iowa. This study

observed requirements of between 229 and 317 DD per generation. Jarrard (1997)
also found that observed DD requirements were very similar (all within 35 DD) to
model-based predicted values. Two studies examined C. scripta DD requirements
in Mississippi, USA. Pope and Nebeker (2002) and Nebeker et al. (2001) required
281 DD and 280 DD, respectively, for one C. scripta generation. Their results
agreed closely with those of Jarrard (1997). This information is of significant
importance. Because DD models seem to be adequate predictors of C. scripta life
stages, we can estimate when each C. scripta generation will occur in the field and
treat accordingly. Jarrard (1997) found that predicted DD requirements were within
two calendar days of development observed in the field. This information can be
used to create a better spray schedule based on insect life stage rather than on a strict
calendar schedule. This will save not only time and money, but will reduce
insecticide applications to plantation Populus.
Insecticide applications can be reduced further by incorporating an accurate
economic injury level (EIL) (Pedigo et al. 1986) for C. scripta on plantation
Populus. Fang and Hart (2000) examined the relationship between larval C. scripta
population levels and subsequent plant damage. This study also showed that egg
mass densities may be a useful indicator of potential defoliation. A concurrent study
by Fang (1997) integrated several factors and derived an EIL for C. scripta of 0.2 –
0.9 egg masses per terminal for the second generation. Populations below this level
were not predicted to cause sufficient economic loss to justify pesticide application.
Economic gain would occur only when populations or damage above the EIL were
treated.
Natural enemies do contribute to C. scripta population control, but seemingly
not to a great extent in commercial plantations. Burkot and Benjamin (1979)
examined the natural enemies responsible for C. scripta mortality in Wisconsin.
Natural enemies had the least effect on C. scripta populations during the first C.
scripta generation, yet exhibited greater control in successive generations. This was
primarily accomplished by coccinellid predation on egg masses and pupal parasitism
by a parasitic wasp, Schizonatus latus Walker (Hymenoptera: Pteromalidae).
Schizonatus latus parasitized over 25% of the pupae during the third C. scripta
generation, and coccinellids accounted for up to 25% of egg mortality in the fourth
generation. Jarrard (1997) examined the natural enemy complex in central Iowa.
Similar to the study in Wisconsin, coccinellid predators were the most numerous C.
scripta natural enemy. The greatest natural enemy influence occurred on egg
masses in the second C. scripta generation, where over 70% mortality was recorded.
Thus, natural enemies do exert control on C. scripta populations, primarily in the
sessile (egg and pupal) stages. However, because of the multivoltine lifestyle and
reproductive potential of C. scripta (Coyle et al. 1999) natural enemies alone do not
seem to be able to control populations effectively in plantations.
In summary, many components of an IPM program for C. scripta have been
developed. What is needed is the integration of all the pieces of the puzzle together
in different planting strategies for at least one rotation. This could serve not only to
test the accuracy of the information elucidated to date, but would serve as a
benchmark to determine the most effective directions for additional research.
208 D. COYLE et al.
4. CLONAL DEVELOPMENT AND DEPLOYMENT STRATEGIES FOR

TODAY AND FUTURE RESEARCH NEEDS
Based on our experience to date, the best clonal development strategy appears to be
to breed and select for tolerance and/or resistance to Septoria and Melampsora
diseases and then genetically transform the best clones with the Bt genes or
proteinase inhibitors and other insect resistance mechanisms.
The mosaics of monoclonal stands deployment strategy seems to have the most
potential for large-scale use at this time (Zsuffa et al. 1993), while the high
dose/refugia strategy should be added as soon as the problems with commercial
plantings of transgenic clones are satisfactorily addressed. Matching clones to
specific soil conditions or production objectives will increase the efficacy of these
systems further. An obvious, but sometimes overlooked, issue is that clonal
deployment strategies can not overcome poor quality clones if they are used in
plantings (Zsuffa et al. 1993).
To ensure clonal diversity and therefore protect clone longevity and plantation
success, Hall (1993) recommends the following: 1) establish a maximum block size
that can be planted to one clone, 2) prohibit two fields of the same clone from
bordering one another, and 3) within any one growing region, no clone should make
up any more than 15% of the plantings in any given year. Empirical research on
commercial plantations will probably be the only practical way to refine these
recommendations.
While we believe that host plant resistance is an important pest management
tool, other aspects of IPM also should be examined in order to effectively utilize the
various approaches available and reduce the selective pressures on the target pest
(Hart et al. 1992). Incorporating effective clonal deployment strategies with host
plant resistance and other IPM tactics will reduce selective pressure even further.
We also must remember that SRWC plantations are delicate biological systems.
Systematic monitoring for the efficacy of the resistance trait is necessary, as is the
continued search for potential new pests and new pest management tactics.
ACKNOWLEDGEMENTS
Preparation of this manuscript was sponsored by the Bioenergy Feedstock Development
Program of the U. S. Department of Energy under contract DE-AC05-00OR22725 with
University of Tennessee-Battelle LLC. Partial Funding was provided by the Department of
Energy-Savannah River Operations office through the Forest Service Savannah River and the
Forest Service Southern Research Station under Interagency Agreement DE-IA09-
00SR22188. We thank the book editors for inviting us to speak and write on this subject.
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CHAPTER 10
STRATEGIES FOR DEPLOYMENT OF INSECT

RESISTANT ORNAMENTAL PLANTS
Substantial Hurdles, Vast Potential
DANIEL A. HERMS
Department of Entomology, The Ohio State University, Ohio Agricultural Research and
Development Center, 1680 Madison Ave., Wooster, OH 44691 USA
1. INTRODUCTION
In the 50 years since Painter (1951) published his landmark treatise, host plant
resistance (HPR) has become a central component of IPM programs for many
agronomic crops (e.g. Beck, 1965; Gracen, 1986; Smith, 1989; Stoner, 1996). HPR
has also long been recognized as an ideal pest management strategy for ornamental
plants and shade trees (Felt, 1905; Houser, 1918; Weidhaas, 1976; Morgan et al.,
1978; Nielsen, 1989). Despite this great potential, Weidhaas (1976) questioned
whether host plant resistance was a practical goal. His pessimistic forecast has been
confirmed, as little progress has been made over the past 25 years. Deployment of
resistant germplasm remains virtually ignored as a management tool for insect pests
in urban forests and ornamental landscapes (Morgan et al., 1978; Nielsen, 1989;
Raupp et al., 1992).
Recent trends provide reasons for optimism. As social and regulatory pressures
act to decrease the use of pesticides in urban areas (Shaw, 1998), host plant
resistance is receiving increased attention from researchers and appreciation from
the horticulture industry as a pest management tool for ornamental plants (e.g.
Aker, 1998). In this chapter, I review the progress that has been made toward
development and deployment of insect resistant ornamental plants, as well as toward
understanding the effects of environmental stress and cultural practices on
expression of resistance.
217
218 D.A. HERMS
2. FACTORS CONSTRAINING THE DEPLOYMENT OF INSECT

RESISTANT ORNAMENTAL PLANTS
A number of reasons have been cited as justification for increased emphasis on
development of pest resistant ornamental plants, including the great economic value
of shade trees and ornamental plants as well as the high cost of their maintenance
(Potter, 1986; Wu et al., 1991; Raupp et al., 1992), the desire to decrease pesticide
applications in urban areas (Olkowski et al., 1976; Raupp et al., 1992; Shaw, 1998),
the potential long-term effectiveness of HPR, and its low cost of implementation
once resistant plants are developed (Weidhaas, 1976; Santamour, 1977). However,
a number of factors have constrained the development and deployment of host plant
resistance (Weidhaas, 1976; Morgan et al., 1978; Nielsen, 1989; Raupp et al., 1992).
Historically, nurseries have experienced very little demand from the market place
for insect resistant plants, and plant improvement programs have focused largely on
ornamental traits such as flower color and growth habit (e.g. Erstad & Hansen,
1990). Because ornamental plants are valued for their beauty and appearance,
resistance must be very effective to be a viable pest management tool. Pest
populations must be maintained below thresholds that mar aesthetic appearance,
which may be far lower than those that decrease growth or otherwise physiologically
impact the plant (Sadof & Raupp, 1997).
The great diversity of ornamental plants and their associated pests (e.g. Johnson
& Lyon, 1988) also complicates efforts to develop resistant plants. Many species
are plagued by multiple key pests, and genotypes resistant to one may lack
resistance to others (Weidhaas, 1976). This tremendous biodiversity has also diluted
efforts of the few researchers focused on insect resistance of woody ornamental
plants. Few systems attract the attention of more than one researcher, and resources
are insufficient to investigate the vast majority of plant-insect interactions.
Furthermore, there has been little logistical and funding support for the long-term,
interdisciplinary research programs necessary to develop and evaluate insect
resistant trees (Hanover, 1975; Morgan et al., 1978; Nielsen, 1989).
3. DEVELOPMENT AND IDENTIFICATION OF INSECT RESISTANT

GERMPLASM
Despite these constraints, progress is being made. For example, insect resistance
has been a primary objective of the breeding and selection program of the U.S.
National Arboretum (Santamour, 1977; Aker, 1998). Of the three primary
approaches for developing insect resistant germplasm, evaluating existing genotypes
for resistance has more potential, at least in the short-term, than does classical
breeding (including hybridization) or genetic engineering. A review of the literature
reveals a substantial acceleration over the last 10 years in the screening of
ornamental plants for insect resistance (see Section 3.3).
DEPLOYMENT OF INSECT RESISTANT ORNAMENTAL PLANTS 219
3.1 CLASSICAL BREEDING

There are numerous examples in which classical breeding has been used
successfully to generate insect resistant agricultural plants (e.g. Gracen, 1986;
Smith, 1989; Stoner, 1996). However, due to lack of funding and logistical
difficulties associated with conducting long-term, multidisciplinary research,
classical breeding (including hybridization) of woody plants specifically for insect
resistance has received very little attention (Hanover, 1975; Raupp et al., 1992).
Breeding of woody plants for disease resistance has received more attention (e.g.
Santamour, 1977; Aker, 1998), with attempts to develop Dutch elm disease resistant
elms (Ulmus) at the forefront of these efforts (e.g. Karnosky, 1979; Ware, 1992).
Many of these elm genotypes have now been screened for resistance to key insect
pests (see Table 1, Section 3.3).
3.2 TRANSGENIC TREES

The potential benefits and risks of enhancing insect resistance of trees through
genetic engineering are well recognized (Raffa, 1989; Strauss et al., 1991; Rogers &
Parkes, 1995). However, genetic modification of ornamental plants for insect
resistance has received little attention. Most woody plants that have been
genetically modified for insect resistance, such as hybrid poplars (Populus)
(Robison et al., 1994) and some fruit trees (Snow & Palma, 1997), are not widely
used as ornamental plants or shade trees. Sweetgum (Liquidambar styraciflua),
which is commonly planted as a shade tree, is an exception. Sweetgums that were
genetically modified to over-express tobacco peroxidase showed higher levels of
resistance to gypsy moth (Lymantria dispar) than did wild-type trees (Dowd et al.,
1998).
Genetic engineering clearly offers great potential for enhancing insect resistance
of ornamental plants, but current backlash against transgenic crops suggests that the
public may not be ready to accept genetically modified ornamental plants.
Furthermore, many ornamental plants are themselves native species, or have close
relatives among the native flora, creating potential for gene flow from genetically-
modified ornamental species to their wild relatives (Rogers & Parkes, 1995; Snow &
Palma, 1997). This risk is further aggravated by the long-lived nature of woody
plants, coupled with the fact that many are cultivated specifically because of the
ornamental value of their reproductive structures, although this problem potentially
could be mitigated by insertion of genes that confer sterility.
3.3 SCREENING FOR RESISTANCE

Horticulturists have selected and bred for substantial genetic diversity within many
taxa of ornamental plants, much of which is maintained through asexual
propagation. Screening existing genotypes represents a practical and cost-effective
opportunity for identification and deployment of insect resistant germplasm
(Santamour, 1977; Raupp et al., 1992). Smith-Fiola (1995) compiled a
220 D.A. HERMS
comprehensive list of ornamental plants for which published claims of insect and
disease resistance have been made. However, not all of these claims have been
substantiated by rigorous screening. An example of the pitfalls of resistance claims
based on observational evidence is discussed below. Peer-reviewed studies in which
woody ornamental plants were screened for their resistance to key insect pests have
increased substantially in recent years, and are catalogued in Table 1. Virtually all
reveal substantial variation in insect resistance. Many taxa have also been evaluated
for their suitability as hosts to gypsy moth (Peterson & Smitley, 1991; Liebhold et
al., 1995), which is an increasingly important pest in urban forests as it continues to
expand its range in the United States (Czerwinski & Isman, 1986; Ticehurst &
Finley, 1988). Although screening creates potential for immediate deployment of
resistant germplasm in ornamental plantings and urban forests, there is little
evidence that host plant resistance has yet to be adopted as a pest management
strategy.
--- Continued ---

--- Continued ---

222 D.A. HERMS
3.3.1 CASE STUDY: THE SEARCH FOR BRONZE BIRCH BORER

RESISTANT WHITE-BARKED BIRCHES
In a rigorous example of resistance screening, David G. Nielsen has conducted a 20-
year, large-scale field study of interspecific variation in birch (Betula spp.)
resistance to bronze birch borer (Agrilus anxius) at The Ohio State University’s
Ohio Agricultural Research and Development Center in Wooster (Nielsen & Herms,
in preparation). White-barked birches are highly valued as landscape plants
(Weaver, 1978; Dirr, 1981). Historically, European white birch (Betula pendula)
was the most commonly cultivated birch, because it grows rapidly and develops
white bark at a young age (Santamour, 1982; Schilling, 1984). However,
infestations by bronze birch borer have dramatically curtailed its use in landscapes
(Ball & Simmons, 1980). Larvae feed under the bark on phloem tissue, which
girdles and often kills the tree (Anderson, 1944; Barter, 1957). The high
susceptibility of European white birch to bronze birch borer spawned a search for
other white birches suitable for landscapes (Dirr, 1981), with bronze birch borer
resistance specified as the “single major selection criterion for landscape use”
(Santamour & McArdle, 1989).
Nielsen initiated his study in 1979 by planting eight species of birch (a total of
1200 trees) in a randomized complete block design. Species tested included the
European species B. pendula and B. pubescens, the Asian species B.
maximowicziana and B. platyphylla var. szechuanica, and the North American
species B. papyrifera, B. populifolia ‘Whitespire’, and B. nigra. B. populifolia
‘Whitespire’ was initially misidentified as B. platyphylla var. japonica, which is
native to Asia. Recently, chemotaxonomic and morphological evidence has
confirmed its identity as B. populifolia (Santamour & Lundgren, 1996).
Bronze birch borer colonization and tree mortality were quantified throughout
the 1980s and again in 1999. Bronze birch borer infestations, which were first
detected in the plots in 1982, had resulted in 100% mortality of B. p. var.
szechuanica, B. pendula, and B. pubescens by 1986 (Table 2). Intensive
quantification of larval colonization and successful adult emergence confirmed that
mortality was caused by bronze birch borer. By 1990, bronze birch borer had killed
86% of B. maximowicziana, and all individuals were dead by 1999. B. papyrifera
and B. populifolia ‘Whitespire’ experienced much lower levels of infestation (Table
2). Mortality of both species increased slightly between 1988 and 1990, possibly as
a result of the severe 1988 drought, which triggered substantial mortality of native
B. papyrifera throughout forests of the Great Lakes region (Jones et al., 1993). The
minimal amount of mortality that did occur in both species between 1990 and 1999
was probably due to canopy closure in the experimental plot. Birches are early
successional species intolerant of shade (Perala & Alm, 1990), and mortality was
concentrated among suppressed individuals.
The high rate of survival of B. papyrifera and B. populifolia ‘Whitespire’ over
the 20-year study, in the face of outbreaks that killed hundreds of neighboring trees,
as well as substantial droughts in 1988 and 1991 (trees were not irrigated), suggests
that these native white-barked birches can be grown successfully in landscapes of
the Midwestern United States. B. nigra (which does not have white bark) showed
no evidence of bronze birch colonization, and virtually no mortality (Table 2),
confirming its suspected immunity to bronze birch borer (Santamour, 1999).
224 D.A. HERMS
Theory of biogeography predicts that geographic variation in herbivore

resistance corresponds with geographic patterns of natural selection exerted by key
herbivores (e.g. Bryant et al., 1994; Swihart et al., 1994). The high level of
resistance in the North American species coupled with complete mortality of the
Asian and European species is consistent with this prediction. Bronze birch borer is
native to North America, as are the species showing the highest level of resistance:
B. nigra, B. papyrifera and B. populifolia. The Asian and European species, which
share no evolutionary history with bronze birch borer, exhibited a very high degree
of susceptibility, suffering 100% mortality. The lack of resistance in Asian and
European species indicate that bronze birch borer will have a devastating impact on
the birch resource on these continents, should it become inadvertently established.
These results stand in stark contrast to claims of bronze birch borer resistance in
B. maximowicziana and B. platyphylla as they were released to the nursery industry
during the 1970s (Kozel & Smith, 1976; Santamour & Clausen, 1979; Dirr, 1981).
That they were eventually proven highly susceptible underscores the pitfalls of
resistance claims based on anecdotal observation and other forms of circumstantial
evidence, which may represent escape from infestation rather than true resistance.
Claims of resistance should be backed by rigorous screening in replicated plantings
that ideally contain genotypes known to be susceptible, which can be used as
“positive controls” to provide a frame of reference.
Santamour and Lundgren (1997) and Santamour (1999) hypothesized that the
absence of the secondary metabolite rhododendrin in the inner bark of birch was
mechanistically associated with resistance to bronze birch borer, and thus could be
used as a screening trait in the selection and breeding of resistant trees. This
hypothesis was based on the observation that river birch (B. nigra) and monarch
birch (B. maximowicziana), both of which they assumed to be borer resistant, do not
contain rhododendrin, while species known to be susceptible do. However, the high
level of susceptibility of monarch birch to bronze birch borer (Table 2) indicates that
the absence of rhododendrin is not a reliable marker for bronze birch borer
resistance, again emphasizing the importance of a rigorous long-term screening
program.
4. ENVIRONMENTAL MODIFICATION OF RESISTANCE: DOES URBAN

STRESS TRIGGER PEST OUTBREAKS?
Plant resistance to insects results from a suite of physical and chemical traits that
decrease the growth and survival of insects, the attractiveness of plants to insects,
and/or the ability of plants to tolerate insect feeding (Painter, 1951). Although
resistance traits are genetically based, their expression can be altered dramatically by
environmental factors, including biotic and abiotic stress and cultural practices such
as fertilization (Painter, 1958).
A large body of predominantly observational evidence has led to the proposition
that a mechanistic relationship exists between plant stress and the population
dynamics of herbivorous insects that is mediated by stress effects on host quality
(Mattson & Haack, 1987). Stress has been proposed to increase the nutritional
quality and/or weaken the natural defenses of plants, thereby increasing insect
fecundity and survival (Rhoades, 1983; White, 1984). This “Stress Hypothesis” is
widely accepted within the horticultural industry, and management
recommendations for enhancing insect resistance of trees have long emphasized
cultural practices that increase tree vigor (Houser, 1918; Nielsen, 1989). However,
recent reviews of empirical studies have concluded that effects of environmental
stress on host plant quality are highly variable, and challenge the generality that
stressed trees are more susceptible to insects (Larsson, 1989; Waring & Cobb, 1992;
Koricheva et al., 1998).
Relative to natural forests, urban environments are clearly more stressful
(Berang et al., 1985; Krizek & Dubik, 1987; Whitlow & Bassuk, 1988; Whitlow et
al., 1992; Kjelgren & Clark, 1993; Craul, 1994; Close et al., 1996a,b; Cregg & Dix,
2001). Trees in urban sites experience greater drought stress because of higher
temperatures, restricted rooting zones, compacted soil, and decreased water
infiltration due to impervious surfaces. Urban environments are also often
characterized by soils deficient in organic matter and nutrients, air pollution, deicing
chemicals, and increased incidence of mechanical injury.
In natural forests, stress quickly eliminates seedlings or saplings that are not at
least reasonably well adapted to the site on which they happen to establish. Trees
that do become established acclimate to stress via a suite of phenotypic responses
that enhance stress tolerance, including increased root:shoot ratios, increased
accumulation of storage reserves, and higher concentrations of secondary
metabolites (Chapin, 1991; Chapin et al., 1993). But in urban forests and
ornamental landscapes, trees and shrubs are often planted with little consideration as
to whether they are actually adapted to the stresses associated with the particular site
(Nielsen, 1989; Raupp et al., 1992), which may dramatically decrease their ability to
acclimate to stress.
Numerous cases have been documented of insect outbreaks in urban forests by
species that rarely, if ever, reach high densities in natural forests (Frankie & Ehler,
1978; Dreistadt et al., 1990). Stress effects on host quality have been implicated as
a key causal factor (Nielsen, 1989; Dreistadt et al., 1990; McIntyre, 2000).
However, the generality of this pattern has been questioned by Nuckols and Connor
(1995), who found that trees in ornamental plantings did not receive more herbivory
than conspecifics in natural forests (although, they did not actually quantify insect
performance or other measures of host plant resistance).
Only a few studies have actually examined the relationship between urban stress
and insect infestation. In urban environments, Speight et al. (1998) reported that the
density of horse chestnut scale (Pulvinaria regalis) was highest where water and
nutrient infiltration was inhibited by impermeable surface substrate under the trees.
They concluded that higher insect densities resulted because stress enhanced host
quality. However, they did not examine host plant effects on fecundity or survival.
In general, drought stress has been found to decrease host quality of woody plants
for sucking insects (Koricheva et al., 1998). For example, Hanks and Denno (1993)
found that survival of the armored scale Pseudaulacaspis pentagona on mulberry
226 D.A. HERMS
(Morus alba) was lower on water stressed trees in urban environments than on trees
in forested sites that experienced less stress, challenging the idea that stressed trees
are better hosts.
Effects of drought stress on folivores also have been variable. Water stress
decreased folivore performance in some cases (e.g. Craig et al., 1991; Mopper &
Whitham, 1992; Floater, 1997). However, other studies reached the opposite
conclusion (Thomas & Hodkinson, 1991; Cobb et al., 1997), or found effects to be
minimal (McCullough & Wagner, 1987; Talhouk et al., 1990). Studies with bark
beetles have also reached conflicting conclusions. In some studies, stressed trees
were the most susceptible and fastest growing trees the most resistant (e.g. Larsson
et al., 1983; Wright et al., 1984; Waring & Pitman, 1985). However, Lorio and his
colleagues have concluded that moderately stressed loblolly pine (Pinus taeda) trees
are more resistant to southern pine beetle (Dendroctonus frontalis) than are faster
growing trees (Lorio, 1986; Reeve et al., 1995; Wilkens et al., 1997). Similarly,
white pine weevil (Pissodes strobi) preferred to feed on bark from nonstressed white
pine trees (P. strobus) over bark from drought stressed trees (Lavallée et al., 1994).
It has been proposed that stress effects on insect resistance may be nonlinear,
with moderately stressed trees more resistant to herbivores than either severely
stressed or rapidly growing trees (Lorio, 1986; Mattson & Haack, 1987; Larsson,
1989; Herms & Mattson, 1992). The existence of quadratic effects of stress on
herbivore resistance provides a potential explanation for otherwise contradictory
results of stress studies (e.g. English-Loeb, 1989). While evidence for quadratic
responses is very limited, there is some. For example, Lorio and his colleagues
found that when moderate drought stress decreased growth of loblolly pine without
affecting photosynthesis, production of constitutive levels of trunk resin increased
(Reeve et al., 1995), which decreased the reproductive success of southern pine
beetle. But when severe drought stress decreased both growth and photosynthesis,
resin production decreased (Dunn & Lorio, 1993).
Ozone may be an important predisposing stress in tree decline, particularly in
urban forests (Kozlowski, 1980; Pye, 1988; Taylor et al., 1994; MacKenzie et al.,
1995; Schmieden & Wild, 1995). It has been proposed that ozone stress may
decrease tree resistance to insects (Hain, 1987), but this has been investigated in
only a few cases. Experimental ozone fumigation decreased resistance of quaking
aspen (Populus tremuloides) to four species of outbreak Lepidoptera (Herms et al.,
1996), but this does not seem to be a general pattern. Ozone exposure had no effect
on host quality of sugar maple (Acer saccharum) or hybrid poplar as hosts for gypsy
moth (Lindroth et al., 1993). Similarly, exposure of cottonwood (Populus deltoides)
to ozone had no effect on the aphid Chaitophorus populicola (Coleman & Jones,
1988a). Ozone did decrease the growth and fecundity of the cottonwood leaf beetle
(Plagiodera versicolora). However, this insect preferred to feed on, and consumed
more foliage of, plants exposed to elevated ozone (Coleman & Jones, 1988b; Jones
& Coleman, 1988). Gypsy moth preferentially fed on white oak (Quercus alba)
foliage exposed to the highest concentration of ozone (about 3X ambient), but
preferred foliage exposed to ambient air over that exposed to intermediate levels of
ozone (Jeffords & Endress, 1984).
Atmospheric nitrogen deposition also imposes a substantial anthropomorphic

impact on natural and urban forests (Taylor et al., 1994). Deposition of nitrogen
originating from fossil fuel combustion increases available nitrogen in the soil,
resulting in increased foliar nitrogen concentration of trees (Johnson, 1992; Fenn et
al., 1998). Numerous studies have shown that increased nitrogen availability
frequently decreases tree resistance to insects by increasing nutrient and/or
decreasing secondary metabolite concentrations (Mattson, 1980; Herms & Mattson,
1992; Kytö et al., 1996). For example, in Australia, atmospheric nitrogen deposition
has been implicated in the increased susceptibility of Eucalyptus forests to
defoliation (Landsberg, 1990).
Wood borers deserve special attention because of their often lethal impact on
trees. There is substantial evidence that stressed trees are more susceptible to wood
borers (e.g. Anderson, 1944; Wargo, 1977; Dunn et al., 1986; Potter et al., 1988;
Dunn et al., 1990; Hanks et al., 1999). For example, Cregg and Dix (2001) found
that green ash (Fraxinus pennsylvanica) planted in a downtown urban environment
experienced more severe drought stress and suffered higher levels of borer damage
than trees planted on a park-like campus. Consideration by landscape architects and
designers of the ecological requirements and adaptations of trees when deciding
where to locate plants could help reduce urban stress (e.g. Flint, 1985) and thus
incidence of borer infestation. For example, flowering dogwood (Cornus florida) is
an understory tree that poorly tolerates mid-day water stress compared to species
adapted to full sun (Bahari et al., 1985). Not surprisingly, Potter and Timmons
(1981) found that dogwood trees planted in full sun were much more susceptible to
colonization by dogwood borer (Synanthedon scitula) than were trees planted in at
least partial shade.
It is obvious that the effects of environmental stress on tree resistance to
herbivores are highly variable and complex (Larsson, 1989; Waring & Cobb, 1992;
Koricheva et al., 1998). Evidence suggests that effects of stress on herbivore
performance will be dependent on the outcome of the three-way interaction between
(1) the type, timing, and intensity of stress (e.g. McMillin & Wagner, 1995), (2) the
physiological response of the plant, and (3) the behavior, physiology, and life
history of the herbivore (Mattson & Haack, 1987; Larsson, 1989; Jones & Coleman,
1991; Koricheva et al., 1998).
Further research clearly is necessary before a solid predictive framework will
emerge. However, it is also clear that, with the exception of wood borers, there is
little evidence to support the hypothesis that urban stress generally decreases tree
resistance to insects, or that stress effects on host quality are responsible for
destabilizing herbivore population dynamics in urban environments. Other factors
may have more important effects on the population dynamics of insect herbivores in
urban forests. For example, the regulating effects of natural enemies generally may
be weaker in urban forests (e.g. Houser, 1918; Frankie & Ehler, 1978; Hanks &
Denno, 1993; Ruszczyk, 1996).
228 D.A. HERMS
5. FERTILIZATION AND TREE RESISTANCE TO INSECTS:

REASSESSING AN ENTRENCHED PARADIGM
Fertilization is one of the most common tree maintenance practices in ornamental
landscapes (Braman et al., 1998), based in large part on the rationale that it enhances
pest resistance by increasing tree vigor (Potter, 1986; Rathjens & Funk, 1986; Neely
& Himelick, 1987; Nielsen, 1989; Iles, 2000). However, there is little evidence to
support this claim (Raupp et al., 1992). Indeed, in a recent review, Kytö et al.
(1996) concluded that “where a statistically significant effect of (nitrogen)
fertilization on insect performance (body size, development time, survival) was
recorded, it was nearly always beneficial for the insects.”
Fertilization has been shown, for example, to decrease tree resistance to spider
mites (Wermelinger et al., 1985), aphids (Wainhouse et al., 1998), scales (McClure,
1980), adelgids (McClure, 1991), caterpillars (Bryant et al., 1987; Mason et al.,
1992), sawflies (Popp et al., 1986; Wainhouse et al., 1998), leaf beetles (Lawler et
al., 1997), leafminers (Marino et al., 1993), and browsing mammals (Nams et al.,
1996), as well as shoot and stem borers, including Nantucket pine tip moth
(Rhyacionia frustrana) (Ross & Berisford, 1990) and white pine weevil (Xydias &
Leaf, 1964). Recent evidence also indicates that fertilization may also decrease
loblolly pine resistance to bark beetles by decreasing constitutive resin flow
(Wilkens et al., 1997; Warren et al., 1999), which has been shown to affect the
reproductive success of southern pine beetle (Reeve et al., 1995).
In general, the beneficial effects of fertilization on herbivores have been
associated with fertilization-induced increases in plant nitrogen content and
decreases in secondary metabolite concentrations (Mattson, 1980; Bryant et al.,
1983; Herms & Mattson, 1992; Kytö et al., 1996). However, not all studies found
fertilization to decrease the resistance of woody plants to insects, or to decrease
secondary metabolite concentrations. For example, in extremely nutrient deficient
forests, fertilization of jack pine (P. banksiana) (McCullough & Kulman, 1991) and
Scots pine (Pinus sylvestris) (Björkman et al., 1991) increased foliar nitrogen and
monoterpene concentrations. Sawfly performance was not affected in either study,
perhaps because negative effects of increased terpene concentrations on host quality
were offset by positive effects of increased foliar nitrogen.
In summary, there is little evidence to support the paradigm entrenched within
the tree care industry that fertilization enhances insect resistance of trees. In fact,
substantial evidence demonstrates that fertilization almost always decreases tree
resistance to herbivores.
6. SUMMARY
Host plant resistance has been recognized as an ideal pest management strategy for
ornamental plants and shade trees for many years. Yet, little progress has been
made in the deployment of resistant germplasm in urban forests and ornamental
landscapes. A number of factors have constrained the development and deployment
of insect resistant ornamental plants, including lack of market demand for insect
resistant plants, and low pest thresholds for plants valued for their aesthetic
appearance. The great diversity of ornamental plants and their associated pests both
complicates efforts to develop resistant plants and dilutes the efforts of the few
researchers working in this area. Furthermore, there has been little logistical and
funding support for the long-term, interdisciplinary research programs necessary to
breed and evaluate insect resistant ornamental plants.
The future looks brighter. Horticulturists have selected and maintained
substantial genetic diversity, which provides a golden opportunity for identification,
selection, and deployment of insect resistant species and cultivars. Indeed, this
genetic variation increasingly is being screened for insect resistance. Claims of
resistance should be rigorously substantiated, as erroneous claims based on
observational evidence have plagued the landscape industry in the past.
Although resistance traits are genetically based, their expression can be altered
dramatically by the environment. It has been widely accepted within the landscape
industry that stressed plants are more susceptible to insects, and IPM programs have
emphasized cultural practices that increase tree vigor. Furthermore, effects of urban
stress on tree resistance to insects is frequently cited as triggering outbreaks of
insects in urban forests that rarely, if ever, reach high densities in natural forests.
However, experimental evidence does not support this generality. The effects of
environmental stress on tree resistance to herbivores are highly variable and
complex. With the exception of wood borers, there is little evidence that urban
stress generally decreases tree resistance to insects, or that stress effects on host
quality are responsible for destabilizing herbivore population dynamics in urban
environments. In many cases, stressed trees were found to be more resistant to
insects.
Nor is there evidence to support the entrenched paradigm that fertilization
enhances pest resistance by increasing tree vigor. Indeed, the vast majority of
studies conclude that fertilization favors insects and mites, although some have
found that fertilization had no effect on tree resistance to insects. I am not aware of
any studies that show fertilization to increase the resistance of trees to herbivores.
In 1976, Weidhaas questioned whether host plant resistance was a practical goal
for shade trees and other ornamental plants. So far, his pessimistic forecast has been
confirmed. Little progress has been made in the deployment of resistant germplasm.
However, research focused on identification of insect resistant germplasm, as well
as understanding how environmental stress and management practices impact the
expression of resistance, has accelerated. There is also evidence that the value of
host plant resistance as a pest management tool is increasingly appreciated by the
Green Industry. These trends provide reason for optimism that the next 25 years
will see substantial progress towards unleashing the vast potential of host plant
resistance as a management tool for insect pests in urban forests and ornamental
landscapes.
230 D.A. HERMS
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CHAPTER 11
POSSIBILITIES TO UTILIZE TREE RESISTANCE

TO INSECTS IN FOREST PEST MANAGEMENT IN
CENTRAL AND WESTERN EUROPE
(1) (2)
C.M.HEIDGER AND F.LIEUTIER
(1) Hochschule Zittau/Goerlitz (FH) Univ.of Applied Sciences,Dept.of Ecology and

Environmental Management, P.O.Box 261, D-02755 Zittau, Germany.
(2) Univ. Orléans , Laboratoire de Biologie des Ligneux et des Grandes Cultures, B.P. 6759,
F. -45067 Orléans Cedex, France.
1. INTRODUCTION
Temperate forest ecosystems are the historic natural vegetation in Central and
Western Europe. Broad leaved trees are dominant (Ellenberg, 1996). Beech (Fagus
sylvatica) is dominant in all stands with average moisture and soil condition. Under
dryer conditions, such as in the lowlands, oak species (Quercus robur and Quercus
petraea) are dominant. Only under very unfavorable dry or wet conditions pine
(Pinus sylvestris) occurs as natural stands. Spruce (Picea abies) only occurs in the
higher altitudes, as in the Alps or the Bavarian forest and reaches its maximum
western natural distribution in the lowlands at the river Wisla (Ellenberg, 1996).
Presently in Central Europe the actual forests in large areas do not consist of
historic natural vegetation, but of plantations in which broad leaved trees in the last
centuries have been replaced by spruce and pine over a large range. Therefore the
former dominance of broad leaved trees was converted to one of conifers (Plachter,
1991). In Western Europe, Great Britain and Ireland most forest stands were
converted to arable land and the rest of the forests mainly consist of plantations. In
France also, broad leaved trees were replaced by spruce and pine through forestry,
but also in many locations broad leaved trees were planted in their natural
distribution range. So even if planted, the French forests correspond in many places
239
240 C.M.HEIDGER and F.LIEUTIER
to the natural vegetation. Conifers have been planted especially in mountain areas,
but sometimes, as in the Massif Central, in the place of broad leaved trees in low
mountain areas. Also, as in central Europe, even at very low altitudes, conifers have
replaced broad leaved trees in large areas such as in the southeast in place of
Quercus ilex and Quercus suber and in the region of Orleans in place of Q. petraea
and Q. robur.
Consequently, the most relevant forest trees for our discussion of resistance in
Central and Western Europe presently are Norway spruce (Picea abies), Scots pine
(Pinus sylvestris), Maritime pine (Pinus pinaster), beech (Fagus sylvatica) and
several oak species (Quercus petraea, Q. robur, Q. pubescens, Q. suber, Q. ilex).
In this area, those species are attacked by several pests among which the most
aggressive belong to the bark beetles, weevils and Lepidoptera, and to a lesser
extent, aphids and scale insects (Table 1). Damage can be considerable. For
example, in the beginning of the 90´s, the bark beetle Ips typographus killed over 30
million of spruce in 2-3 years, which can be estimated at a loss of about 750
million Euros. In the 70`s, the Mediterranean scale Matsucoccus feytaudi Duc. has
been responsible for the destruction of most maritime pine plantations in
Southeastern France. The pine processionnary moth Thaumetopoea pityocampa
causes periodic damage in Mediterranean pines. Generally, broadleaved trees are
less damaged than conifers, although defoliators such as Tortrix viridana or
Lymantria dispar can cause spectacular outbreaks on oak.
Trees however, as all living organisms, are able to defend themselves against
biotic aggressions, at least to some extent. They have developed resistance
mechanisms against all of these insects and the existence of more or less long
periods without damage proves that these natural mechanisms are efficient most of
the time. It could thus be an efficient and environmentally friendly strategy for the
forester, in the context of pest management in a sustainable forest, to try and utilize
these resistance mechanisms to control insect pests and to improve forest health.
In the present chapter, after briefly reviewed the main mechanisms of resistance
in trees and the factors which can make resistance levels vary, we suggest
possibilities to utilize tree resistance for forest protection and give examples of such
utilization for Central and Western European forest pests.
2. MAIN MECHANISMS OF RESISTANCE IN TREES

These mechanisms depend essentially on the location of damage in the host and the
feeding behavior of the pest (defoliator, sap-sucking, phloem feeders, xylophagous).
In Central and Western Europe, several investigations in this field have been
undertaken for the insects in Table 1, revealing different kinds of plant resistance
mechanisms, which range from avoiding the pest to constitutive and induced local or
systemic defense.
POSSIBILITIES TO UTILIZE TREE RESISTANCE 241
2.1 AVOIDING THE PEST

The life cycle of the pest and that of the host must often be strictly synchronized to
allow the feeding stages of the insect to find the appropriate organ of the tree at the
right stage of development. If the plant develops genotypes with a different
--- Continued ---

phenology, the coincidence between its life cycle and that of the insect is largely
broken, and the sensitive pest stage cannot develop on a wide scale. A resistance is
thus created in the tree by avoiding the pest attack in time.
One good example is the phenological resistance of oak spp. to the green oak
leafroller Tortrix viridana. In spring, the newly hatched larvae rapidly enter the
flushing buds of their host to feed and develop. This is possible however, only if
hatching occurs not too early for the buds to be tender enough, and not too late for
the larvae not to be rejected outward by the rapidly developing foliage. The extent
of damage to the foliage thus varies depending on climatic conditions which can
allow phenological asynchrony between egg hatching and bud flushing from one
year to another, but it also depends on the genetic characteristics of the trees.
Generally, late flushing trees escape defoliation (Du Merle, 1988). However, T.
viridana is able to adapt to the phenologically different oak species and ecotypes
(Du Merle, 1983). This is due to genetically fixed differences in egg hatching dates,
through which each green oak leafroller population is specialized on a certain
phenological type of oak (Altenkirch, 1966; Rubtsova, 1977, 1981; Du Merle, 1983).
Also in the case of Lymantria monacha, phenological variations of its host
(Norway spruce) cause resistance, whereas late flushing individual trees are less
affected by the moth. But genetic selection of the late ecotype raised the attack level
of Lygaeonematus abietinus (Tenthredinidae) and caused heavy infestations by this
insect (Bouvarel & Lemoine 1957). Phenological asynchrony reducing insect attack
was also reported by Thielges & Campbell (1972) for Adelges abietis attacking
Picea abies.
The strategy of avoiding the pest could be used for applied purposes in Europe
by creating, enhancing or preserving the phenological variability among tree species
in heterogeneous stands under the precondition that the different phenological types
are genetically fixed and therefore can be used in genetic improvement programs.
For example, the bud flushing date with respect to control of T. viridana populations
can vary in such a way among the trees that the average phenological coincidence
between the pest and its host will constantly be as low as possible (Du Merle, 1988).
However it was found by Schütte (1957) that this strategy was not offering much
safety against an outbreak of T. viridana.
2.2 CONSTITUTIVE ( PREFORMED) RESISTANCE

The structures and processes involved in constitutive resistance exist before attacks
occur. Various physical or chemical structures can be involved, but chemically
mediated resistance plays the most important role. In conifers, mainly terpenes and
phenols are involved. These chemicals counteract insect attacks and are involved in
defence against a wide array of aggressors, be they xylophagous, sap-suckers or
defoliators.
The genera Pinus, Picea, and Larix possess a system of resin ducts in phloem
and xylem which contain the primary resin (Bannan, 1936). It consists of axial
ducts in the wood and radial ducts in the phloem and xylem. Such primary resin
ducts can function for 25 years and are responsible for the primary defence reaction
against bark beetle attack (Reid et al., 1967; Berryman, 1972). In addition to resin
terpenes, phenols located in phloem parenchyma cells can also play an important
role in constitutive resistance against bark beetles, and between clone differences
have been demonstrated for stilbenes and flavonoids (Brignolas et al., 1995;
Franceschi et al., 1998) (See also Lieutier, this volume).
Constitutive resistance of Pinus pinaster against the pyralid stem borer
Dioryctria sylvestrella is also genetically determined and terpinolene could be used
to select resistant genotypes of the host species (Jactel et al., 1999), since the attacks
are always most severe on trees with high levels of terpinolene in their volatile
emissions.
In P. pinaster, investigations on the survival after natural infestation by the scale
Matsucoccus feytaudi have also demonstrated a high between-provenance variability
in host resistance (Schvester & Ughetto, 1986). Another example for a sap sucker is
given by the green spruce aphid Elatobium abietinum; its performances varied with
provenance of Picea sitchensis (Day et al., 1999). In most cases, the best growing
provenances were the most resistant ones and insect performance was related to
variations in stilbenes. A relation even existed between aphid infestation and the
bark consumption rate by the bole weevil Hylobius abietis; the more aphids found
on the provenance, the higher was the amount of bark consumed by the weevil (Day
et al., 1999).
In Pinus sylvestris, several families of phenolic compounds have been
characterized (Popoff & Theander, 1977; Niemann, 1979). The toxic effects of the
phenolic content of the foliage from different clones on insects were described by
Thielges (1968) and several other authors and these compounds have been reported
often to be involved in defence mechanisms against defoliating insects (Lunderstädt,
1976, Harborne, 1985). Females of the European pine sawfly Diprion pini oviposit
on different clones of P. sylvestris, but significant host preferences among clones
have been demonstrated. Rohmeder (1954) and Wright & Wilson (1967) found
differences among Scots pine varieties in susceptibility to this insect. Egg and larval
survival varied significantly between clones (Pasquier-Barré & Auger-Rozenberg,
1999). As taxifolin is known as an anti-growth-chemical for insects (Elliger et al.,
1980), absence and presence of taxifolin in different clones were studied (Lebreton
et al. 1990; Yazdani & Lebreton, 1991). Auger et al. (1994) found that high rates of
mortality of D. pini occurred when Scots pine needles contained high concentrations
of taxifolin and taxifolin glucosid. Also, it could be shown that resistant clones that
were toxic for D. pini contained taxifolin (Géri et al., 1994). Those clones were also
toxic for the processionnary caterpillar Thaumetopoea pityocampa and the larvae of
the endangered butterfly Graellsia isabellae.
Preformed resistance also occurs in broad leaved trees. For example, Schopf et
al. (1999) found that the performance of Lymantria dispar was better on Quercus
cerris than on Q. petraea.
Constitutive resistance could be used in genetic improvement programs by
selecting clones with high levels of defence chemicals. However, it is not clear yet if
plants with raised levels of defence chemicals are of practical use because there is
still a lack of information on the genetic differences between the populations of pest
insects and on the reaction of natural enemies of the pest species.
2.3 LOCAL INDUCED DEFENCE
In the case of local induced defence, the structures involved in these resistance
mechanisms are expressed only in response to attack, and this response is located in
the tissues situated in close vicinity to the place of attack. As for constitutive
defenses, all kind of structures can be involved but the chemically mediated
mechanisms generally play the most important role. Local induced defence is also
known to act against various kinds of insect guilds.
Trees react to attack by microorganisms such as bark beetle vectored fungi with
the formation of a necrotic zone around the attack area, both in the phloem and the
sapwood. This is considered as a hypersensitive reaction (Berryman, 1972;
Christiansen et al., 1987). The resistance of conifers to bark beetle attack depends
mainly on the efficiency of these induced local reactions. The reaction seems to be
induced by wounding itself, but also the fungi introduced by the beetle into the
wound can stimulate considerably the development of the reaction (Lieutier et al.,
1995). Drastic changes in phytochemical contents occur in the lesion zone formed
in the tissues around the attack site, especially in phenolics and terpenes. These
chemicals stop the attack by the insect and its associated fungus (Reid et al., 1967;
Berryman, 1969; Raffa and Berryman, 1982; Langström et al., 1992; Lieutier et al.,
1996). According to Christiansen et al. (1999), a Norway spruce tree attacked by
Ips typographus vectored fungus Ceratocystis polonica forms a circle of axial
traumatic resin ducts in the xylem of the stem which produces secondary so called
wound resin. The resistance level of P. abies to Ceratocystis polonica is correlated
with the concentration of resin in the phloem necroses (Christiansen et al., 1987).
Trees with a high production of in the reaction zone are less susceptible
to bark beetle attack (Birgerson, 1989). The resistance is also correlated with a
particular phenolic composition in the reacting tissues, especially with the ability of
the tree to rapidly increase catechin synthesis in the phloem reaction zone (Brignolas
et al., 1995, 1998). Christiansen et al. (1999) also discovered that a Norway spruce
tree that survived bark beetle attack could be more resistant because traumatic resin
ducts formed in the delayed induced reaction described above already existed (For
induced defences against bark beetles see also Lieutier, this volume).
Like in bark beetles, local induced defence could be of greater importance than
constitutive defence in the resistance of P. abies to Pissodes strobi (Lavallée et al.,
1999). Although better known and much more frequent against attacks by
xylophagous insects, local induced defense has also been demonstrated to play a
decisive role in trees attacked by other insect guilds. The resistance of a certain
Norway spruce tree to the females and larvae of the aphid Adelges abietis is related
to the capacity of the tree to rapidly develop a local induced reaction in the buds
around the zone where the fundatryx nymph has inserted its mouth parts (Rohfritsch,
1988).
Local induced defence of trees could be used by selecting or genetically
engineering plants with strong and fast responses to aggressor attacks. Also the
formation of traumatic resin ducts could be used if it would be possible to induce it
in a way that the tree survives with an increased resistance. This could function as a
“vaccination” for endangered stands.
2.4 SYSTEMIC INDUCED DEFENCE

Systemic induced defence results in stimulation of the defence mechanism only after
attack begins. The situation however completely differs from the local induced
defence because the structures or processes concerned are dispersed in the whole
tree instead of being localized at the point of aggression, as insect attacks can
modify the metabolics of phenolics in the whole plant (Wagner, 1988). Due to this
the content of the defence chemicals is raised in the whole plant after attack.
A good example is the resistance of Larix decidua to the larch bud moth
Zeiraphera diniana in the Alps. Periodic outbreaks of this moth could be explained
by induced defence responses of the trees after heavy defoliation. The new needles
growing after heavy defoliation contain more non-digestible fiber material and less
nitrogen than the needles prior to heavy defoliation. This results in reduced food
quality for later moth generations and could play a considerable role in the collapse
of the outbreak (Roques, 1983). It can therefore be called a delayed induced
systemic reaction.
Combined effects of preformed (constitutive) defence and systemic induced
defence were found in the resistance of different clones of Pinus sylvestris to
Diprion pini by Auger et. al (1994). During feeding tests or defoliation a strong
increase in taxifolin glucoside occurred in the needles which was correlated with
tree resistance.
Induced systemic responses could be used in genetic improvement programs by
selecting clones with strong and fast responses in conventional breeding programs,
or by raising levels of such defences in the plants using genetic engineering.
3. FACTORS INFLUENCING TREE RESISTANCE AND

CONSEQUENCES FOR UTILIZATION IN FOREST PEST MANAGEMENT
Very few practical attempts have been made to use tree resistance mechanisms in
forest pest management, but there are several examples in research to clarify
whether those mechanisms can be a tool in forestry. This is a rather difficult task
because the phenotypic response of the tree species to a pest species is determined
by the interaction of different major factors, which also influence the resistance level
of a tree.
Four categories of factors must be considered: 1) the genetic information in the
tree; 2) the genetic information in the pest species; 3) the genetic information in the
pathogens introduced by the pest species; 4) the environmental conditions (moisture,
temperature, nutrient availability, air pollution, soil conditions, competition).
In most investigations, the genetic information in the tree has been investigated
by tests with clones or provenances and, as seen above, many examples of tree
resistance to insects have been demonstrated. However, as emphasized by Bastien
(1999), only a few investigations so far have taken into account the genetic
variability of the insect pests themselves and the pathogens introduced by the pest
species. An example of this is the genetically differing populations of the defoliator
T. viridana specialized on different phenological oak types as pointed out above.
Several investigations in that field are presently being conducted in Europe on other
pest guilds, such as cone and seed insects, sap suckers and bark beetles.
Environmental conditions also influence the level of tree resistance, making
silvicultural practices a potentially important tool to enhance resistance of forest
trees. For example, a susceptible host can become more resistant due to favorable
environmental conditions (e.g. weather) (Lévieux, 1986). This resistance, called
pseudo-resistance, lasts only as long as optimal conditions continue, and is therefore
temporary. In Southern and Central England almost all individuals of Pinus
contorta are attacked by Rhyacionia, but in Scotland the same provenances are not
attacked, thus reflecting the role of environmentally induced pseudo-resistance
(Lévieux, 1986). In this case, the effects of climate impact the performance of the
pest, leading to a situation of resistance in a susceptible provenance. Also, adverse
effects from climate can occur, as in the case of bark beetle attacks in Central
Europe, where warmer climatic conditions allow the bark beetle Ips typographus to
produce more offspring (2 generations per year) than in the natural distribution
range of norway spruce (Heidger, 1994). More trees, even resistant ones, can be
attacked due to higher population levels (Vité, 1984). Another example concerns
Tomicus piniperda. In Northern Europe extensive tree mortality is very rare because
attacks are localized in the shoots only (Langström et al., 1992), but in the warmer
climate of Southern Europe stem attacks and tree mortality occur (Triggiani, 1984).
Consequently, two main possibilities can be considered for the utilization of tree
resistance in forest pest management: 1) tree breeding for genetic resistance, by
taking into account resistance criteria in genetic improvement programs; and 2)
enhancement of the resistance level and efficiency of defense mechanisms in the
trees with the aid of silvicultural practices that optimize environmental conditions.
4. ENHANCEMENT OF RESISTANCE BY GENETIC IMPROVEMENT

PROGRAMS
Some of the resistance mechanisms described above offer the possibility to select
resistant clones for genetic improvement of resistance to insects. However, breeding
for resistance to biotic aggressors is much more complex than to abiotic factors, as
sequential evolution of the pest species or plant-aggressor coevolution can take
place (Holubcik, 1978). Trying to enhance resistance of trees using a single gene is
problematic as resistance can easily be overcome in less than a single tree generation
(Lévieux, 1986). It would thus probably be better to select horizontal resistance
which is more effective over longer time periods. It has been also pointed out that
often monogenic resistance mechanisms can be found, but many tree insect
interactions are complex phenomena being controlled by several loci (Bastien,
1999). There are also practical restrictions for the use of clones because it could
lead to restriction of genetic diversity in the tree population. A special problem is
also to define against which of the different pest species of a certain tree species
resistance should be raised (Führer, 1975). This is even more complicated because of
the various demands of the different insects according to their feeding strategy and
their age class specificity. Tree breeding programs, no matter whether they are
based on classical breeding programs or on the production of transgenic plants, must
thus recognize the need to achieve a durable genetic resistance against the many
aggressors. Again, this is possible only if conservation of genetic variability is part
of the breeding program, otherwise insects and pathogens vectored by them can
easily overcome tree resistance due to their short generation cycles in comparison to
those of the trees. Consequently, for all these reasons and like in agriculture, so
called multiline or polyclonal cultures should only be planted as already
recommended by Holubcik (1978).
Another question is, which genotypes should be selected. According to Führer
(1975), the selection should not be focused necessarily on the most unsuitable
genotypes for the pest. Genotypes that offer it a constant food quality, even under
changing environmental conditions, should be preferred. Indeed, under these
conditions the pest population level would be stabilized because of both a constant
food quality and a high level of natural antagonists due to the constant presence of
the pest, thus avoiding mass outbreak. Such genotypes, stable or unstable under a
changing environment, have already been reported to exist, for example in the
xeromorphism of spruce needles regarding water availability (Führer, 1975).
When selecting resistant genotypes, one must pay attention to the mechanisms
involved in the resistance, especially regarding their specificity for the target
species. A first clue of the problem could be the investigation by Géri et al. (1994)
on Scots pine resistance to the sawfly D. pini. In performance tests on clones that
were unfavorable to D. pini because of their content in certain flavonoid compounds,
the larval development of the butterfly Graellsia isabellae, a rare and protected
species in France, was slowed down and the pupal weight reduced. Also
Thaumetopoea pityocampa was negatively effected through slower larval
development and increased larval mortality. Thus, it has already been demonstrated
that resistant clones of pine can have negative effects on non-target insects.
The main methodologies to be used by the geneticist in order to improve forest

tree resistance are first the search for useful genotypes, directly by screening tree
provenances or clones or indirectly by using resistance markers. The next step is the
use of those genotypes in genetic improvement programs.
4.1 SEARCH FOR USEFUL GENOTYPES

The first step is the search for useful genotypes. To find them the existing genetic
variability of trees and aggressors must be investigated. This is done generally by
exposing clones to natural pest infection as seen in the results presented above.
However, this method raises problems because there is no control of the variability
of the aggressors, or of the level and homogeneity of the attacks (Doudrick et al.,
1996). According to Bastien (1999), the lack of any control of the aggressor
variability is the reason why clonal selection for poplar genotypes resistant to the
rust Melampsora larici-populina turned out to be ineffective 10 years later. Another
possibility is to perform laboratory tests which allow control over the aggressiveness
or pathogenicity of the pest species, the attack level and the environmental
conditions. In this situation however, the number of genotypes and the size of the
experimental design is necessarily limited by the capacities of the laboratory. Also,
due to the artificial environment of the experiment, results may not be replicable in
the field.
The use of markers linked to the tree response to aggressors is an important tool
in the search for resistant genotypes. The important thing is that such indicators,
whether or not involved in a causal relationship with tree resistance to the
aggressors, must be correlated with the host response and resistance level. They can
be biochemical, morphological, physiological or genetic indicators.
4.1.1 Biochemical indicators

Several defensive chemicals (secondary metabolites) involved in the tree response to
biotic aggressors have been proposed as biochemical markers (Bastien, 1999).
Some have been proved to be related to tree resistance and can therefore be used as
indicators of tree resistance to describe or to search for genetic diversity within the
host population. They are summarized in Table 2.
The phenolic composition of the wound resin of Scots pine (Pinus sylvestris)
attacked by Leptographium wingfieldii, a fungus vectored by Tomicus piniperda, is
very likely a chemical marker for resistance, since Bois & Lieutier (1997) found that
high concentrations of taxifolin glucoside in unwounded phloem, and high
concentrations of taxifolin, pinocembrin, pinosylvin and pinosylvin
monomethylether in the reaction zone of wounded phloem could only be found in
the resistant clones. It was also found that a high concentration of p-coumaric acid
in the reaction zone could be an indicator of Scots pine susceptibility.
Similarly, there is a highly significant correlation between ranking clones of
Norway spruce (Picea abies) according to the general phenolic composition of their
phloem and ranking them according to their level of resistance to artificial mass
inoculation by Ceratocystis polonica, a fungus vectored by Ips typographus

(Brignolas et al., 1998). This suggests that the phloem phenolic content could be
used to predict Picea abies resistance to attack by Ips typographus and its associated
fungus. This is also true for some particular phenolic compounds such as
isorharpontin and catechin. The same authors found that the concentration of (+)-
catechin, 6 days after inoculation with the fungus, was higher in the resistant clones
and that isoharpontin concentration was high in the unwounded phloem of the
susceptible clones before any aggression. In another investigation Brignolas et al.
(1995) found that resistant clones of Picea abies contained taxifolin and lower
concentrations of piceid and isoharpontin and showed a higher tanning ability than
those susceptible to C. polonica attack. As isoharpontin and taxifolin glucoside can
be measured in unmanipulated phloem, they are valuable markers of tree
susceptibility and resistance respectively.
Christiansen et al. (1987) have suggested that the most critical variable to
determine is the actual flux of carbohydrates involved in the synthesis of defense
chemicals. However, no attempt has been undertaken yet to try to correlate such
parameters with tree resistance. Instead, a recent study focused on a predominant
role of the local reserves of the tree (Guérard et al., 2000).
Indicators of resistance can also be found in other systems apart from conifers
and bark beetles. Charles (1976) compared the resistance of different pine species to
Rhyacionia buoliana. Pinus halepensis and P. pinaster were more resistant than
Pinus contorta and P. ponderosa, which was attributed to differences in the terpene
profiles.
Intra-specific differences in terpene composition (phellandrene, 3-carene,
camphene) have also been reported (Charles et al. 1982). The terpene 3-carene was
found besides terpinolene in varieties of Pinus sylvestris resistant to Hylobius abietis
attacks (Wright 1976). Jactel et al. (1999) found that the resistance of Pinus pinaster
to Dioryctria sylvestrella was genetically determined and that terpinolene could be
used to select susceptible genotypes.
When testing biochemical indicators of resistance, it is however crucial to take
into account possible physiological variations in the biochemical content of tree
tissues. Auger et al. (1994) showed that taxifolin and taxifolin glucoside
concentrations in Scots pine needles change with season. Taxifolin concentration
peaks in autumn when taxifolin glucoside concentration drops. Taxifolin glucoside
reaches its highest level from June to August when attacks by the sawfly Diprion
pini take place. Seasonal changes in phenolics have also been observed in Q.
petraea by Beres (1984). Moreover, within the same plant, differences in
concentration can occur as leaves in the shaded part of the crown contained lower
levels of taxifolin and taxifolin glucoside than leaves in the sunny part of the crown.
Variations between populations can also make the use of resistance indicators
difficult, as for the interaction between Pinus pinaster and Dioryctria silvestrella.
In tree populations of Southeastern France, Sueron (1982) found a significant
correlation between the terpene profile in bark tissues and resistance to the insect,
but no correlation was found in Corsica. Due to such high physiological variations
between individual trees and under different environmental conditions, the value of
biochemical indicators of resistance is often very low. This however may depend on
the chemical family. Until now, no difference in the phenolic content of Scots pine
phloem could be found after severe experimental water stress, which tends to prove
that phenolics do not vary much with the tree physiological status of the tree (Croise
et al.,
1998). On the other hand, Chiron et al. (2000) observed that ozone pollution
induces a hypersensitive phenolic response in the tree similar to that induced by
fungus inoculations. Since there is no specificity in the tree response this might also
be the case for the markers, and phenolics might thus be indicators of resistance to a
high diversity of abiotic and biotic factors.
4.1.2 Morphological and physiological indicators

In addition to biochemical resistance markers, morphological and physiological
parameters can also be used. In bark beetles the length of beetle galleries or speed of
fungus extension in the phloem or the sapwood can be linked to tree resistance. In
Scots pine, both parameters were larger in clones susceptible to mass inoculation
with Leptographium wingfieldii than in resistant clones (Bois & Lieutier, 2000).
Physiological indicators of tree resistance to bark beetles could also be tree
productivity indices calculated as the ratio between wood production and leaf area
(tree vigor index). Such indices have been demonstrated to be related to the
threshold of attack density above which trees are overcome by natural attacks
(Waring & Pitman, 1983; Mullock & Christiansen, 1986). High tree vigor indices
were never found together with high content of phenolics, which fits with the
growth-differentiation-balance hypothesis (Viiri et al., 1999).
Other structural indicators of resistance to bark beetles could take into account
the polyphenolic parenchyma cells of the phloem. These cells are active in the
synthesis, modification and storage of phenolic compounds and are involved in
constitutive and induced resistance (Franceschi et al., 1998). They have been
reported to be 40% more frequent in P. abies clones resistant to artificial mass
inoculations with C. polonica than in susceptible clones (Franceschi et al., 1998).
A positive relationship exists between the freezing point of Picea sitchensis
needles and the mortality of Elatobium abietinum. Thus the freezing temperature of
the needles could be used as an indicator of the spruce resistance to the aphid (Parry,
1982).
4.1.3 Genetic markers

Recently, genetic markers have been found by Hertel & Kaetzel (1999) for
resistance of P. abies to the aphid Adelges laricis. The NADH-dehydrogenase B -
locus was investigated and it was found that homozygotes with a special isoenzyme
(B1B1) were susceptible to the aphid, while homozygote genotypes with the
isoenzyme (B2B2) were almost completely resistant. This does not mean that this
enzyme influences resistance, but that other genes in the same linkage group might
be involved. With the phosphoglucose-isomerase (Pgi B) locus, another genetic
marker was found for the resistance to the sawfly Pristiphora abietina. Picea abies
clones with the homozygote genotype (B3B3) contained much more carbohydrate
than the heterozygote clones. All strongly infested clones had low concentrations of
soluble carbohydrates and high chlorophyll concentrations, while clones with high
soluble carbohydrate levels and low chlorophyll concentrations were less severely
infested (Hertel & Kaetzel, 1999). In Pinus eliotti, Davies et al. (1999) identified a
gene that codes for chitinase, an enzyme involved in many defensive processes.
4.2 GENETIC IMPROVEMENT PROGRAMS

Genetic improvement of forest trees can be undertaken in three different ways:
classical tree breeding, hybridization and genetic engineering. Genetic engineering
and hybridization are of particular advantage because they achieve faster results than
classical breeding programs.
The new methods of genetic engineering are now available for the enhancement
of resistance in forest trees and could be very useful. In agriculture it has already
been introduced, and genetically engineered crops are becoming more and more
important in several countries while other countries are opposed to their utilization.
Transgenic forest plantations will likely have an important role to play in high
intensity tree farming systems. Because of the limited history of forest tree
domestication and the slow rate of traditional breeding programs imposed by long
generation times, forestry is likely to benefit more from biotechnology than annual
crops (IUFRO Working Party S2.04.06, 1999). An overview of the successful
genetic transformation in trees was given by Levée et al. (1997).
With the aid of Agrobacterium, genetic information can be introduced into the
plant. For the first time, this was achieved for conifers by Shin et al. (1994), who
inserted genes coding for herbicide resistance (aro-A-gene) and for insect resistance
(Bt-toxin-gene) into larch (Larix decidua). The gene that codes for the toxin of
Bacillus thuringensis has also already been introduced into poplars: Populus nigra
in China to reduce damage from L. dispar attacks and Populus alba experimentally
in France against attacks by Melasoma populi (Wang et. al. 1996, Ewald 1997).
Also, the first introduction of that gene into the larch hybrids decidua X kaempferi
was recently achieved (Ewald et al., 1999).
However, using this technique in the field creates a permanent selection pressure
for resistance to Bt, leading to rapid selection for resistant insect populations.
According to Ewald (1997), this can be avoided by always planting genetically un-
manipulated trees mixed with transgenic trees. Even more than one resistance gene
should be offered to avoid the development of Bt-resistance in the insect
populations. Problems also can arise regarding the low specificy of Bt. Indeed, the
toxin acts on different kinds of insects, but lepidopteran species are especially
susceptible, without any particular specificity. The presence of the toxin in the
environment of insects all year round is thus critical from the view point of
biodiversity. Populations of rare and endangered insect species can be further
reduced or become extinct, since there is no way for them to avoid being in contact
with the toxin. To reduce the effects on non target species, Ewald (1997) proposes
to include promotors that turn on Bt-toxin only after attack, but such a promotor still
needs to be found. Another critical point is the uncontrolled spread of transgenic
material; Ewald (1997) argued that additional genes must be introduced into the
plants leading to male sterility. But the author also states that, up to now, a stable
genetic expression of that gene has not been achieved.
5. ENHANCEMENT OF RESISTANCE BY SILVICULTURAL MEANS

Silvicultural enhancement of resistance is increasing the defence efficiency of any
given tree genotype to the maximum level of resistance of that individual tree. This
could be done by providing optimal environmental conditions for each tree species,
because in most cases a tree that suffers from environmental stress has a lower level
of resistance. Plants under stress can be a better food resource than unstressed
plants (Plant Quality Hypothesis). According to Björkman & Larsson (1999) they
have a higher nutritional value due to a higher content of soluble nitrogen and/or
reduced resistance, because they produce less defence chemicals. According to
Christiansen et al. (1987), every factor influencing crown size or photosynthetic
activity in a negative way can reduce the level of defence chemicals and therefore
increase susceptibility of a tree. This is in agreement with the Growth-
Differentiation-Balance-Theory (GDB); The production of defence chemicals is
described as a trade off with growth (Herms & Mattson, 1992). Nutrient availability
also influences defence levels, which is described in the Carbon-Nutrient-Balance-
Theory (CNB); growth is the primary sink for assimilates during conditions
favorable for growth, characterized by high nutrient availability (Tuomi et al., 1988).
When conditions limit growth, differentiation and therefore the production of
defence chemicals becomes the primary sink.
The level of environmental stress can also influence resistance. A reduction in
the stress levels on trees can create a pseudo-resistance against the insect pest
(Bogenschütz & König, 1976), but the effects of moderate and severe stress may be
different (Plant-Quality-Hypothesis). In all situations however, one must keep in
mind that, if a silvicultural practice reduces damage, it is often difficult to determine
if that is due to an increase in tree resistance or to an effect on the pest population
itself or their natural enemies.
There are several silvicultural practices that can influence tree resistance to
insects: 1. stand compositions that fit the environment (natural vegetation); 2. plant
trees only on sites that fit their ecological demands (moisture and soil conditions); 3.
fertilization; 4. irrigation; 5. avoiding monocultures; 6. avoiding clean forestry; and
7. thinning (reduction of intra-specific competition). We explain these possibilities
in the following sections, using GDB- and CND- Theory where appropriate, and
using examples from research on European insects.
5.1 STAND COMPOSITION ACCORDING TO NATURAL VEGETATION

Most stands that are severely attacked by forest pests in Central Europe are not
growing within their natural distribution range, such as Norway spruce, which does
not belong to the natural vegetation of Central Europe, except at higher altitudes as
in the Bavarian forest or in the Alps. This situation enhances susceptibility to certain
pests in different ways. For example, the climatic effects can act directly on the tree,
such as the greater danger of drought in the lowlands, but climate can also have
indirect effects by speeding up the development of the pests when the tree is
growing under warmer than normal conditions (Merker & Müller, 1951; Merker,
1956; Kalandra, 1962; Vité et al., 1984). Severe bark beetle outbreaks in Central
Europe very likely result from human actions leading to the production of two beetle
generations per year (Schimitschek, 1953, 1954).
In Western and Central Europe the cultivation of tree species belonging to
potential natural vegetation is gaining more and more attention space in silviculture.
In this context natural propagation of the trees is of advantage compared with
planting, because natural genetic diversity is preserved.
5.2 OPTIMIZATION OF SOIL PARAMETERS

Soil conditions, especially soil water potential and nutrient content which depends
on soil acidity (pH), play a major role in determining the distribution of tree species
and genotypes in natural forest ecosystems (Ellenberg, 1996), and also the level of
tree resistance. Viiri et al. (1999) state that unfavorable sites and climate conditions
often reduce assimilation rates of plants and therefore can reduce their ability to
defend themselves. This is also described by Führer (1975) as the resistance of a
individual tree is not static but fluctuates, which is also true for resistant genotypes.
Causes of such fluctuations are weather effects in combination with soil parameters.
Therefore, resistance can also be enhanced by choosing the tree species and
ecotypes that fit best with the site conditions (Schimitschek, 1969). In forestry
however, this is only possible in a restricted way because the plant-insect-site
relationships are still poorly understood.
5.3 FERTILIZATION
Bogenschütz & König (1976) give an overview of the effects that fertilization can
have on different insect groups. According to several authors, fertilization of forest
stands can increase resistance to disturbances in stands growing in unsuitable site
conditions (Schwenke, 1960; Büttner, 1961; Merker, 1962). However, as practical
experiences and causal analytic studies have shown (Luterek, 1969; Otto, 1970,
1971), the effect of this method is still very unsure. Only the exact evaluation of all
processes involved can clarify the outcome of forest fertilization (Bombosch, 1972;
Eidmann, 1963; Schimitschek, 1969; Thalenhorst, 1972).
Contradictionary results could depend on different site conditions in the
experiments and could be explained by the CNB-Theory. If site quality is already
good, which means high nutrient availability, additional fertilization leads to higher
growth activity and therefore the carbohydrate pool is depleted, and as a
consequence resistance level sinks. On poor stands the additional amount of
nutrients might not be enough to provide optimal conditions for growth, and
therefore carbohydrate flow into growth is low and they stay available for defense.
Hättenschwiler & Schaffelner (1999) reported increased performance of
Lymantria monacha on Picea abies fertilized with N. In the fertilizer treatment, the
concentration of starch, condensed tannins and total phenolics decreased, whereas
sugar and N-concentrations increased, in agreement with both Plant-Quality-
Hypothesis and CNB-Theory. Fertilization can also increase damage by sap sucking
insect species, especially aphids. Viiri et al. (1999) investigated the influence of N-
fertilization on resin flow and phenolics in P. abies and P. sylvestris. In Picea abies
fertilization treatments increased tree growth, stem diameter and tree vigor index.
This growth response was not reflected in resin flow and phloem phenolic content;
in individual trees a combination of high tree vigor index and high phenolics / resin
content was never found. This may be due to morphological barriers and / or
resource based trade offs in accordance with the CNB-Theory. Nitrogen fertilization
can increase the resin acid concentration in the needles formed one year after the
fertilization treatment but not in the needles formed before treatment (Björkman et
al., 1998), suggesting that the effects on defoliators may be complex. Kytö et. al.
(1998, 1999) and Viiri et al. (1999) investigated the influence of nitrogen-
fertilization on the constitutive induced defence mechanisms of P. abies and P.
sylvestris against attacks by bark beetles and their associated fungi. The fertilization
treatment increased tree growth, stem diameter and tree vigor index. No effect was
observed on resin flow and density of vertical resin ducts, parameters representative
of constitutive resistance, and on phloem phenolic content in the reaction induced by
fungus inoculations. The hypothesis that nitrogen fertilization reduces resistance
could not be proved. Later however, on Norway spruce, it was found that nitrogen-
fertilization significantly reduced the concentrations of total stilbene aglycon and
total terpenes in the phloem reaction zone induced by artificial inoculations with
Ophiostoma polonicum, suggesting the tree’s ability to defend itself against
aggressions was also reduced (Viiri et al., 2001).
The entomological aspect of fertilization represents a step towards stabilization
of food quality for the insects. This together with natural enemies could lead to
stabilization of pest population levels (Bogenschütz & König, 1976).
Enhanced resistance via fertilization is currently being tried by fertilizing
susceptible spruce stands, but this must be undertaken with care because influences
on the soil fauna are not yet sufficiently investigated. In this context, Funke (1990)
showed, that after the use of calcium fertilizer in areas of Germany where soils
depleted due to acid rain, drastical changes in soil fauna occurred. Therefore the
effects of fertilization, not only on the resistance of forest trees but on the whole
ecosystem, must be investigated carefully before it is applied over a large range.
Also vast areas of landscape, that had so far been unfertilized will disappear and the
whole area will sooner or later be covered only with eutrophic ecosystems. This will
increase pressure on many plant species requiring oligo- and mesotrophic
conditions, and thus species extinction will be enhanced.
5.4 IRRIGATION
Christiansen et al. (1987) state that water stress increases host tree susceptibility by
affecting the exudation of resin so that bark beetle colonization is easier. The
content and production of monoterpenes can be influenced by water stress; the
stronger the water stress, the more monoterpenes are released (Mattson & Haak,
1987). Bark beetles may take advantage of this, because they are able to identify
susceptible trees by a high level of monoterpenes in the odor plume around them
(Baier et al. 1999). In accordance to the GDB-Theory, Lorio & Hodges (1968) and
Christiansen et al. (1987) point out that moderate water stress (short term drought)
does not stop photosynthesis completely and therefore carbohydrate reserves would
be even larger, because shoot growth requires less carbohydrates during drought.
The tree can therefore become even more resistant under moderate drought
(Christiansen & Glosli, 1996). On the other hand, long term extended drought would
stop photosynthesis completely and the carbohydrates would thus be depleted,
leading lowered production of defense chemicals. This could be an explanation for
the severe bark beetle outbreaks that are often observed after long drought periods.
Moderate stress can be defined as a situation where the relative extractable water in
the soil is not less than 40% of the water reserves (Granier et al., 1999). Under these
conditions, in the temperate zones of Western and Northern Europe, only moderate
stress occurs in nature. In Central Europe, an acute drought can occur, mostly
restricted to late summer and fall. This does not cause problems in Northern
countries, but in Central and Western Europe this is just the time when the first
beetle generation starts colonization of new trees, therefore allowing the insects to
take advantage of the drought. Furthermore, drought is expected to have a stress
effect of decreasing magnitude upon sucking, mining, chewing and gall forming
insect species (Larsson, 1989). However, results on Picea abies do not fit
completely with the plant stress insect performance hypothesis (Björkman &
Larsson, 1999). Mining insects (Epinotia tedella) were more sensitive than expected
to changes induced by drought stress in their host plant, and the response of galling
insects (Sacchiphantes abietis) needs to be divided into at least two different
aspects: gall occurrence and size. Drought had a positive effect on gall initiation but
a negative effect on gall growth. Nevertheless, drought had no effect on the
chewing sawfly (Gilpinia hercynae) where as larger numbers of sucking aphids with
wing buds were observed on drought stressed trees; which is in accordance with the
original hypothesis.
For practical use irrigation is not a very suitable way to manipulate tree
resistance. There are high technical demands in the construction and operation of
irrigation systems and limited availability of water or competition for water use with
agriculture.
5.5 AVOIDING MONOCULTURES AND CLEAN FORESTRY

Clean forestry, where any dead wood is removed from the stands, decreases the
possibilities for natural enemies to survive because their prey or hosts are kept at
very low population levels. Together with monoculture, this situation can enhance
the chance of mass outbreaks of the pest species after windfall or severe drought.
In monospecific forests, bark beetles at low endemic population levels before
windfall can breed in low densities in the highly susceptible damaged trees which
increases their performance. Their populations can then easily reach the epidemic
stage during which healthy trees can be killed by mass attacks (Thalenhorst, 1958).
Nevertheless, there are also several cases where monocultures do not increase
damage and other cases of important damage in mixed forests. The problem is not
clear and further research in this field is required. In many European forests, there
are always some very weakened or recently felled trees that stay in the forest. In
contrast, in Southern China absolutely no wood stays in the forest because it is
immediately collected by local people for firewood. This lack of trees without
resistance may be the reason why Tomicus piniperda massively attacks shoots in
Southern China at the end of the winter (100% of the shoots can be killed). This
massive shoot attack induces such a dramatic reduction in tree resistance that the
trunk attacks succeed and trees are then killed by the beetles (Ye & Lieutier, 1997).
In Europe T. piniperda rarely kills trees, possibly because it always find some
suitable breeding material on the ground.
5.6 THINNING
Thinning reduces intraspecific competition between trees and therefore can also be
used to reduce the stress level of a plant and increase access to water, nutrients and
light. This allows higher photosynthetic rates and more carbohydrates are thus
available for growth and defense. Indeed, several authors found a relationship
between bark beetle attack level and indicators of severe competition, such as
reduction in radial growth (Hard, 1985) or crown competition (McCambridge &
Stevens, 1982; Worell, 1983a,b). For defoliators, a beneficial effect of thinning was
also reported, as found by Habermann & Bester (1997) for L. monacha on Pinus
sylvestris. But thinning can enhance bark beetle attacks because of root damage,
resulting from an increase in air turbulence in the stand (Christiansen et al., 1987).
5.7 OTHER PARAMETERS

Complications in the use of silvicultural practice arise because a combination of
various factors can interfere. Lunderstädt (1999) found that infestation of F.
sylvatica stands by Cryptococcus fagisuga is promoted by combinations of the
following factors: accelerated flushing in cool, unthinned valley sites and reduced
flushing on warm, thinned plateau sites. In the case of both extremes the resistance
was lower.
It must also be mentioned that, in certain areas of Central Europe, air pollution
with also plays a role in insect damage, reducing tree resistance and leading to
severe outbreaks especially of bark beetles (Scherzinger, 1996). The effects of
can also be explained by GDB- and CNB-Theories. Thus, air cleaning measures also
are a potential tool to enhance resistance of forest stands. Man-made accumulation
of in the atmosphere could have an influence on plant resistance. Such effects
have been reported by Hättenschwiller & Schaffelner (1999) on the performance of
L. monacha larvae on P. abies. In assays under high concentration, larvae reached
35% less biomass compared to the experiment under ambient concentrations.
In high treatments, specific leaf area and N content were decreasing but
concentrations of starch, condensed tannins and total phenolics increased.
6. PROSPECTS AND CONCLUSIONS

Increased resistance of forests to insect pests could be achieved by several means,
but the details of how this can be accomplished are not completely understood.
Many investigations about differences in susceptibility of clones and provenances of
forest trees to insect attacks have been undertaken up to now, but the mechanisms of
inheritance are still poorly understood (Lévieux, 1986), mainly because of the
influence of the environment which can lead to pseudo-resistance. To clarify this
point, it is necessary to segregate genetic from pseudo-resistance in controlled

laboratory experiments. In this context Bastien (1999) pointed out that it is
important to know how a variable environment can change resistance performance
of the genotype, since this genotype-environment interaction might limit tree
resistance in time and space. Therefore especially variable climatic conditions, such
as extreme drought must be evaluated experimentally as well.
Because of the intense pressure from numerous pests, maintaining genetic
variability in forest tree populations is a necessity. In addition, a sufficient level of
genetic variability is considered as a prerequisite for long-term stabilization of host-
parasite interactions because of pre-adaptations and redundancy in ecosystems
(Hertel & Kaetzel, 1999).
Parallel to the study of host variability in resistance, it is also important to take a
close look at the genetic diversity of the pest insects and the pathogens vectored by
them, especially to take into account the adaptive capacity of the pests to host
resistance. In Europe, that has already been done for T. viridiana (Du Merle, 1988)
and presently this topic is an important aspect of forest entomology research. It
concerns a wide array of pest guilds, such as sap sucking, defoliating, cone and seed
insects, and bark beetles and their associated pathogenic fungi.
The reactions of natural enemies to improve of tree resistance are also an
important aspect that must be investigated carefully. Indeed, when the plant
resistance level against the pest is increased by any method, population density of
the pest is lowered, and this may cause problems for the complex of natural enemies
controlling the pest. Increased resistance might cause a food shortage for the third
trophic level and therefore their regulative capacity could be lowered (Führer, 1975).
This concern is even more relevant in intensely managed monocultures where the
population densities of prey or hosts are very low during the endemic stage of the
population dynamics and therefore populations of natural enemies are already
limited in their ability to increase. Raising resistance of such stands will even more
diminish the regulatory effects of the antagonistic complex. Therefore it is crucial
that a critical level of the prey population density is maintained. In most cases it is
not yet known, how high the critical prey or host population must be to sustain
population of natural enemies. It has thus been proposed to avoid the use of
resistance enhancing measures in areas with low bark beetle population densities
(Führer, 1975). Moreover, as pointed out by Führer (1975), all forest practices at the
moment try to reduce food quality for the pest insects to raise their mortality. Due
to this, the risk of gradation increases because many pests such as Bupalus piniarius
are mainly controlled by natural enemies, which are reduced in density due to food
shortage when their prey populations are reduced below a critical threshold. Instead
of cultivating resistant genotypes, it seems more advantageous to stabilize food
quality, and therefore also the stage of susceptibility in combination with
augmentation of natural antagonists. It is thought that the antagonists can influence
pest populations more, if plant attributes which are important for pest population
development only show low oscillations under extreme environmental conditions.
Paine et al. (1993) also state that high tree vigor and growth can be reached by
combining augmentation of beneficial arthropods with optimization of site

conditions.
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CHAPTER 12
DEPLOYMENT OF TREE RESISTANCE TO PESTS

IN ASIA
NAOTO KAMATA
Kanazawa University, Kakuma, Kanazawa, Ishikawa 920-1192, JAPAN
1. INTRODUCTION
1.1 TREE BREEDING IN CHINA

In China, the total land area is with of forested
area. The percentage of forest coverage is ca. 13% of the total land area. After 1950,
ca. 4.5 million ha of land was planted every year. In 1987, the total area of artificial
forests was 28 million ha. The main purpose of tree breeding from the 1950s to the
early 1980s has been to breed fast-growing trees to re-establish vegetation on
degraded land (Gu 1987). The influence of Lysenkoism (the belief that plants could
acquire genetically improved traits by growing them in new environments) slowed
the progress of tree breeding by the 1960s. At the early stage, selection had been the
main method of tree breeding. During later periods, breeding by crossing and
hybridization of poplars were the major projects. Thereafter, hybridization of pines
(Pinus spp.), willows (Salix spp.), and larches (Larix spp.) also started. The major
governing ideas of the tree breeding were heterosis, genetic additivity, and genetic
complementation. Because fast-growing trees tend to be infested by pests, many
plantations of poplars and willows are susceptible to attack by insects. Pest of fast-
growing plantations include: longhorn beetles, Apriona japonica, Batocera
lineolata, and B. horsfieldi, and folivorous insects, Lymantria dispar and
Apocheimia cinerarius. Projects to breed insect-resistant tress have been going on
since the 1980s (e.g. Zhu and Zhang 1991; Wang 1995). One of the major projects
265
266 N. KAMATA
has been the development of transgenic poplars transformed with the Bacillus
thuringiensis toxin gene. A major project is the selection and breeding of super
poplar clones for fibre production that are resistant to wood-boring insects.
1.2 TREE BREEDING IN SOUTH KOREA

In South Korea, a forest rehabilitation program started after the Korean War. The
major trees planted for rehabilitation have been pines and poplars (Shim 1987).
Breeding of popular started in 1953. In 1954, more than 300 strains of Italian
cultivars of poplar were introduced. Amongst these, the cultivars, I-214, I-476, and
V-211, were selected as cultivars suitable for the climate in Korea and were planted
in areas totalling ca. 670,000 ha. The hybrid, P. alba X P. grandulosa was thought
to have the best of both parents and has been planted in an area totalling ca. 180,000
ha since 1967. The F1 progeny grew fast but were highly susceptible to the salty air
from the sea. In the late 1950s and early 1960s, a great amount of Pinus taeda pollen
was introduced from the USA to breed the hybrid Pinus rigida X P. taeda (P. rigi-
taeda). Because P. rigi-taeda grew 2.5 times faster than P. rigida when it was
young, ca. 1,000 ha of plantations were established. However, this hybrid was not
tolerant to strong cold wind in winter and the growth rate slowed down as it
matured. Many native pine trees have also been planted but have been damaged
badly by the pine needle gall midge, Thecodiplosis japonicus. The Korean Forest
Research Institute first tried to select a resistant strain but changed the strategy to
breed hybrids by crossing between susceptible and resistant species (Son et al.
1999). Effective hybrids of insect-resistant pines were obtained using this technique.
Pine wilt disease caused by the pinewood nematode (PWN), Bursaphelenchus
xylophilus, is also a serious problem in the southern part of South Korea (La et al.
1999). An experiment to test the cold tolerance of the hybrid, P. thunbergii X P.
massoniana, is in progress (Shim 1987).
1.3 PEST-RESISTANT TREE BREEDING IN JAPAN

In Japan, breeding larch trees resistant to the vole, Clethrionomys rufocanus, has
been successful. As for pines, selection for P. thunbergii clones that are resistant to
T. japonensis is the most successful and advanced among many projects in Japan.
DNA markers available for marker-assisted selection (MAS) of resistant trees have
been identified. The pine wilt disease caused by pinewood nematode has been the
most serious pest for the past 30 years. A national project to select pine trees that
were resistant to PWN started in 1978, which was successful for P. densiflora and P.
thunbergii. The hybridization of P. thunbergii X P. massoniana also started in 1983.
These resistant pines have started to be used in plantations. As for the Japanese
cedar, Cryptomeria japonica, selections for clones resistant to each of several bark-
and wood-boring insects have been carried out (Tajima 1990, Tamura et al. 1996,
Ueki 1999).
DEPLOYMENT OF TREE RESISTANCE TO PESTS IN ASIA 267
2. POPLAR
2.1 BREEDING OF POPLARS IN CHINA
Poplars are distributed almost throughout China. They include 59 species, 35
varieties, and 11 cultivars. In China, hybridization of poplars has been conducted
since the 1960s. Some of the major parent tree species were P. simonii, P. nigra, P.
cathayana, P. alba, and P. pyramidalis. Hundreds of hybrids were tested each year.
Table 1 shows the major popular cultivars that were developed in the 1960s and that
have been planted in the country. The major goals of the poplar breeding program
were to develop cold-tolerant, fast-growing trees for the northern regions and to
develop fast-growing trees in the regions around the Chang Jiang River, in central
China.
268 N. KAMATA
2.2 TRANSGENIC POPLAR PLANTS TRANSFORMED WITH THE BT TOXIN

GENE IN CHINA
In China, transgenic poplars, Populus nigra and P. deltoides, transformed with the
Bt toxin gene have been developed to protect them from insect defoliation (Chen et
al. 1995a; Tian et al. 1995).
An effective regeneration system for P. deltoides was first developed by Chen et
al. (1995a). Agrobacterium tumefaciens LBA 4404 strains harbouring the Bt toxin
gene expression vector pB48.214 or pB48.215 were used for transforming poplar
plants by means of the leaf disc method. After transformation, adventitious buds
formed at the cut explant on media with kanamycin nearly one month later. When
shoots reached 1cm long, they were transferred to rooting media and supplemented
with kanamycin.
PCR analysis showed that Bt toxin genes were successfully integrated into the P.
deltoides chromosomes. A similar regeneration system was developed for P. nigra
(Tian et al. 1995). Transformation of P. nigra was obtained by co-cultivating leaves
and stem segments with A. tumefaciens LBA 4404 carrying the binary vector
containing the toxin chimeric gene. Candidates of transgenic plants were
selected from regenerated Kanamycin-resistant plants by DNA-DNA hybridization.
Insect tolerance tests proved that the transgenic plants were toxic to two defoliating
insects, Lymantria dispar (Lepidoptera: Lymantriidae) and Apochima cinerarius
(Lepidoptera: Geometridae). Transgenic plants were selected based on the Southern
blot of the PCR products and a cluster analysis using the trees’ growth and insect
resistance (Tian et al. 1995). The western blot analysis showed that the Bt toxin
gene was not only inserted into the chromosomes of poplar but also was expressed
into protein, which explains the high insect resistance of these plants (Cheng et al.
1995b).
2.3. SUPER POPLAR CLONES RESISTANT TO WOOD-BORING LONGHORN

BEETLES
The cultivars I-63, I-69, and I-72 were introduced to China in 1972 from Europe and
have been planted in Hua Dong (East of China) and Hua Zhong (Centre of China)
(Table 1). However, these were sometimes heavily infested with longhorn beetles
and many trees died. In Hubei Province, Cao et al. (2000) investigated insect
damage by A. japonica and B. lineolata to these three major introduced poplar
cultivars planted in three disjunct locations. The authors found a significant effect of
location on the insect damage. However, no consistent relationship was found
between the amount of damage and the tree cultivar. The selection and breeding of
super poplar clones as fibre products that are resistant to a wood-boring longhorn
beetle, Batocera horsfieldi, has been conducted in China since 1983 (Qing 1991).
Artificially controlled pollination was conducted in 1983 using I-69 as the female
parent plant, and using P. nigra, I-63 and P. x euramericana (Dode) Guineir. cv.
“Seroutina 272” as the male parent plants. Cross combinations were numbered No.
32 for I-69 X P. nigra, No .34 for I-69 X I-63, and No. 37 for I-69 X P. x
euramericana. A field test to compare the hybrid clones was carried out in Mian
County, Shangxi Province, after selection in the nursery (Wang et al. 1995). At first,
23 clones including two control clones were tested. These 23 clones were divided
into three groups by using a systematic cluster analysis. The first group (G1)
included trees that were fast-growing and that had a high resistance to B. horsfieldi.
This group included the clones 34-37, 34-135 and 34-314. The second group (G2)
included clones that grew fast but that were less resistant to B. horsfieldi. This group
included I-69 and 12 hybrid clones including 34-301. The third group (G3) included
trees that grew slowly and that were less resistant to B. horsfieldi. This group
included all the clones originating from combinations of No.32 and No.37, and P. x
euramericana (control). The resistance of G1 was significantly higher than the
resistances of G2 and G3. Based on their high resistance (100%), clones 34-37 and
34-135 were combined to form a subgroup named Nan-Kang No.l. Clone 34-314,
which was slightly damaged by B. horsfieldi, was named Nan-Kang No.2. Second,
two poplar clones (34-301 and 34-286), which grow fast, are resistant to insects, and
have good quality, were selected. Nine years after planting, Clones 34-301 and 34-
286 were 24.9% and 16.6% higher than that of I-69, respectively, and 16.7% and
8.9% higher than that of 34-314 (Nan-Kang No.2), respectively. Clones 34-301 and
34-286 were significantly more resistant to B. horsfieldi than I-69: the number of B.
horsfieldi per tree was 0.4 for 34-301, 0.5 for 34-286 and 5.38 for I-69. There was a
positive correlation between the resistance to B. horsfieldi and the total phenolic
contents. By a random amplified polymorphic DNA (RAPD) analysis, a molecular
marker (OPAD-01) was found, which is linked to genes of resistance to B. horsfieldi
and is useful for MAS of resistant trees (Wang et al. 1995).
3. PINE
3.1 PINE NEEDLE GALL MIDGE, THECODIPLOSIS JAPONENSIS
The pine needle gall midge, T. japonensis, was first found in central Japan (Sasaki
1901). This insect forms a gall on the basal part of the needles. Heavily infested pine
trees are weakened and sometimes die. Population outbreaks of this insect were
recorded in 1929 in Korea (Takagi 1929). In Korea, more than 300,000 ha of pine
plantations are heavily damaged by this insect every year (Office of Forestry Korea
1981). In Japan, the first outbreak record was reported around 1950 from Nagasaki
Prefecture in Kyushu, the southernmost main island of Japan (Takizawa 1964). The
outbreak area spread from the southwest to northeast (Sone 1986). In 1976,
outbreaks were recorded in Hokkaido, the northernmost main island.
An outline of the life history of T. japonensis in central Japan is as follows (Sone
1986). This species is univoltine. Adults emerge from the end of May to late June
with a peak in mid-June. The life span of adults is about one day. Females copulate
soon after emergence and deposit egg batches on the surface of the cavity between a
pair of developing needles in a fascicle. The incubation period is about one week
and newly hatched larvae move to the base of the needles where they form galls.
The larvae moult two times in the galls, and matured third instars drop from galls to
the ground during the period from November to March in the following year. The
dropped larvae crawl into the litter layer and the surface of the soil, where most of
270 N. KAMATA
them spin cocoons and over winter. Pupation takes place from April and adults start
to emerge from the end of May.
There is great variation in pine tree resistance to T. japonensis among species
(Furuno and Sone 1978; Furuno 1987; Sone 1987) and also among individuals
within the same species (Nishizawa 1969; Ozawa l971; Saito 1978). There are great
variations in the number of deposited eggs among tree species and among individual
trees of the same species. However, the number of eggs deposited did not have any
significant relationship with tree resistance to T. japonensis (Terada 1992). Both
among-species and within-species variation in the resistance are related to the
mortality of hatched larvae after entering the needles. The salicylic acid
concentration in the needles was closely related to the insect mortality (Son et al.
1999). Pine species highly resistant to T. japonensis contained higher concentrations
of salicylic acid. For example, the salicylic acid concentration in needles of P.
virginiana and P. rigida was 37 ppm to 50 ppm. However, as for P. thunbergii and
P. densiflora the concentration was below 10 ppm. Salicylate-mediated signal
transduction plays an important role in disease resistance (Klessig and Malamy
1994). A high concentration of salicylic acid induces expression of a stilbene
synthase (STS) gene in pines (Kubota et al. 1996; Yamauchi et al. 1997). When
salicylic acid was applied externally, the contents of internal salicylic acid in the
needles of susceptible pines increased from 9.5 ppm to 20.6 ppm after direct
external irrigation of salicylic acid solution and flour treatment on the roots. As a
result, the frequency of gall formation decreased to a level that was 17-19 times
lower than that of the control.
In Korea, hybridisation has been the major strategy to breed resistant pines
against T. japonensis. In Japan, a project to breed pine trees that are resistant to T.
japonensis started in 1971 (Terada 1992). This project is considered as one of the
most successful among many projects to breed trees that are resistant to pests in
Japan. In order to develop P. thunbergii that are resistant to this insect, 60 candidate
trees, which were growing without signs of damage in severely damaged maritime
forests of P. thunbergii, were selected. Thirty-six of the selected trees were found to
be free from the parasitism of T. japonensis following inspections. In further testing
9 of the 36 trees were attacked by T. japonensis at the same rate as damaged trees. A
clonal test of the selected trees was carried out by planting grafted ramets as a block
in the severely damaged forest and then leaving the planted materials under natural
conditions. Thirty-eight clones out of the 53 tested had either zero or a very low
percentage of parasitism. From the results of the inspection of the selected trees and
their clonal test, 42 trees were judged to be resistant to the gall midge. In progenies
produced from artificial pollination, the seedlings were segregated into ones with
non-parasitism (0%: resistant) and ones with high-parasitism (81-100%). Seedlings
with a parasitism percentage of 1-80% appeared very rarely. The average
frequencies of appearance of resistant seedlings were 73% in the progenies of
Resistant X Resistant, 48% in Resistant X Non-resistant and 0% in Non-resistant X
Non-resistant, respectively. From the above segregation ratio, the resistance of the
P. thunbergii to T. japonensis appears to be governed by one dominant gene and the
parent trees used for pollination were heterozygous. Three RAPD markers linked to
the resistance gene (RPGM) were detected by a bulked-segregate analysis (Kondo et

al. 2000). Of these three markers, was also located in the confirmed
map position in the map made by AFLP, and and were
regarded as accessory markers at its most likely position (Hayashi et al. 2001).
These markers might be useful for MAS of resistant trees.
Hopefully, the function of the resistance gene (RPGM) will be investigated and
the relationship between the function of this resistance gene (RPGM) and the
salicylic acid concentration in the needles will be examined in future studies. The
proximate factors causing the mortality of hatched larvae after entering the needles
should also be studied.
3.2 PINE WILT DISEASE CAUSED BY PINEWOOD NEMATODE,

BURSAPHELENCHUS XYLOPHILUS
The major pine species in Japan, P. densiflora and P. thunbergii, have suffered
heavy mortality for several decades (Kobayashi 1988; Kishi 1995). In the early
1970’s, the causal disease agent was found to be the pinewood nematode (PWN), B.
xylophilus (Kiyohara and Tokushige 1971). The Japanese pine sawyer (JPS),
Monochamus alternatus (Coleoptera: Cerambycidae) is the principle insect vector in
Japan. The existence of the nematode was reported in the United States, where only
exotic pine plantings were severely damaged suggesting that the nematode was
native in the US. Recent genetic studies of the systematics of PWN found that PWN
in Japan had possibly been introduced from the USA and that PWN in Asian
countries was derived from the same strain (Iwahori et al. 1998).
A large-scale national control project was started in 1977 when a federal law
was passed complementing an insecticide spray program by either federal or local
governments. The major control tactics were aerial spraying of standing trees to kill
aerial populations of the vector insects and using the cut-and-treat method for
treating infested logs to kill the vectors before emergence. The latter method
includes cut-and-spray, cut-and-burn, and cut-and-slash methods.
The resistance of pine trees to PWN varies greatly among tree species (Futai
and Furuno 1979; Furuno 1982; Furuno and Futai 1986) (Table 2). At the species
level, there is a close relationship between susceptibility and phylogenic
classification: pine species belonging to the subsection Australes are the most
resistant, followed by the subsection Contortae. Pines belonging to the subsections
Ponderosae and Oocarpae are susceptible. The subsection Sylvestris contains both
resistant and susceptible species. The resistance also has a relationship with
geographical distribution (Furuno et al. 1993): the resistant pines (ranked HR and R
in Table 2) are distributed in only two regions, the east coastal area of North
America and the area from Taiwan- S China-southern part of Himalayan mountains.
272 N. KAMATA
--- Continued ---

Pathophysiological changes during the development of symptoms of pine wilt

disease is as follows (Fig. 1) (Fukuda 1997): The development of symptoms is
divided into two stages: the early and advanced stages. In the early stage, a small
number of nematodes migrate into the cortex, and then into the xylem of the stem,
and induce denaturation and necrosis of parenchyma cells (Ishida et al. 1993), which
result in terpene synthesis in xylem cells and embolism in tracheids. Such changes
in the early stage can be induced in both susceptible and resistant pine species by
either virulent or avirulent isolates of PWN. No change occurs in the physiological
status of leaves, and nematode reproduction is suppressed during the early stage
(Fukuda and Suzuki 1988a, b). Pine trees can survive if the symptoms do not
progress from this stage. The symptoms of the advanced stage usually occur only in
susceptible pines infected by virulent nematode isolates. At the beginning of the
advanced stage, enhanced ethylene production by stems that coincides with cambial
destruction occurs (Mamiya 1975, 1980, 1984, 1985; Mori and Inoue 1986) and
results in embolism of the outermost xylem in the portion (Fukuda 1997). The
embolism causes a decrease in leaf water potential and cessation of photosynthesis
(Fukuda and Suzuki 1988a, b). After cessation of photosynthesis, symptoms develop
drastically with a burst of the nematode population.
274 N. KAMATA
Some of the secondary metabolic compounds in pine trees relate to pine wilt
disease caused by PWN (Table 3). Resistance of pine trees to PWN must separately
be discussed at each of at least two different stages of PWN infection: resistance at
the time of PWN invasion into the bark and resistance in the wood after invasion.
PWN has some difficulty in invading the bark of a resistant pine, P. taeda, but easily
invades the bark of a susceptible pine, P. thunbergii (Futai 1985a, b) suggesting that
the resistance of pine trees at the time of PWN invasion is related to a species-level
difference in pine resistance to PWN. Unidentified water-soluble substances in pine
bark were responsible for immobilization of PWN (Bentley et al. 1985) and acted as
a repellent against PWN (Futai 1979). The quantity of the active substance from P.
taeda was greater than that from P. densiflora (Bentley et al. 1985). These water-
soluble substances were thought to act as a constitutive defence of pine trees at the
time of invasion (Futai 1987). After a successful invasion, the nematodes increased
in number and spread rapidly in the susceptible pine trees, but not in the highly
resistant trees such as P. taeda. The responses of the resistant pine species, wound
periderm formation and occlusion of cortical resin duct, trapped the nematode within
damaged tissue (Ishida et al. 1993; Yamada and Ito 1993a). Since PWN never
invaded the trunk, the tree survived although the inoculated branches died. Among
secondary metabolic compounds shown in Table 3, pinosylvin monomethylether
(PSME) showed the strongest virulence to PWN, which was followed by pinosylvin
(PS). After PWN invasion, these stilbenes, PSME, PS, and 3-0-methyl-7,8-
dihydropinosylvin (MDPS), rapidly accumulated in the wood of the basal part of
inoculated branches and the bark of the branches of P. strobes, which is ranked as
“resistant” in Table 2 (Yamada and Ito 1993b; Yamada et al. 1999). These stilbenes
act as an induced defence against PWN. However, in P. thunbergii, which is ranked
as “highly susceptible”, no PS and PSME concentrations were recognized after
inoculation of PWN (Yamada and Ito 1993b). For P. densiflora, stilbene synthesis
was not induced by the infection of PWN (Yamada and Ito 1993b) although P.
densiflora has the STS gene (Yamauchi et al. 1997). These facts indicate that PWN
infection did not induce expression of the STS gene in P. densiflora.
In Japan, a national project to select resistant pine trees started in 1978.

Survivorship of P. densiflora after PWN inoculation was 63.2% (37.9-84.6%) for
the selected clones and 47.9% for non-selected clones (Toda 1999). Pinus
thunbergii, which is an important species for protecting the seashore, is much more
susceptible to PWN than P. densiflora. Survivorship of P. thunbergii after
inoculation of PWN improved considerably from 12.5% for non-selected clones to
50.7% (29.1-67.9%) for the selected clones. Another way of breeding pines that are
resistant to PWN is hybridization. The hybridization, P. thunbergii X P.
massoniana, was first conducted in the USA in the 1930s (see Furukoshi 1986). In
Japan, crossing of various combinations of many pine species have been tested since
1972, which proved the high compatibility between P. thunbergii and P.
massoniana. An international hybridization project of P. thumbergii X P.
massoniana was started in 1983 by introducing 20 liters/year of P. massoniana
pollen from China. The same hybrid was also studied in Korea (Shim 1987). The
276 N. KAMATA
tolerances of the hybrids to cold climate, strong winds, and sandy soils have been
tested both in Korea and Japan. Trials of artificial hybridization between P.
thunbergii X P. densiflora have also been conducted (e.g. Toda et al. 1990) because
a natural hybrid between P. thunbergii and P. densiflora was found to show a
stronger resistance to PWN than P. thunbergii (Ooyama and Shiraishi 1981).
Several studies have reported that prior inoculation with an avirulent isolate of
PWN induced resistance of young pine trees in the nursery and of adult pine trees in
the forests (e.g. Kiyohara 1989). In the case of resistance-induced seedlings,
embolism in the xylem was conspicuous, but water conduction was maintained in a
very thin layer of the outermost xylem near the living cambium, and PWN did not
multiply (Fukuda et al. 1997). Induced resistance of pine is considered as one of the
possible control tactics of pine wilt disease (Kosaka 2000).
4. LARCH
4.1 LARCH IN HOKKAIDO, JAPAN
The Japanese larch, Larix leptolepsis, is the only native larch species in Japan.
Natural distribution of Japanese larch is restricted to the high elevation areas in
Central Japan. However, it has been widely planted in Europe, North America and
Asia because it grows well in cold regions. Especially in Europe, the hybrid
Dunkeld larch L. x eurolepsis (Larix decidua X L. leptolepsis) is one of the major
plantation tree species because of its fast growth, good shape, and resistance to
canker.
In Japan, it is also widely planted in central and northern Japan, especially on the
island of Hokkaido. However, L. leptolepsis tends to suffer serious damage by the
vole Clethrionomys rufocanus, and many trees died by girdling. Larix gmelini var.
japonica, which is naturally distributed in the Kuril Islands and Sakhalin, suffers
little damage by the vole but it has not been planted in Hokkaido Island much
because it grows slowly there. The hybrid L. g. var. japonica X L. leptolepsis has
been widely planted because it suffers little damage by the vole and grows faster
than L. g. var. japonica. Recent studies reported that there is a great variation in the
vole resistance both in the hybrid and L. g. var. japonica (Nagata et al. 1989). The
resistance of the hybrid was closely related to the resistance of their parents.
Compounds that are repellent to the vole were identified as 13-epimanool and larixol
(Sukeno and Ozawa 1997). Larixol showed activity at a concentration of 0.25%. The
compound 13-epimanol showed activity at a concentration of 0.5%. These
compounds will be useful tools for instant screening for vole resistance in larch
trees.
5. JAPANESE CEDAR, CRYPTOMERIA JAPONICA

5.1 HISTORY OF CRYPTOMERIA JAPONICA PLANTATION IN JAPAN
The Japanese cedar, Cryptomeria japonica, is the major commercial conifer
plantation species in Japan. The natural range of its distribution is Honshu, Shikoku,
Kyushu, and Yakushima Islands. Pure native stands of Japanese cedar still remain in
Yakushima Island and the west coastal area of the northeast part of Honshu Island.
In Japan, after WWII, natural broad-leaved forests were cut over and changed to
conifer plantations. Japanese cedar has been one of the major plantation species and
is planted from the southern part of Hokkaido Island to Kyushu Island, which is
wider than its natural distribution.
In the Japanese cedar plantation, tussock moth Calliteara argentata
(Lepidoptera: Lymantriidae) populations sometimes reach outbreak levels and cause
serious defoliation. After insect defoliation, the mortality of Japanese cedar was
reported to be 13.0-28.6% (Shibata 1981). Several wood- and bark-boring insects
that reduce timber value have been considered as more important pests than C.
argentata. These species include the bark borer Semanotus japonicus (Coleoptera:
Cerambycidae), the twig borer Anaglyptus subfasciatus (Coleoptera:
Cerambycidae), the bark midge Reeseliella odai (Diptera: Cecidomyiidae), and the
bark moth Epinotia grantialis (Lepidoptera: Tortricidae).
Improvement of Japanese cedar has been focused on to breeding trees that are
resistant to these wood- and bark-boring insects except for A. subfasciatus, damage
from this insect can be avoided completely if trees are pruned to remove dead
branches. Pine trees have constitutive resin ducts, but Japanese cedar does not.
Therefore, traumatic resin duct formation seems important to reduce damage by
these insects. However, the mechanisms of resistance to each of these insects are
different among insects and sometimes contradictory to each other. When larvae of
E. grantialis were released into the trunks of the Japanese cedar that had been
regarded to be highly resistant to S. japonicus, most of E. granitalis larvae grew to
the adult stage contrary to prediction (Kato 2000). This result suggests that the resin
flow from the inner bark, which was regarded to be most important to protect
against attacks by S. japonicus larvae, could not protect against attacks by E.
japonicus. Possible reasons for the difference in effectiveness of the resin flow are a
difference in the boring period and a difference in the boring system between the
two pests. Larvae of E. granitalis bore in early of the seasons when the host trees
cannot metabolically respond to the attack. The boring period of E. granitalis is
shorter because it ingests only a small amount of plant tissue. Because of its high
mobility, E. granitalis larvae can escape from wood if the resin flow deters the
course of boring. Because young larvae of E. granitalis start to feed on current-year
shoots, the characteristics of current-year shoots are probably more important in
determining tree resistance to E. granitalis. The thickness of inner bark is an
important factor determining resistance of Japanese cedar both to S. japonicus and
to R. odai. To make matters worse, trees with a thin inner bark are resistant to S.
japonicus but more susceptible to R. odai (see below).
278 N. KAMATA
5.2 BARK MIDGE, RESSELIELLA ODAI

In the year 2000, the bark midge, R. odai, was distributed in Kyushu Island and in
the westernmost part of Honshu Island, and is believed to be spreading eastward on
Honshu Island (Sudo et al. 2000). In these areas, the damage caused by R. odai is
serious for Japanese cedar forestry. When the larvae of this insect feed on Japanese
cedar, timber values are reduced by stains in the sapwood. A project to breed
Japanese cedar that is resistant to R. odai started in 1985. In this project, trees that
were not infested by R. odai and those on which no stains were formed, although
they were infested by this insect, were considered as “resistant” and have been
selected (Tajima 1990). The mechanism of resistance is still unclear. However,
resistance is closely related to the thickness of the inner bark. The stain is formed by
the digestive fluid secreted by the larvae feeding on the surface of the inner bark.
When the inner bark is thick enough to prevent the fluid from reaching the
cambium, no stains were formed in the xylem although flecks were formed in the
inner bark (Figure 2) (Yoshida and Sanui 1979). Therefore, Japanese cedar with
thick inner bark is considered to be “resistant” to R. odai.
5.3 BARK BORER, SEMANOTUS JAPONICUS

Semanotus japonicus (Coleoptera: Cerambycidae) is one of the most damaging pests
of Japanese cedar (Kobayashi 1985). In central Japan, the life cycle of S. japonicus
is usually completed in 1 year (Kobayashi and Shibata 1985). Mature adults emerge
in spring, mate on the surface of the trunk soon after emergence, and the females lay
their eggs in bark crevices. Newly hatched larvae enter the bark and feed in the
cambial region, primarily on the inner bark (Kobayashi 1985). The larvae usually
molt four times (Maeto 1985). Full-grown larvae enter the wood in late summer,
pupate in cells in autumn, and overwinter as adults.
Population fluctuations and outbreaks of S. japonicus in Central Japan are as

follows (Ito 1999b): Semanotus japonicus established a population in the stand 5
years after planting. It continuously increased in numbers, reached a peak abundance
6 years later, and subsequently declined rapidly. This insect damaged ca. 50% of the
initial tree population during the outbreak and ca. 35% of the infested trees were
killed. The number of adults that emerged from each tree was correlated positively
with tree diameter. Particular trees tended to consistently produce more adults
during the outbreak than other trees. Larger, faster-growing trees were more
vulnerable to mortality due to S. japonicus attack. The depletion of favourable host
trees led to the collapse of the outbreak.
This insect attacks living cedar trees with larvae mainly feeding in the inner bark
(or phloem) of the trunk. There is a great variation in S. japonicus adult body size
(Kobayashi and Shibata 1985). Enhanced nutritional conditions of the inner bark,
i.e. nitrogen concentration and water content, could affect borer development
(Shibata 1998). Primary borers are able to attack a healthy, living tree and complete
their normal development, whereas secondary borers are incapable of attacking and
completing normal development in healthy trees (Knight and Heikkenen 1980).
Shibata (1995, 2000) hypothesized that Semanotus japonicus was placed in a
transition category between primary and secondary borers, or in other words a
‘weak’ primary insect: S. japonicus may be trapped by ‘resin flow’ if they attack
vigorous living trees or die due to ‘poor nutrition’ if they attack dead trees.
Semanotus japonicus lives in a delicate balance with its host tree.
Resin exuded by infested Japanese cedars is important as a mechanisms of host
resistance to larval feeding by S. japonicus (Kobayashi 1985; Shibata 1987),
although Japanese cedar normally lacks resin-producing structures. It is known that
Japanese cedar forms traumatic axial resin ducts and produces resin in the inner bark
in response to various kinds of injuries, including feeding damage by S. japonicus
(Yamanaka 1984; Ito 1998). Only the 1- and /or 2-year-old growth layers of the
inner bark were capable of forming new resin ducts in response to injury (Kanazashi
et al. 1988; Ueki et al. 1989, Arihara and Suda 1996). This traumatic resin flow has
been considered as the most important determinant of resistance to S. japonicus (Ito
1998, 1999a). Spatial extent of inducing traumatic resin ducts is different among
individual trees and is an important determinant of tree resistance to this insect (Ito
1998). In some trees, resin duct formation was confined to the proximity of each
larval gallery. However, in other trees, induction of resin ducts was extended
throughout the whole trunk. Larval mortality was higher in trees that exhibited
systemic induction of resin ducts than in other trees that showed a localized
response. Time lags in inducing traumatic resin ducts and chemical and physical
characteristics of resin are also possible factors related to the resistance. However,
these factors have not been well studied.
Under the leadership of the Forestry Agency Japan, a project to breed Japanese
cedar that are resistant to S. japonicus started in 1985. Forest Tree Breeding Centres,
Regional Forest Offices, and ca. 80% of Prefectures in Honshu and Shikoku Islands
participated in the project. Four screening procedures have been conducted in the
project (Ueki 1999). First, individuals that suffered no injury from S. japonicus
280 N. KAMATA
were selected from heavily infested stands. From Honshu and Shikoku Islands, a
total of 1413 individual trees were selected as candidates. Second, resistance of
these trees were checked by pricking them with a pin. Formation of traumatic resin
ducts and secretion of resin were the screening criteria. Third, a primary screening
test was conducted in cages in which S. japonicus adults were released. Candidate
tree clones (four trees per clone) were divided into five categories according to the
average number of feeding signs on the sapwood in each clone. The clones in the
lowest of the five classes passed the primary screening test. Then for each of the
clones that passed the primary test, three fresh trees of each of these clones were
subjected to a secondary screening test, in which 10 hatched larvae were inoculated
on the outer bark. Only trees that were successfully inoculated were used in the
secondary test; inoculation was considered successful when at least 4 of the 10
larvae showed feeding signs on the inner bark. If a tree was not successfully
inoculated, another fresh tree of the same clone was inoculated. When no feeding
signs were found on the sapwood of any of the three successfully inoculated trees of
each clone, the clone was considered “resistant”.
However, a few “resistant clones” could completely inhibit injury by this insect
(Ueki 1999). Even on the same clone, the number of feeding signs of hatched larvae
on the inner bark and on the sapwood varied greatly by both year and location in
which the screening tests were conducted. The number of feeding signs was strongly
influenced by environmental factors. Kato (2001) reported a low relationship
between the ability of traumatic resin duct formation evaluated by a prick-with-a-pin
method and the resistance to S. japonicus. This is partially because the ability of
traumatic resin duct formation of the Japanese cedar varies greatly among individual
trees (Kobayashi and Shibata 1985; Tajima 1986; Miyaura and Yamada 1991). In
addition to traumatic resin-duct formation, the thickness of the inner bark was
shown to be an important determinant of larval attack success (Arihara and
Kawakami 1998). In trees in which traumatic resin-ducts are normally induced,
insects could grow in the following way (Figure 3): First, larvae fed on the
outermost layer of the inner bark, in which no traumatic resin ducts were formed and
no resin was secreted. Thereafter they moved to the lower portion in which the
conducting system had already been destroyed and formation of traumatic resin
ducts was not so active. In trees with thin inner bark, larvae will be killed by resin
because young larvae must feed on the innermost layer of the inner bark in which
traumatic resin ducts will be formed.
Resistance of Japanese cedar to S. japonicus is determined primarily by the
formation of traumatic resin ducts but secondarily by the thickness of the inner bark.
Its mechanism seems highly complicated and is likely to be a polygenetic trait (Ueki
1999).
EPILOGUE
In this paper, development of tree resistance to pests in Asia was reviewed. The
information was mainly available from China, South Korea, and Japan in East Asia
and amongst these three countries, most of the information was from Japan.
Techniques of tree breeding have progressed greatly with the progress in molecular
genetics. However, among all the tree breeding projects in Asia, there is still not one
in which resistance mechanisms, substances related to it, and related genes are fully
understood. For example, MAS using DNA markers is now available for breeding P.
thunbergii that are resistant to the pine needle gall midge, although the mechanism
of the resistance is still unclear. Breeding trees that are resistant to pests should be
carried on by elucidating the resistance mechanisms, development of selection
assisted by chemical substances, and development of a MAS method by elucidating
related genes.
ACKNOWLEDGEMENTS
I express my sincere thanks to Drs. Eui-Rae NOH (Former Director, KFRI, South Korea), MENG
Yangqing and HAN Yifan (CAF, China), Kazutaka KATO and Eiji HAYASHI (FTBC, Japan), Takashi
DAIDO and Yoshiaki NAGATA (Oji Tree Breeding Research Centre, Japan), Kazuyoshi FUTAI (Kyoto
University), and Kenji FUKUDA (The University of Tokyo) for providing useful information. I also
thank to Eiichi SHIBATA, K. FUTAI, Kensuke ITO, K. KATO, and E. HAYASHI for reviewing the
earlier draft of this article. I am grateful to Prof. Dr. Michael R. WAGNER for his helpful comments.
Yiqun LIN helped with the manuscript. I also thank her.
282 N. KAMATA
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CHAPTER 13
USING RESISTANCE IN TROPICAL FOREST

PLANTATIONS
J. DOLAND NICHOLS1, MICHAEL R. WAGNER2,

JOSEPH R. COBBINAH3
1. School of Environmental Science and Management, Southern Cross University,

Lismore, NSW, Australia 2480
2. Northern Arizona University, Box 15018, Flagstaff, AZ, USA
3. Forestry Research Institute of Ghana, University Box 63, Kumasi, Ghana
1. PLANTATIONS IN THE TROPICS

Technically speaking the tropics are centered around the equator, extending from 23
½ ° N to 23 ½ ° S latitude. But nearly “tropical” conditions – particularly the lack
of frost – may extend well to the north and south of these lines. Plantations,
especially those in the tropics, can be highly productive, if species and provenances
are properly chosen, yielding up to 40 cubic metres of wood per hectare per year or
more, in the case of Eucalypts in Brazil. This compares with a growth rate of usable
timber in natural forests that varies from Providing these figures are
correct and assuming a conservative average production of , Sedjo and
Botkin (1997) estimate that an area in plantations of only 0.15 billion hectares, or
4% of the global forested area, could produce most of the of industrial
wood consumed annually in the world. Although there is high rainfall throughout
the tropics, especially near the equator, species and provenances need to be carefully
matched to sites to achieve consistently high growth rates. Also, since insect
population increases are not limited by frosts in most of the tropics and because
monocultural stands of young rapidly growing trees may be an ideal food source for
herbivorous insects, care needs to be taken with respect to pests. This of course
should include the use of tree stock that is partially or completely resistant to major
287
288 D. NICHOLS et al.
insect pests, as well as having high growth potential, good form, and other desired
characteristics.
1.1 EXTENT
Estimating the exact number of hectares of plantations in the tropics is difficult,
given that much of the data is reported on a per-country basis, rather than by
ecological or climatic zone. Brazil for example includes some areas of subtropical
plantations as well as those that are truly in the tropics. Also, within the tropics there
are temperate-like conditions at higher elevations, where considerable tree planting
has been taken place, as in Mexico, Central America, Colombia, Peru, Ecuador,
Kenya. Also, “plantation” is not clearly defined, extending from enrichment
planting in native forest through standard monocultural tree plantations to various
types of agroforestry systems. Some surveys include rubber (Hevea) and coconut
(Cocos) as well as standard timber or pulp producing species. Nevertheless,
estimates of the total area in the tropics under plantations range from 30 million in
1990 (FAO, 1997) to as great as 42 million ha (Evans, 1992), while the latter source
includes areas in warmer parts of the subtropics. The FAO (2001) estimated 51
million ha, when counting all of India as well as Brazil as “tropical”.
In 1990 Eucalyptus spp. accounted for 23% of the total area planted in the
tropics, followed by Pinus spp. (10.5%), Acacia spp. (7.7%) and Tectona grandis
(5%) (FAO, 1997). Estimates of these proportions had shifted somewhat by the year
2001, with Eucalyptus at 26.2%, Pinus at 10.9%, Acacia at 14.9%, and Tectona
grandis at 10.3% (FRA, 2001) (Table 1). In tropical Africa, about half of the
plantation area is occupied by eucalypts and pines (mainly Pinus patula). In the
moist parts of West Africa are Gmelina arborea, Terminalia superba and T.
ivorensis, and mahoganies, especially Khaya species. In drier areas in Africa Acacia
mearnsii is planted for tannin production, A. Senegal for gum arabic. Finally, the
Asia/Pacific region has the most diversified plantation sector with eucalypts and
pines on 20% of the total area, with the rest mainly occupied by Tectona grandis,
Acacia spp., Dalbergia sisso, Paraserianthes falcataria, Casuarina spp., Gmelina
arborea, and Swietenia spp. (FAO, 1997). Although large-scale plantations tend to
be of exotic species, there are of course hundreds of native species in the tropics
with potential to be used in plantations. Considerable information on these species
is contained in older works on their silvicultural characteristics (Taylor, 1960), in
summaries of newer research trials (Cameron and Jermyn, 1991; Haggar et al.,
1998) and informal reviews of regionally-based knowledge (Nichols and Gonzalez,
1992).
RESISTANCE IN TROPICAL FOREST PLANTATIONS 289
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2. INSECT OUTBREAKS IN TROPICAL PLANTATIONS

Insect outbreaks may be more or less common in tropical plantations, depending on
a complex of factors, which are discussed near the end of this chapter. Speight
(1997) listed four major causes for insect pest outbreaks in the tropics:
1) Natural disasters – fire, cyclones, drought, and unexpected frost. These events
can create stressed trees and-or produce food or breeding sites.
2) Tree stress and susceptibility through management. This includes the all-
important but often neglected art and science of matching species and provenances
with sites. It also involves good nursery management and the production of healthy
seedlings, the choice whether to plant monocultures or mixed-species plantings,
silvicultural manipulation, particularly thinning to relieve drought and other stresses,
and post-harvest treatments, especially removal or burning of slash.
3) Pest invasions. These can be from outside the country, mainly accidental
imports, and from inside the local area or region.
4) Misuse of control systems. This can mean manipulating a system so that natural
enemies are lost or that tree stress is encouraged by use of phytotoxic chemicals.
2.1 TYPES OF RESISTANCE

One way of categorising resistance is to divide resistance to insect attack into three
major types (Gullan and Cranston, 2000; Watt et al., 2001):
1) Antixenosis, or non-preference, in which a plant is not preferred for use (feeding,

oviposition).
2) Antibiosis, in which insects perform more poorly than on non-resistant plants,

taking longer to complete their life cycles, having greater mortality, or having less
reproductive success.
3) Tolerance, in which a plant can be attacked but maintains health and growth,
recovering from insect attacks.
The differing forms of resistance are quite complex, often difficult to distinguish
from environmental effects, and may or may not be directly inherited. In any case,
the nature of the plant, whether chemical, morphological or physiological, causes a
response in the insect. Physical characteristics such as hairiness or leaf toughness
may deter insect feeding and-or slow it down; plant chemicals may cause insects to
develop more slowly or even die; and some resistant plants be “tolerant” in that they
grow especially quickly through the stage at which they are susceptible (Watt et al.,
2001).
Among the many physiological forms resistance takes are: differences in
morphological structures and tissue strength, in the exudation pressure and quantity
and quality of gums and resins, differences in nutrient levels, hormonally active
compounds in the plant, chemical behavior modifiers, protective substances,
sensitivity to injury, phenology of flowering, leaf flushing and other processes
(Barbosa and Wagner, 1989; Watt et al., 2001).
To what extent resistance is acceptable depends largely on the type of damage
done. Considerable foliar feeding can take place, even to the extent of several
events of nearly total defoliation, without destroying the long-term potential of a
sapling to become a well-formed tree. But only a few attacks by a shoot- or stem-
boring insect can ruin the form of a tree, rendering it economically worthless.
2.2 TROPICAL TREES AND RESISTANCE

It can be argued that some temperate forest species, such as Douglas-fir,
Pseudotsuga menziesii in the Pacific Northwest of the USA, or various pine species
in the Southeast, tend to form nearly pure stands naturally and have evolved
mechanisms for co-existing with herbivorous insects. But in the tropics, particularly
in humid lowland rainforests, there is a high diversity of tree species and one of the
most often invoked theories to explain this phenomenon is the Janzen (1971)-
Connell (1970) hypothesis, also called the “Escape Hypothesis”. They argue that
predators on seeds and species-specific herbivores on seedlings are quite dense near
mother trees and tend to eliminate all progeny in the immediate vicinity of those
trees, with only the occasional seedling “escaping” by being at some distance away
from its parent. Thus creating pure stands of single species would not mimic the
diversity of tropical rainforests and those plantations would not be “resistant” to
pests and would be inviting major outbreaks.
2.3 DETERMINING THE PRESENCE OF RESISTANCE

Determining whether a given provenance or clone is truly resistant to a specific
insect pest is not as straightforward as it might appear at first glance. One technique
is simply to look through plantations under attack for apparently resistant
individuals. Whether these have escaped merely through chance or perhaps flushed
later or earlier than other trees within the plantation are possibilities, as well as their
being genetically resistant.
The other technique is of course to plant replicated trials of a group of species
and-or provenances or even known genotypes and assess their performance in
relation to a given pest. Then a decision would have to be made which considers
resistance to one pest in the context of the relative growth rates of the tree species or
provenance, its wood quality, site adaptations, susceptibility to other insect pests and
diseases, and the maintenance of genetic diversity. So simply having some
resistance to a given insect of course cannot be the only criterion for selection.
In several cases, there is a complex of tree species within a genus or genera as

well as a complex of insect species within a genus. Thus the search for resistance
may span a group of species. Often the most commonly planted and most available
species is the one which is most susceptible to pest damage. In the genus Leucaena,
in addition to intraspecies evaluations of resistance by provenance or genotype,
comparative evaluations have been made of the growth and resistance to the
Leucaena psyllid Heteropyslla cubana Crawford (Homoptera: Psyllidae) of species
other than the commonly planted L. leucocephala (Austin et al., 1995). The same
sort of pattern is seen with Cupressus lusitanica and other species within the
Cupressaceae, with respect to their resistance to the cypress aphid Cinara cupressi
(Obiri, 1994).
2.4 MAJOR TROPICAL FORESTRY PLANTATION SPECIES

2.41 The Meliaceae
Among the most valued of tropical timbers are those coming from several genera in
the Meliaceae, particularly members of the sub-family Swieteniodeae. These
include Swietenia macrophylla Jacq. (American mahogany) and Cedrela odorata L.
(Spanish cedar) from the American tropics, Toona ciliata M. Roem from Australia
and Papua New Guinea, and various Khaya spp. from Africa. The major pest of this
sub-family is the mahogany shoot borer Hypsipyla grandella Zeller (Lepidoptera:
Pyralidae) from the neotropics and Hypsipyla robusta Moore from Africa and the
Asia/Pacific region. The larvae from these moth species bore into the tips of young
trees and cause bifurcations, rendering the tree economically worthless (Newton et
al., 1993; Mayhew and Newton, 1998; Watt et al., 2001). Recent taxonomic
assessment suggests there are probably eleven species of Hypsipyla world wide, but
H. grandella and H. robusta are still likely the most important species (Horak 2001).
There have been some indications that exotic species of the Swieteniodeae are
less susceptible to the local species of Hypsipyla, that is African and Asian
Meliaceae. should do better in the Americas and American tree species should suffer
less shoot boring when planted in the Asia-Pacific region or in Africa. Eventually
one would expect a breakdown of the defenses to whichever species of the shoot-
borer is present (Zobel et al., 1987), Swietenia macrophylla from the Americas was
perhaps at first resistant to H. robusta when planted in the Asia/Pacific region but
reports from countries in the area indicate this is no longer true (Floyd and
Hauxwell, 2001). Similarly, although Cedrela odorata has been grown successfully
in Ghana (Atuahene, 2001), it is attacked by H. robusta in Australia (Cameron and
Jermyn, 1991). Khaya spp. from Africa have been grown without attack in Latin
America and Toona ciliata from Asia/Pacific has demonstrated some resistance to
the American H. grandella (Watt et al., 2001). For example, Rodriguez (1980)
found in Cuba that Khaya myasica, K. senegalensis and K. ivorensis showed high
levels of resistance to H. grandella. In areas that are naturally Hypsipyla-free there
are still productive S. macrophylla plantations, including in Samoa and Fiji.
Unfortunately, simply recommending that exotic Meliaceae be planted, in pure
stands and with no silvicultural manipulations, “is not the answer to the shoot borer
problem” (Watt et al., 2001).
The mechanisms for resistance in the Meliaceae are complex, involving growth
rates, the phenology of leaf production, and nutrient and secondary compounds in
foliage. Newton et al. (1998, 1999) reported on progeny/provenance trials of
Cedrela odorata and provenance testing of Swietenia macrophylla in Costa Rica in
which intensive assessments were made over 84 months. Height growth by
provenance was significantly different in both species. C. odorata from a wet zone
provenance remained foliated but more than 35% of the leaves of dry zone trees
abscised during the dry season. The mean number of attacks during the peak of
attack (during the second year of growth) varied significantly by provenance for
both tree species. A provenance from San Carlos, Costa Rica was subjected to
fewer attacks during the first year and had a significantly higher mean height to first
point of damage. In this provenance foliar nitrogen concentration was significantly
lower and tannin and proanthocyanidin contents significantly higher than in the
other provenances. Thus both vigorous apical growth (tolerance) and foliar
chemical content (possible antibiosis) were found to be components of partial
resistance to the shoot borer . A poll rating research priorities by persons attending
a conference of Hypsipyla placed research on resistance trees above all other
priorities (Floyd, 2001). The role of resistant in developing integrated pest
management in plantation programs for the Meliaceae is discussed at the end of this
chapter.
2.4.2 Tectona grandis

Teak is one of the world’s most prized woods, having been long appreciated for its
resistance to decay and for its attractive timber. Teak is native to India, Myanmar,
Thailand and Laos and marks the one exception to the general rule that successful
tropical plantations are of exotic species, with considerable areas of teak being
grown in the countries where it is native. Approximately 400 to 600 years ago teak
was introduced to Java, Indonesia, where it now naturalised and there are some 1.5
million ha of plantation. The total planted around the world is somewhere between
2.2 and 5.7 ha. (FAO, 2001; Pandey and Brown, 2001).
Perhaps the most serious pest of teak is the teak defoliator Hyblaea puera
(Lepidoptera: Hyblaeeaidae). The larvae of this moth can cause significant
defoliation in teak plantations. As Speight and Wylie (2001) point out, a study by
Nair et al. (1989) indicated initially that two clones of 25 appeared to have much
lower susceptibility to this herbivore. But subsequent studies showed that those two
clones were in fact no more resistant to defoliation than the other clones tested and
merely out of some unexplained phenomenon were not attacked early in the study.
In searching the Indian state of Kerala for resistant clones in plantations, natural
forests and seed orchards, they encountered unattacked trees, but concluded that this
was due to “phenological resistance”, that is some trees did not make tender foliage
available at the right time in the insect’s life cycle. But this characteristic was not
consistent over several years and therefore could not be used in breeding programs.
Avinash et al. (1998) further evaluated the variation in resistance to H. puera as

well as to the teak leaf skeletonizer Eutectona machaeralis (Lepidoptera: Pyralidae).
They found that over a 4-year period, of some 167 clones from 10 Indian states, two,
ORANR-3 and APT-14, could be identified as the most resistant and most
susceptible. They also categorized the remaining clones into eight different levels,
from highly resistant to most susceptible. Foliar phosphorus, calcium and
magnesium were significantly higher in the most resistant clone and lower in the
most susceptible, while chlorophyll a and b were at a minimum in the most resistant,
and a maximum in the most susceptible. In further studies on yet another teak
defoliator, the leaf skeletoniser Paliga machoeralis (Lepidoptera: Pyralidae),
Avinash et al. (2000) analyzed leaf protein and polyphenol contents for selected
resistant and susceptible teak clones. The protein and polyphenol contents of clonal
leaves were directly and inversely proportional to the amount of leaf damage, so that
a low protein:polyphenol ratio was associated with higher resistance and vice-versa.
Roychoudhruy and Joshi (2000) also found that the most resistant and susceptible
clones in the studies by Avinash had the same response to a nursery pest,
Spodoptera litura (Lepidoptera: Noctuidae).
2.4.3 Pinus species

The pines illustrate the complexity of matching species with site as well as finding
the species most resistant to the insects which are likely to become pests in a given
area. Among the pines planted in the tropics are P. caribaea, P. patula, both native
to the Americas, and P. merkusii, native to Sumatra in Indonesia. One of the
problems with pines as well as other species is that the best growing, most well-
known species or subspecies are: 1) the most susceptible to certain insect pests and
2) their seed is the most available.
For example, Cremiere and Ehrhart (1990) reported on 30 years of experience
with pines in New Caledonia and concluded that Pinus caribaea subsp. hondurensis
had the best performance overall, in terms of tree growth, mortality, shape and
resistance to both cyclones and fire. But this pine, one of the most widely planted in
the tropics, is, as Speight and Wylie (2001) point out, in some areas the most
susceptible to local insects.
In the Philippines, Speight and Speechly (1982) recorded heavy attacks by pine
shoot moths, Rhyacionia and Dioryctria spp. (Lepidoptera: Tortricidae and
Pyralidae) on the P. hondurensis subspecies. Another variety, P. caribaea var.
bahamensis is almost completely resistant (Baylis and Barnes, 1989). But seed of
the hondurensis subspecies was what was available, well known, and therefore
planted. In other areas, P. caribaea might be the best choice not only for its
desirable growth properties but also for its resistance to Dioryctria larvae; in
Indonesia the indigenous species P. merkusii was more susceptible to Dioryctria
damage than either P. caribaea or P. oocarpa, both from the Americas (Intari and
Ruswandy, 1986).
2.4.4 Eucalyptus species

There are more than 500 species of Eucalyptus native to Australia; they occur
naturally from near-rainforest conditions to low semi-arid woodlands (Eldridge et
al., 1994). Several of these have become of great importance as exotics in
plantations, with more than 20 species being planted commercially in about 50
countries (Ohmart and Edwards, 1991). Although some 96 indigenous herbivores
have adapted to feeding on eucalypts in different parts of the world, generally they
appear to have caused little harm, while insects native to Australia which have been
accidentally introduced have been responsible for much more damage (Ohmart and
Edwards, 1991). Termites have caused major mortality of eucalypt seedlings in
tropical and subtropical regions so that, without control measures, plantations may
not be established. In Brazil and other parts of the American tropics leaf-cutting
ants, particularly those in the genus Atta, can also cause defoliation and tree
mortality. There have been at least 21 species of Australian insects recorded
overseas on eucalypts. The most widespread of these is the stem-borer Phoracantha
semipunctata (Coleoptera: Cerambycidae), having the biggest impact in countries
where droughts are frequent, and providing a good example of the need to plant
drought-tolerant species in drought-susceptible areas (Speight and Wylie, 2001). A
weevil, Goniptera scutellatus (Coleoptera: Curculionidae), is the other major pest,
which caused major defoliation of eucalypts, particularly in South Africa, but has
been brought under control by the use of an egg parasite. Strepsicrates rothia,
Meyrick (Lepidoptera: Tortricidae) occurs in humid tropical Africa. In Ghana, it
has been recorded on E. tereticornis and other eucalypt species (Cobbinah, 1973).
E. tereticornis is the most preferred species. The larvae roll single leaves of
eucalyptus, forming a shelter in which it feeds and rests. Damage to eucalyptus
seedlings is high at the beginning of the dry season and seedling mortality may
exceed 50%.
Among the most important planted eucalypts is E. camaldulensis (river red
gum), a highly variable species, and the most widely distributed in its natural range,
from below 13° S to above 38° S latitude. E. camaldulensis is perhaps the most
widely planted tree species in arid and semi-arid areas of the world (Eldridge et al.,
1994). In the 1980s some two tons of seed was exported annually from the northern
(tropical) Australian provenances (one ton yielding approximately 600 million
germinants). Mitchell and Boland (1989) tested a large number of tree species in
Zimbabwe, looking at growth rates and at resistance to termites. E. camaldulensis
had the second-highest growth rate but two-thirds of its seedlings were killed by
termites during the establishment phase. On the other hand, Oliveira et al. (1984)
studied the resistance of 11 eucalypt species to the defoliator Thyrinteina arnobia
(Lepidoptera: Geometridae) in Brazil, and found E. camaldulensis to be the most
resistant.
E. tereticornis (forest red gum) is closely related to E. camaldulensis. Its natural
range was extensive, covering some 30° of latitude, from southern Papua New
Guinea through the summer rainfall region in Queensland down to the cool, wet
winter rainfall climate in Victoria. E. tereticornis tends to be more of a coastal
species than E. camaldulensis although there is a considerable zone of overlap

where trees with intermediate characteristics are found, in northeast Queensland.
Eucalyptus grandis forests are native to northern New South Wales and
southeast Queensland, with another population found in northern Queensland, in
both cases within 100 km of the sea. Generally E. grandis is one of the fastest
growing trees on good sites in subtropical and warm temperate sites while pure E.
grandis is not considered suitable for lowland regions in the humid tropics (Evans,
1992). E. grandis may occupy the greatest area of plantation for industrial wood
production of any eucalypt, with well over one million hectares in Brazil and large
areas in South Africa.
In what may well be a sign for the future, Harcourt et al. (2000) reported on the
development of insect- and herbicide-resistant transgenic eucalypts. They used an
Agrobacterium tumefaciens-mediated transformation of seedlings to produce E.
camaldulensis containing the insecticidal cry3A gene and the bar gene. The former
gene gave resistance to first instars of chrysomelid beetles and the latter gene
provided tolerance to the broad-spectrum herbicide glufosinate ammonium. The
authors stressed the importance of assessing and minimizing any adverse impacts of
wide scale planting of transgenic eucalyptus.
There are only two eucalypts species which do not occur naturally in Australia,
and both are planted extensively throughout the tropics. One of these is E. deglupta,
native to Mindanao in the Philippines, Sulawesi and Irian Jaya in Indonesia, parts of
Papua New Guinea, and on most of New Britain (Eldridge, 1994). E. deglupta is
well known for its impressive growth rates on good sites ( over 15
years). But it is demanding in terms of site, can burn easily, does not coppice as
easily as many eucalypt species do, and is susceptible to some diseases as well as
insect pests, including termites. The countries with the largest plantations are the
Philippines, Indonesia and Brazil, with perhaps 100,000 hectares having been
planted worldwide (Eldridge, 1994).
The varicose borer Agrilus sexsignatus has been a cause of major mortality in E.
deglupta plantations of the Paper Industries Corporation of the Philippines (PICOP)
since 1975. Braza (1987a) pointed out that previous studies had suggested that only
trees under stress were attacked by the borer. He implanted borer larvae into healthy
plantation trees and found that larval development was prolonged and larval survival
quite low on an indigenous provenance of E. deglupta, in contrast to the heavily-
attacked Papua New Guinea provenance. Thus a local native tree species may in
some cases have an advantage over an exotic species or provenance which has not
evolved any resistance mechanisms to cope with a given pest.
The other non-Australian eucalypt is E. urophylla S.T. Blake, native to Timor
and several nearby islands in Indonesia between 7° 30 S and 10° S. In the case of a
white grub Leucopholis irrorata (Coleoptera: Scarabidae) in the Philippines, E.
deglupta, E. urophylla, Acacia mangium and Pinus caribaea, had their roots fed
upon heavily. Braza (1987b) recorded mortality rates of 50-80% after two weeks
exposure. This is an example of a generalist rather than monophagous pest which,
like leaf-cutting ants, is difficult to control. For a discussion of E. grandis x E.
urophylla crosses and their resistance to one pest species, see the section below on
hybrids.
2.4.5 Acacia species

Acacia mangium is native to the the Moluccas, Irian Jaya and northern Queensland
in Australia. It the 1960s it was introduced to Sabah, Malaysia where it is a major
component of a 200,000 ha reforestation program. A. mangium is also of great
importance in Indonesia, where it has been highly productive in reforestation
programs on vast areas of degraded Imperata cylindrica grassland, with there now
being at least 500,000 ha planted, mostly in Sumatra and Kalimantan (Nair and
Sumardi, 2000). Thus, although A. mangium is native to Indonesia it is only so in a
very small part of the country and can be considered an exotic throughout most of
that country.
The sap-sucking mosquito bug, Helopeltis spp. (Hempitera: Miridae) is a
common pest on several horticultural crops as well as on Acacia mangium. Feeding
by Helopeltis causes necrotic spots and often dieback of young shoots (Wylie et al.
1998) and represents the most serious insect threat to A. mangium plantations in
Indonesia (Nair and Sumardi, 2000). Other pests include the subterranean termite,
Coptotermes curvignathus (Isoptera: Rhinotermitidae) which can kill 10-50% of
saplings by eating into the taproot and stem (Wylie et al., 1998) and several pinhole
borers in the genus Xylosandrus (Coleoptera: Scolytidae).
Not a great deal of work on resistance to insects in tropical acacias appears to
have been done (Wylie et al., 1998; Nair and Sumardi, 2000). In a comparison of
early performance of Queensland and Papua New Guinea (PNG) provenances of A.
crassicarpa, Otsamo et al. (1999) found that there were no significant differences in
occurrence of pests and diseases among the PNG provenances but that the PNG
provenances had a higher proportion of trees affect by borers (Xyleborus spp.,
Coleoptera: Scolytidae) than the Queensland provenances. In another case
Faizuddin and Dalmacio (1992) found great variability to pests and diseases in
different provenances of A. mangium in platations in the Philippines.
2.4.6 Cupressus lusitanica

Cupressus lusitanica, native to highland areas of Mexico, Guatemala and El
Salvador, has been widely planted in mountainous areas in the tropics, particularly
in East Africa. Its major pest is the cypress aphid Cinara cupressi (Murphy 1998).
To assess other related conifers Obiri (1994) reviewed the growth rates and
tolerance of the aphid on 24 species within the Cupressaceae in Kenya. Thuja spp.
and Chamaecyparis leylandii were the most tolerant. Several of the cypresses,
Cupressus torulosa, C. funebris and C. arizonica were very resistant while the
commonly planted C. lusitanica was found to be susceptible. Kamunya et al. (1997,
1999) studied genetic control of resistance to Cinara cupressi. They concluded that
there was a strong additive genetic element in resistant trees of C. lusitanica, and
that genetic correlations between aphid damage and growth characteristics were not
significant, so that selection for resistance would be unlikely to have a negative
effect on these economic traits.
2.4.7 Milicia species

Milicia excelsa and M. regia are important timber species across Africa from Kenya
to Senegal. Their situation is similar to that of many of the Meliaceae: in natural
forests Milicia occurs in low densities and when established in plantations it is
severely attacked by an insect, prohibiting production to date from other than natural
forest. Again, as in the case of the mahoganies, developing tree resistance to the
pest is part of a strategy to grow it successfully (Wagner et al., unpublished data).
Perhaps no tree in tropical Africa has been studied more intensively for
resistance than Iroko (Milicia spp.). The pest, Phytolyma lata, a gall forming
psyllid, attacks seedlings and saplings of Milicia forming globular galls. When galls
burst to release adults, the surface fluid is colonised by saprophytic fungi, which
cause dieback. In nurseries and young plantations, large numbers of galls on leaves
and petioles lead to loss of leaves and often times seedling mortality. Prospects for
reducing the impact of P. lata increased with the observation of partial resistance
within natural populations (Cobbinah, 1990). Progeny evaluation by Cobbinah and
Wagner (1995) indicated highly significant variation among 21 half-sib families in
growth and resistance to galling. Further, Ofori et al. (2001) and Appiah et al. (In
press) recorded significant differences among populations and provenances from
Ghana, Cote d’lvoire and Sierra Leone with regard to growth performance and
resistance to P. lata attack (Figure 1). Family and clonal heritability values of 0.94
and 0.3 respectively were observed. Selective removal of less desirable genotypes
resulted in genetic gains of 12 cm in height growth in three months and 22.8 cm in
two years for progeny and clones respectively (Ofori et al. 2001). RAPD survey of
natural populations of Milicia indicated a substantial degree of genetic variation
which is ecologically structured (Ofori et al. unpublished data).
Earlier anatomical (Djabletey, 1994) and chemical (Gbowonyo et al.,
unpublished data) studies indicated that resistant genotypes have two fold more
tannin containing cells and more total phenols and phenolic oxidase activity than
susceptible genotypes. However, because of the likelihood that resistance could
break down, an Integrated Pest Management strategy has been developed for P. Lata
(Cobbinah, 1990; Wagner et al., 1991).
2.4.8 Leucaena species

Leucaena species, particularly L. leucocephala (Lamb.) de Wit, native to Mexico
and Central America, have been widely planted as agroforestry species around the
world in the tropics. Leucaena is a fast-growing nitrogen-fixing tree, useful in alley-
cropping, for soil conservation and enrichment, and as fuelwood and fodder. One of
the major problems Leucaena has had is the leucaena psyllid, Heteropsylla cubana
Crawford (Homoptera: Psyllidae). The psyllid has spread to the Asian/Pacific
region, causing serious devastation, even at moderate damage ratings, with yield
loss in dry weight often being >50% (Mullen et al., 1998). H. cubana was the
subject of a workshop (Napompeth and MacDicken, 1990) and continues to be
widely studied.
Considerable variation has been found in resistance to the leucaena psyllid both
within and among species (Napompeth and MacDicken, 1990; Austin et al., 1995;
Mullen et al., 1998). Generally L. leucocephala – like P. caribaea the most
commonly planted and available tropical species in the genus – has proven to be the
most susceptible. Other species, particularly L. diversifolia (Austin et al., 1995;
Hosalli and Kulkarni, 2000) and L. collinsii (Lapis and Borden, 1993), have been
much more resistant, as well as L leucocephala x L. diversifolia hybrids (Elder et
al., 1998) and some cultivars of L. leucocephala (Austin et al., 1995). Ultimately,
resistance to the psyllid is only one of several desired characteristics selected for in
breeding programs; strategies in Hawaii and Brazil are based on using tetraploid-
level crosses of L. leucocephala, L. pallida and L. diversifolia to achieve several
objectives, including psyllid resistance, increased biomass yield, cold tolerance, and-
or acid-soil tolerance (Austin et al., 1997, 1998). In this case wood production is
not as important as dry weight production of forage. But the quality of that forage
must also be considered. As Speight and Wylie (2001) point out, the secondary
chemicals (possibly tannins) which make species or genotypes of leucaena psyllid-
resistant may also make it less palatable to livestock, so that resistance has to be
balanced with other characteristics.
2.5 HYBRIDS AND RESISTANCE

In many cases insects are more diverse and abundant on hybrid trees than on pure
species, whether those trees occur in natural forests or plantations (Floate et al.
1993; Fritz, 1999; Whitham et al., 1999). To judge the effect of plant genetics on
arthropod richness and composition, Dungey et al., (2000) examined arthropod
communities on both artificial and wild populations of Eucalyptus amygdalina, E.
risdonii and and hybrids. Different communities were supported on pure
species and hybrid populations. In both artificial and wild populations the hybrids
supported higher arthropod richness, with hybrids being a center of biodiversity by
accumulating both common and specialist taxa of both parental species. In a review
of 152 case studies of taxa associated with diverse hybridizing systems, Whitham et
al. (1999) found that in 28% of cases, hybrids were more susceptible than their
parent species. Thus planting pure stands of hybrids in the tropics would appear to
be risky business, given that tropical trees naturally protect themselves by being rare
and that hybrids often are more susceptible to pest and disease damage.
The parent species in hybrids can contribute resistance or susceptibility to
herbivores. Shepherd et al. (2000) examined variation and resistance to Christmas
beetles, Anoplognathus porosus (Leach) (Coleoptera: Scarabaeidae) in Eucalyptus
grandis and E. urophylla. E. grandis is native to the Christmas beetle home range,
whereas E. urophylla is not. Backcrosses of E. grandis x E. urophylla to E.
urophylla had higher amounts of leaf area consumed than other second generation
controlled crosses (Figure 2). E. urophylla is a tropical eucalypt, not native to
Australia, does not encounter A. porosus in its native habitat, and therefore may be
the source of susceptibility to the beetle. Clones of E. grandis from open, drier
forests, as opposed to tall moist closed forests, may represent a source of resistant
individuals. Thus a native species which has co-evolved with an insect pest may
transfer some resistant characteristics in hybrids.
The implications for plantation forestry - particularly in the tropics – where tree
species may not have evolved anti-pest mechanisms - is that care needs to be taken
in committing to plant large areas with a small genetic base of hybrids, which may
have desirable growth characteristics, yet be highly susceptible to potential insect
pests.
2.6 DEPLOYMENT OF RESISTANT TREE STRAINS

In a sense the most common form of resistance that is actually deployed is using an
exotic tree. For the most part, large successful plantations of trees in the tropics are
of species planted outside their native ranges (Table 1).
Traditionally the focus of tree breeding for plantations has been on survival,
growth, form (straightness being an especially heritable characteristic) and wood
quality, and only secondarily on resistance to pests and diseases (Zobel et al., 1987).
Aracruz Celulose in Brazil, represents one of the largest plantation efforts in the
tropics, planting eucalypts for pulp production. Laranjeiro (1994) discussed the role
of resistant stock in the company’s integrated pest management strategy. One
technique used is to maintain 1 ha of native vegetation for each 2.4 ha of eucalypt
planting, thus enhancing the presence of natural enemies of insects which may reach
pest status. Also, systematic monitoring of insect levels is done, and occasionally
various chemical sprays are applied, as is Bacillus thuringiensis. One of the most
serious problems comes from leaf-cutting ants, in this case Atta sexdens rubropilosa.
In eucalypt trials some 90% of plants were totally defoliated. The ants showed
preferences that were categorized as high, medium and low. Laranjeiro advises that
careful analysis of results be done, considering that preferences varied between
species and provenances. Choosing clones solely on the basis of low leaf-cutting
ant preference was not completely strategically suitable for integrated pest
management of all pest species, or for maximum forest productivity and quality– it
being judged not commercially viable to eliminate a clone with good productivity
and quality only because it is preferred by ants.
2.7 RESISTANCE AND EXOTIC VERSUS NATIVE PLANTATION TREES

Considerable confusion abounds on the topic of native vs. exotic tree species,
natural forests vs. plantations, and monocultures vs. mixed-species plantations
(Zobel, 1987; Gadgil and Bain, 1999). Although it would seem intuitive that mixed
stands should be more resistant to insects and diseases, the vast majority of
plantations in the tropics as well as in the temperate zone are monospecific, given
that it is considered impractical to plant and harvest several different species. Since
large areas in temperature North America are naturally occupied by single (or nearly
single) species stands, particularly by Pinus spp. in the West and Southeast and
Pseudotsuga menziesii in the Northwest, often resulting from large-scale fires, it has
seemed reasonable to use pure plantations of those species, which may well have
evolved their own mechanisms for co-existing with indigenous insect populations.
But in the tropics, where highly diverse forests are the norm, it would appear to be a
risky strategy to plant monocultures. This is where the issue of exotic vs. native
species comes in: most tropical plantations to date, have been of exotic species,
either exotic within a region, or more commonly exotic by originating on other
continents. Rubber (Hevea braziliensis) coffee (Coffea arabica and C. robusta) and
cacao (Theobroma cacao) are all examples of tropical plants which have been
grown successfully away from their continents of origin. Similarly in plantation
forestry, eucalypts from Australia and far southeast Asia, have been successful in
India, China, the Americas, especially Brazil, and in South Africa. Likewise,
tropical pines from Central America have had great success pantropically. The one
great exception would be teak, Tectona grandis, which is grown in its native range
in India, Myanmar, and Thailand as well as around the world. Teak may be
somewhat different in that it is not native to equatorial regions with a year-round
wet season but from areas with significant dry seasons. Also, the extractives which
make it such a valuable timber may provide some resistance to insect pests.
As Nair and Sumardi (2000) argue, it is difficult to make a generalization about
whether exotic or native species are more pest-susceptible. In the case of Indonesia,
most planted species are exotic and both exotic and native species have serious pest
problems, with examples being the indigenous Pinus merkusii and the exotic
Swietenia macrophylla. They point out that an indigenous species is unlikely to be
destroyed completely, as it would have co-evolved with a given pest. But an exotic
would be, at least for a while, free from pests native to its home range, although
such pests, once introduced can have catastrophic impacts. Examples are the
leucaena psyllid, conifer aphids, eucalypt trunk borers and the weevils. The exotic
tree species may also be susceptible to local pests and diseases to which it has not
adapted.
The issue of native vs. exotic species is often confused with the differences
between natural mixed stands and monospecific plantations. A large expanse of a
native species of a limited genetic base, fast-growing, and producing nutritious,
tender foliage, would seem to invite outbreaks of native pests, which are normally
held in control by the diversity of tree species and age classes and a complex of
natural enemies found in native forest. Thus developing a new set of influences
artificially, using proper site-species matching, an understanding of pests’ life
cycles, biocontrol agents, judicious spraying of pesticides in certain cases,
silvicultural manipulations and genetically-based resistance would all be involved in
developing successful tropical plantation regimes.
2.8 USE OF RESISTANT TREES AS PART OF AN INTEGRATED PEST

MANAGEMENT STRATEGY
Rather than taking the crude and expensive approach of simply spraying any pest
species with toxic insecticides, integrated pest management aims to develop a
sophisticated understanding of a given pest’s life cycle, and then to recommend
appropriate, minimally invasive if possible, methods of management. These may
include silvicultural techniques, such as regulation of stand density, pruning, etc.,
spraying at key times in the pest’s life cycle, the use of biocontrol organisms and the
use of completely or partially resistant tree stock (Elliott et al., 1998).
The role of resistant trees in an integrated pest management program can be
considered in two major groups of species: Milicia species in Africa and the
mahoganies (Meliaceae) pan-tropically. Wagner et al. (2000) outlined the
components of a research program designed to develop production of Milicia in
Africa. As discussed above, provenances resistant to the gall-forming psyllid
Phytolyma lata have been identified and cuttings from them can be utilized in
planting programs. But resistance is not total; in fact levels of dieback among more
resistant stock are still not acceptable for commercial plantation forestry. So in
addition to recommending the use of partially resistant trees, it could also be
recommended that silvicultural techniques such as planting Milicia in low densities
in a matrix of other plantation species or in native forest (enrichment planting) may
enable some individuals to escape serious dieback. Further, exploration for
biocontrol agents may yield some predators or parasitoids that can lower populations
of P. lata (Bosu et al., 2001).
In the case of the Meliaceae, Newton et al. (1993) suggested using resistant tree
stock in combination with silvicultural methods, namely establishing mixed-species
plantations or enrichment plantings in natural forest, although the exact
requirements in terms of site-species matching, shade, densities, and so on are not
known. They also advocated combining these methods with chemical and
biological controls, while admitting that losses to Hysipyla would still take place. In
a later assessment, Speight and Cory (2001) state that mahogany can still not be
successfully grown, since Hysipyla is a pest which has high impact, making timber
production uneconomic, at low insect densities. They propose that the development
of an integrated pest management program for Hypsipyla spp. should involve
several levels. The first of these can be called preventative, including careful site
choice so that low tree vigor is avoided, selection of resistant species or genotypes,
understanding the presence of pest in the region and nearby forests, designing
silvicultural systems, and so on. The second stage involves on-going monitoring,
particularly during vulnerable growth periods and devising a definition of economic
threshold that would indicate the need for treatments. The third level covers control
strategies which would have to be applied if prevention fails or modelling predicts a
serious risk of outbreak.
3. SUMMARY
Tropical forest plantations are a major source of wood fiber throughout the world.
These plantations are subject to depredation by pest insects much like other forests
of the world. The use of exotic species is a common form of managing forest pests,
but this approach is not without limitations in general and is certainly not a
sufficient control strategy to limit all pests. Substantial work has been done to
understand mechanism of resistance in tropical tree species such as mahogany, teak,
pine, eucalyptus, Leucaena, Acacia, and Cupressus. A pest-resistant transgenic
Eucalyptus has been developed but is not operationally deployed. The substantial
diversity of tropical trees represents both an opportunity to search for resistance to
pests and a challenge to manage the huge array of current and potential forest insect
pests.
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Keyword Index
abietic acid 123, 275 attack failure 109

abiotic environment 3 attack pressure 48
abiotic factor 4, 247 attack rate 107, 108, 111
abiotic induction 1 attack strategy 49
accidental introduction 67 attractant 108, 113, 154, 155, 164, 275
activated defense 32 attraction 17, 67, 110, 125
adaptation 5, 11, 65, 67, 108, 124, attractive odor 113
176, 227, 258, 293 axial parenchyma cell 36
adapted insect 6, 7, 9, 12, 14, 90
additive inheritance 155, 159, 164 bacteria 15, 138
aggregation 35, 37, 47, 48, 50, 56- balance between carbon and nutrient
60, 66, 67 availability 6
aggressive agent 46, 139 balance between growth and
aggressor 33-35, 39-41, 43, 44, 46- differentiation 6
51, 55, 56, 61, 64, 65, 67, 68, bark beetle 6, 13, 14, 16, 31-33, 35-39,
243, 245, 247, 248 41, 43-45, 47-68, 71, 73, 75, 77,
alkaloid 5, 11, 122, 125 132, 133, 140, 179, 183, 226, 228,
allelochemical 81, 100 240, 243-246, 249, 251, 253, 255-
allocation cost 8 258
allocation of resources 6 bark beetle attack 13, 14, 31, 32, 38,
ambrosia beetle 132 41, 43, 44, 48-51, 62, 68, 133, 243,
amplification 39, 44 244, 246, 257
anatomical 33-35, 39-41, 43, 44, bark beetle attack strategies 31
46-51, 55, 56, 61, 64, 65, 67, 68, bark beetle biology 31
243, 245, 247, 248 bark beetle life cycle 31
antibiosis 4, 292, 295 bark resin canal 109, 114, 117, 119,
antibiotic effect 110 121, 124, 125
antifungal properties 36 bark thickness 32, 109, 115, 121, 123
anti-predator defense 17 beetle aggregation 35, 37, 47
antixenosis 4, 292 beetle behavior 49
apical dominance 132 beetle colonization strategies 49
apparency 6, 108, 113, 114, 125, beetle establishment 56
173 beetle galleries 39, 57, 251
artificial diet 90, 92-97, 199 beetle maternal galleries 49
artificial inoculation 33, 51, 52, 57, beetle success 38, 50
58, 61, 63, 255 beetle-associated fungi 46, 60
artificial larval diet 11 behavior, avoidance 4
asynchronous attack 48 behavior, feeding 198, 240
asynchrony 8, 79, 83, 100, 101, 242 behavior, oviposition 4, 112
attack behavior 59 behavioral adaptation 5
attack densities 47, 51, 62
311
312 KEYWORD INDEX
bioassay 6, 12-14, 52, 64, 83-86, cage experiment 114, 115

88, 92, 95, 99, 101, 114, 173, cambial layer 132
175, 176, 197, 198 cambium 51, 117, 120, 121, 131, 132,
biochemical 5, 6, 12, 44, 45, 99, 141, 274, 276, 278
109, 121-123, 138, 139, 175, camphene 95, 249, 250, 275
248, 249, 251 carbohydrate 5, 80, 81, 90, 249, 251,
biochemical adaptation 5 254, 255, 257
biochemical cascade 12 carbon allocation strategies 13, 81
biochemical change 139 carbon-based defensive chemical 82
biochemical indicator 248, 249 carbon-nutrient-balance-theory 253
biorational spray 206 carene 123, 164, 249, 250, 275
biotic 1, 3, 4, 11, 14, 15, 16, 19, 39, carpenterworm moth 131
58, 67, 110, 171, 172, 193, 224, cell 2, 12-14, 17, 32, 33, 35-41, 43, 44,
240, 247, 248, 250 47, 48, 50, 59, 109, 115, 119-121,
biotic agent 14, 171 124, 133, 134, 139, 140, 141m 154,
biotic aggression 39, 240 251
biotic environment 3 cell differentiation 121
biotic factor 4, 247, 250 cell division 36, 40, 41, 43, 47
biotype 11, 140, 172, 174, 175, cell metabolism 37, 47
177-183, 195, 196, 204-206 cell necrosis 38
biotype development 177, 179-181 cell wall 139
bisabolene 122, 123, 275 cerambycid reproductive behavior 133
blister 33, 35, 43, 58 cerrado vegetation 143, 144
blue stain 51, 53-55, 58, 63, 64 chalcone synthase 45, 52
borer 105, 131-134, 140, 203, 220, chemical 3, 5-8, 12, 13, 19, 32, 34, 35,
222-224, 227-229, 243, 277, 279, 37-40, 44-46, 51, 64, 81, 82, 99,
281, 294, 295, 297-299, 305 100, 107-110, 113-117, 121-124,
borer colonization 133, 223 133, 134, 138, 139, 150, 155, 158,
boring damage 131 159, 174, 186, 191, 193, 194, 196,
boring sawfly 131 198, 199, 202, 203, 206, 224, 225,
boring species 131 243-245, 248-250, 253, 255, 279,
bornyl acetate 95 281, 292, 293, 295, 300, 302, 304,
breeding program 66, 67, 108, 123, 305
124, 177, 190, 194, 245, 247, choice experiment 109, 114
252, 267, 295, 302 citronellol 95
bud break phenology 84, 85 classical breeding 218, 219, 247, 252
bud burst 79, 84, 86, 88 clean forestry 253, 256
bud flush 84, 242 clearwing moth 131
bud phenology 84, 85 climate change 106
budbreak 7, 116 climate parameter 67
budburst 80, 84, 85, 116, 117 climatic condition 47, 48, 134, 242,
budburst phenology 84, 85 246, 258
bud-galling 156, 158
KEYWORD INDEX 313
clonal deployment strategies 191, de novo resin terpenoid formation 121

194, 196, 208 dead and dying tree 133
clone 1, 10, 36, 42, 64, 66, 83-86, deathwatch beetle 132
88, 89, 95, 96, 99, 101, 109-111, defense system 31, 33-36, 47-50, 62
114, 115, 117, 137, 157, 170, defense-related gene 139
171, 173-179 defensive chemical 32, 46, 51, 81, 82,
colonization by fungus 50 95, 108, 116, 122, 248
colonization process 31 defensive compound 81, 95, 100, 101
colonization strategies 32, 36 defensive function 16, 121, 123
Compartmentalization process 41 defoliator 79-83, 85, 89, 91, 93, 95,
compensation 2, 80 97, 99, 100, 105, 190, 196, 205,
compensatory feeding 4 240, 241, 243, 246, 255, 257, 295-
compensatory growth 3, 80 297
compensatory photosynthesis 80, delayed induced resistance 44
88, 100, 101 delayed induced response 12
compensatory process 2 delayed resistance 36, 41, 50
complementarity 33, 48 density dependent factor 12, 18
complex interaction 16 density dependent mortality 18
condensed tannin 154, 155, 159, deployment decision-making 177
164, 254, 257 deployment of tree resistance 170,
confusion 108, 125, 304 189, 265, 267, 269, 271, 273, 275,
conifer shoot 105, 116, 117, 121 277, 279, 281
constitutive 6, 12, 13, 32, 33, 35, deployment strategies 182, 189-191,
49, 50, 58, 64, 66, 67, 81, 107- 193, 194, 196, 205, 208
109, 114, 117-120, 122, 124, deterrence 46, 67
125, 138, 146, 149, 226, 228, deterrency 114, 119, 123, 124
240, 243-245, 251, 255, 274, 277 deterrent 2, 17, 36, 80-82, 113, 115,
constitutive defense 32, 33, 50, 146, 125, 155, 164, 165
244 detoxification system 5
constitutive resin 35, 117, 118, 120, diet bioassay 83, 92, 101
228, 277 differentiation 6, 12, 36, 40, 41, 43,
constitutive resistance 32, 67, 114, 47, 121, 251, 253
119, 138, 243, 244, 255 digestibility reducer 81
constitutive secondary metabolite 6 dispersal 7, 80, 11, 112, 114
containment 139 dispersal behavior 111
cooperative strategy 56, 60 dispersal capacity 7
cortical resin acid 123 dispersal pattern 112
cossid moth 132 diterpene 52, 123
crop rotation 193, 196 diterpene resin acid 123
cross talk 15 dose-response function 67, 82-101,
cytological 39 293
Douglas-fir 67, 82-100, 293
314 KEYWORD INDEX
drought 3, 7, 133, 134, 171, 223, false powderpost beetle 132

225-227, 253, 255, 256, 258, farnesene 123
292, 297 fecundity 4, 13, 18, 19, 85, 137, 138,
dynamics of herbivore populations 201, 225, 226
138 feeding behavior 198, 240
feeding bioassay 114
early-season feeder 79, 83 feeding deterrency 123, 124
ecological cost 8 feeding deterrent 36
ecophysiological 6 feeding stimulant 115, 198
ectomycorrhizal 82, 100 feeding tunnel 132
egg 4, 13, 17, 57, 59, 60, 80, 81, fertilization 64, 100, 169, 28, 229,
109-112, 114, 117, 119-121, 124, 253-255
206, 207, 225, 227, 242, 243, field-testing for resistance 109
269, 270, 278, 297 fire 133, 292, 296, 304
elicitor 12, 40, 63, 123 fitness 12, 16, 17, 84, 85, 92, 95, 196
endemic range 134 fitness, insect 18
energetic consideration 51 fitness, plant 3
energetic expenditure 51 flood 120, 133, 171
energy-demanding process 51 foliage toughness 89
enhancement of resistance 247, 252 foliar biochemistry 82
enviornmental factors, abiotic 11, foliar terpene 95, 96, 113, 114, 123
224 folivore 226
environmental conditions 49, 64, food quantity 31
112, 154, 246-249, 252, 258 forest pest management 2, 65, 194,
environmental factor 9, 11, 14-16, 239, 245, 246
31, 49, 64, 68, 133, 163, 197, forest protection 67, 240
224, 280 fungal endophyte 100
environmental factors, biotic 11, fungal growth 39, 46
14, 224 fungal infection 42, 155
environmental gradient 154 fungi 31-33, 35, 38-41, 44, 46, 47, 50-
environmental variation 154, 163 60, 63-65, 67, 68, 82, 132, 138, 143,
enzyme 45, 109, 121-123, 139, 251 155, 156, 165, 244, 255, 258, 300
enzyme activities 39, 52, 62, 123 fungistatic effect 39
eucalyptus longhorned borer 133 fungus aggression 40 .
evolution of conifer defense 49 fungus inoculation 47, 51, 52, 54, 250,
evolutionary history 4, 224 255
exhaustion of host defense 50
exhaustion of tree defense 50-52, gall 10, 105, 131, 137, 140-142, 144,
55, 56, 58, 63 147, 156, 164, 241, 256, 266, 269,
exotic beetle 67 270, 281, 300, 305
exotic versus native plantation trees gall diversity 150
304 gall induction 138, 141, 143, 149
gall initiation 7, 143, 256
KEYWORD INDEX 315
galler 140 192, 196, 199-202, 206, 218, 220,

gallery boring 34 221, 243, 251, 253-258, 266, 268,
gallery initiation 34 276, 279, 287, 288, 292=301, 303,
gall-forming insect 137, 140, 143 306
gall-inducing 140, 141 growth and defense 8, 257
galling 140 growth rate 16, 19, 68, 80-82, 86, 88,
galling herbivores 138, 144, 146, 101, 137, 138, 196, 200, 202, 266,
150 287, 293, 295, 297-299
galling insect 8, 138, 140, 143, 146, growth-differentiation-balance-theory
147, 150, 256 253
galling population 144 guild defence 108
galling sawflies 154, 155, 158, 164
galling species 141, 144 hairs 7, 141
galling-agent 140 half-sib seedling 83, 87, 100, 101
gene activation 32, 39, 45, 47 healthy host 132
gene expression 123, 200, 268 heartwood 45
gene transcription 32 herbivore response 154, 156, 160-162
generalist 15, 17, 19, 20, 153, 155, herbivore-induced volatile emission 17
156, 164, 176, 177, 298 heritable trait 84
genetic difference 83, 163, 244 histological 39, 40, 42-44, 48, 138
genetic diversity 169, 173, 180, horizontal galleries 34, 49, 59
182, 219, 229, 247, 248, 253, horntail 131
258, 293 host acceptance 4
genetic engineering 172, 178, 179, host choice 154
190, 194, 199, 204, 218, 219, host plant phenology 80
245, 251, 252 host plant specialization 5, 17
genetic factor 64, 154 host range 4, 164
genetic improvement program 172, host shift 153
173, 177, 183, host-driven mortality factor 144, 146
genetic marker 251 host-selection behavior 111
genetic re-arrangement 153, 165 hybrid 107, 153-165, 183, 190, 191,
genetic resistance 106, 111, 190?, 197-200, 203, 204
173, 246, 247 hybrid chemistry 164
genotype by environment hybrid heterosis 155
interaction 258 hybrid susceptibility 155
geographic distribution 67, 134 hybrid zone 153
ghost moth 131 hybridization 107, 153, 154, 183, 198,
glandular exudate 7 203, 204, 218, 219, 251, 265, 266-
glandular trichome 7 268, 275, 276
growth 3-9, 12, 16, 19, 39, 45, 46, hypersensitive reaction 36-41, 44-46,
57, 68, 80-90, 92-97, 100, 101, 48, 49
116-118, 125, 132, 137, 140, hypersensitivity 137, 140, 146, 149
157, 158, 165, 169, 183, 190,
316 KEYWORD INDEX
hypersensitive response 12, 14, 34, insect adaptation 124

40, 47, 48 insect behavior 4, 111, 201
insect bioassay 12
inactivation 139 insect emergence 80
indirect defense 17 insect fecundity 225
individual strategy 59 insect fitness 17, 18
Induced 12-14, 16, 17, 32, 37-40, insect growth 4, 5, 8, 16, 90
43, 44, 51, 55, 58, 117, 121, 123, insect life history 7, 12, 18
124, 138, 142, 144, 145, 147, insect outbreak 1, 16, 19, 225, 292
198, 240, 244, 250, 256, 273, insect performance 4, 5, 13, 15, 16, 19,
275, 280 225, 228, 243, 256
induced defense 32-34, 36, 37, 41, insect pest management 1
43, 47-49, 64, 81, 99-101, 124, insect population dynamics 12, 15, 16,
125, 133, 137, 244, 245, 255, 19
274-276 insect preference 4
induced plant response 12 insect resistance 1, 173, 177, 180, 181,
induced protection 41-44 183, 196, 202, 205, 208, 218-220,
induced reaction 12, 43, 44, 62, 225, 226, 228, 229, 252, 268
134, 244, 245 insect resistant germplasm 218, 219,
induced resin flow 34, 36, 37, 40, 229
44-47, 52, 58 insect response 2, 9, 11, 15, 90, 178
induced resistance 6, 12-15, 17, 32, insect survival 202
44, 61, 67, 81, 99, 137-139, 143, insect-induced resistance 12
149-151 insect-resistant plant 1, 9
induced response 12, 41, 45, 48, 56, integrated pest management 1, 68,
124, 134, 137 189, 295, 300, 303-306
induced susceptibility 12, 41,45, intercellular communication 39
48, 56, 124, 134, 137 intermediate plant 149
induced synthesis 34 interspecific hybridisation 153, 154
induced trait 146 interspecific tree hybridization 183
inducible plant defense 108 interspecific variation 3, 34, 222, 223
inducible resistance system 146 intra-specific variability 66
inducible strategy 147, 149 intraspecific variation 11, 154
inducing agent 138 invader 32, 138, 139
induction 1, 6, 12-15, 17, 18, 39, irrigation 190, 253, 255, 256, 270
43,44, 99, 101, 114, 138, 141, isoprenoid 122
143, 149, 279
inheritance pattern 154-156, 159, jasmonate 123
164 juvabione-type terpenoid 122
inhibitory effect 46
inoculation 13, 33, 39, 42, 43, 47, key nutrient 90
51-53, 57, 58, 60, 61, 100 key-factor 31
inoculation density 51, 61, 63, 65 kino 133, 134
KEYWORD INDEX 317
larval chemical defense 19 mechanism of resistance 2, 3, 66, 79,

larval defense 18 82, 84, 85, 88, 89, 95, 99, 105, 118,
larval growth 80, 199 178, 179, 240, 277,278, 306
larval predation 18 mechanisms of attack 32, 50
larval survival 18, 195, 202, 243, Mediterranean climate 134
298 meristematic tissue 132, 140
latex 107 metabolic activities 51, 57
leader kill 110, 111 metabolic modification 40
leader silhouette 113 metabolism of cells 36, 37
leafbeetle 7, 17, 154, 156, 158-165, metallic or flatheaded borer 132
222, 226, 228 microbial mutualist 82, 99-101
leaf gall 141, 142, 156, 158, 160, microcapsule 95
161 microorganism 3, 4, 12, 13, 138, 139,
leaf toughness 9, 81, 292 244
leaf-beetle 154, 156, 158, 160, 161 miner 105, 140, 203, 221, 222
leaf-folding 156 mineral 81, 83, 90, 91, 100
leaf-galling 156, 158, 160, 161 minimum threshold 155
lethal density 42 models of tree resistance 2
levopimaric acid 123 modification of resistance 224
life history trait 5, 7, 9, 18 moisture availability 134
life table 109, 146 molecular biology technique 14
lignin 33, 133, 136 monoterpene 33, 40, 45, 46, 52, 57,
lignin stone cell 133 644, 83, 95, 96, 98, 99, 101, 120,
limonene 46, 95, 123, 2751 228, 255
linalool 95 morphological changes 13
localization 139 mortality 7, 16-18, 52, 80, 109, 117,
localized resistance 138 134, 140, 143, 144, 146, 148, 178,
long term response 36 192, 197, 201, 203, 204, 207, 223,
longhorned or roundheaded borer 224, 243, 246, 247, 251, 258, 271,
132, 133 277, 279, 292, 296, 297, 300, 301
long-term induced response 41 mortality pressure 146
long-term inducible response 36, 41 multicomponent resistance index 123,
124
magnesium 94, 296 multiple pest screening 205
mass attack 48, 54, 55, 60, 256 multitrophic defence system 108
mass inoculation 42, 43, 53, 54, 58, multitrophic plant insect interaction
60, 251 122
mass screening 108 mycorrhizae 82, 100, 101
mechanical stress 39 myrcene 95, 123, 275
mechanical trait 138
mechanical wound 13, 14, 39, 43, natural enemies 5, 9, 16, 17, 80, 82,
58, 123 100, 101, 137, 143, 144, 146, 148,
318 KEYWORD INDEX
156, 179, 193, 207, 227, 244, palatability 154, 155, 157
253, 255, 256, 258, 292, 303, 305 parasitic fungi 155-157, 165
natural enemy-driven 146 parent host plant 153, 156
necrosis 38, 140, 273, 274 parental species 153-157, 159, 302
necrotic response 139 pathogen 4, 12, 13, 31, 41, 42, 53, 55,
necrotic tissue 14, 140 57-62, 65, 82, 100, 122, 123, 132,
needle resin 18, 19 133, 138, 139, 144, 146, 148, 150
needle toughness 80, 88 pathogenic fungi 51, 53, 55, 57, 59,
nematode 138, 266, 271-275 60, 132, 258
neosynthesis 45 pathogenic fungus 13, 42, 55, 57, 59,
nitrogen 5, 9, 64, 80, 82, 83, 90, 60, 62
198, 227, 228, 245, 253-255, peptide 139
279, 295, 301 performance of the insect 14, 18
no-choice experiment 109, 114 pest biotype evolution 175, 181
non-outbreak population 48, 65 phasmid 79
nonpathogenic stimuli 138 phenol 33, 36, 39, 40, 44-47, 50-52,
non-target organism 195, 206 64, 125, 243, 275, 300
nutrient 5, 6, 12, 39, 46, 81-83, 90, phenolic 5, 6, 36, 38, 40
99, 139, 157, 190, 225, 227, 228, phenolic compound 38, 39, 64, 164,
246, 253, 254, 257, 293, 295 243, 251
nutrition 108, 138, 150, 279 phenolic glucoside 154, 155, 157, 164,
nutritional niche 83 198, 199, 202, 203, 205
nutritional status 81 phenolic secondary metabolite 154
nutritive quality 81, 89, 100, 101 phenological asynchrony 83, 100, 101,
242
oleoresin 35, 95, 133 phenological defence 116
oleoresin exudation pressure 35 phenological development 116
olfactory or gustatory stimuli 114 phenological resistance 117, 242, 295
ontogenetic 5, 81 phenological stage 108
ontogeny 8 phenology 4, 7, 8, 80, 83-86, 88, 108,
opportunity cost 8 116, 117, 124, 125, 157, 158, 242,
optimality 6 293, 295
outbreak population 48, 65, 66 phenotypic plasticity 14, 16
outer bark 33, 35, 132, 134, 278, phenotypic response 12, 225, 246
280, 281 pheromone 35, 37, 50, 56-60, 65
oviposition 4, 6, 10, 39, 52, 55, 81, phloem 16, 33-36, 38, 39, 45, 47, 50-
109-114, 116, 117, 119, 120, 52, 54-56, 58, 62, 63, 66, 105, 119,
123-125, 147, 155, 164, 197-199, 120, 124, 132, 141, 240, 241, 243,
206, 292 244, 248-251, 279
oviposition behavior 112 phloem colonization 50, 62
oviposition deterrency 119, 123 phloem parenchyma cell 33, 40, 43,
oviposition repellency 110 44, 243
oxidative 139 phloem reaction zone 40, 49, 52, 244
KEYWORD INDEX 319
phloem tissue 132, 222 population growth 19, 85, 92-94

phosphorus 82, 94, 296 population outbreak 269
photoperiod 106 population strategy 56, 108
physical factor 4, 7, 133, 134, 198 positive feedback loop 82
physiological condition 132, 133 potassium 94
physiological process 50, 274 powderpost beetle 132
phytoalexin 139 precursory compound 32
phytocentric hypotheses 12 preference 4, 11, 100, 112, 114, 137,
phytopathogenic fungi 31, 57 138, 157, 164, 176, 197-199, 243,
phytophagous insect 36, 198 304
pinene 95, 123, 244, 275 preference test 156-161, 165
pinocembrin 46, 248, 250, 275 preformed 32, 34
pinosylvin 45, 46, 248, 250, 275 preformed defense 32, 36
pinosylvine methyl transferase 45 preformed induced defense 32-34, 37
pioneer beetle 57 preformed resin 34, 35, 37, 38
plant apparency 6, 113 preformed resistance mechanism 32
plant breeding 2 preformed response 48
plant form 132 prenyltransferases 121
plant gall 140 primary metabolite 4, 5, 81, 90
plant genotype 2, 9, 18 primary resistance 133
plant nutrition 138, 146, 150 progeny trial 107
plant pathologist 138 protein 8, 12, 81, 90, 139, 154, 268,
plant phenology 8, 80, 116 296
plant phenotype 3 proteinase inhibitor 195, 199, 200,
plant quality hypothesis 253, 254 201, 208
plant trait 2-4, 6, 9,, 11, 13, 15-19, pure individual 153
82, 155, 164
plant/insect interaction 2, 11, 14 radial growth 86, 87, 118, 257
plantation strategies 191 rapid aggregation 50
plant-driven 144, 146 rapid induced resistance 14
plasmodesmata 39 rapid induced response 12
plastic response 14 rapid tree response 47
pollinator 9 ray parenchyma cell 39
polygenetic resistance 111 reaction mechanism 38
polymorphism 9, 10 reaction tissue 46
polyphenolic compound 3, 139 reaction zone 39-41, 45-47, 51, 52,
polyphenolic parenchyma cell 13, 244, 258, 250, 255
35, 36, 251 reductive 139
polyphenolic resin 133 refugia 179-182, 202, 208
polyphenolic substance 141 repellency 110, 114, 123-125
population dynamics 12, 15, 18, 19, repellent 35, 46, 106, 108, 113, 125,
31, 38, 43, 93, 95-97, 224, 227, 154, 155, 274-276
229, 258
320 KEYWORD INDEX
resin 33-35, 38-40, 43, 46, 48, 50, 205, 208, 240, 244, 245, 247, 277,
55, 57, 59-61, 108, 109, 115, 278, 281, 298, 305
116, 120, 122, 124, 125, 133, resistance of conifers to bark beetles
226, 243, 244, 248, 255, 279, 31, 38, 65, 66, 243
280, 293 resistance trait 3, 4, 6, 7, 9, 11, 12, 14-
resin acid 18, 19, 33, 45, 120, 123, 19, 81, 82, 159, 165, 169, 172, 180,
254 208, 224, 229
resin canal 107, 109, 114, 115, 117- resistance, genetically determined 4,
125, 276 243, 249
resin crystallization 35 resistance-screening program 106, 177
resin duct 13, 33-35, 37, 39, 41-45, resistant 1, 2, 4, 8, 12, 15, 16, 36, 42,
48, 49, 56, 58, 59, 123, 243-245, 56, 59, 80, 82-101, 109, 112-124,
274, 277, 279, 280 139, 146, 149, 154-156, 160, 161,
resin flow 33-35, 37, 38, 40, 44-50, 174, 176, 179-181, 183, 189, 192,
52, 58, 59, 122, 228, 254, 255, 193, 196, 202, 204-206, 217-220,
277, 279, 281 222, 224, 226, 228, 229, 243, 244,
resin impregnated zone 55, 62 246-249, 251, 252, 255, 265, 266,
resin network 34 268, 269-281, 287, 292-306
resin pocket 35, 58 resistant genotype 10, 110
resin system 33 resistant plant 1, 2, 4, 9, 14, 16
resin translocation 37 resource availability 6
resistance 1-5, 7-18, 20, 31, 32, 34- rust fungi 155, 165
36, 42-45, 47, 48, 50, 51, 53-59,
61, 62, 65-68, 79-84, 87-89, 96, sapwood 33, 34, 38, 41, 51, 53-56, 58,
99, 100, 106, 107, 109-112, 114, 61-63, 244, 251, 278, 280
115, 117-119, 123-125, 133, 134, sapwood invasion 53, 58, 63
137-140, 143, 144, 146, 149, sapwood occlusion 50, 53-55, 63
150, 153-155, 158, 159, 162, sawflies 79-81, 154-156, 158, 164,
165, 169-183, 189, 190, 192- 203, 228
196, 199-206, 208, 217-220, 223- screening for resistance 107, 175, 219
229, 239, 240, 242-258, 265, scribble-barked gums 132
268-274, 276-281, 287, 292-305 secondarily invading scavenger 133
resistance against insects 1, 7, 13, secondary chemistry 133, 138, 153,
14, 18, 66, 67, 105, 122, 137 154
resistance gene 12, 14, 199, 254, secondary compound 6, 11, 146, 154,
269, 271 155, 164, 175, 198, 274, 275, 295
resistance gene pool 107 secondary metabolite 4-7, 9, 11, 17,
resistance mechanism 2, 3, 9, 11, 19, 33, 47, 48, 51, 52, 57, 64, 66,
31, 32, 38, 41, 64-68, 79, 81, 83, 81, 122, 164, 224, 225, 227, 228,
84, 88, 95, 99, 105, 108, 109, 248
114, 115, 118, 124, 125, 133, secondary reaction 38
134, 138, 144, 146, 171, 172, secretory cell 32, 33
174-176, 178-183, 189, 195, 204, secretory structure 32
KEYWORD INDEX 321
selection pressure 118, 165, 252 stressed plant 16, 229, 253
selective pressure 66, 153, 172, stressed tree 16, 134, 225-227, 229,
175, 178-181, 208 256, 292
sesquiterpene 52 structural constitutive defence 109
sesquiterpenoid 122 sub-lethal effect 4, 16
shoot growth 84, 116, 255 successful colonization 31
shoot infesting insect 105, 124 sugar 38, 45, 82, 83, 92-95, 226, 254
short term response 36 survival 4, 5, 7, 9, 10, 16, 18, 19, 81,
short-rotation woody crop 190, 191 83-85, 90, 95, 133, 134, 137, 138,
short-term inducible response 36 157, 165, 195, 202, 223-225, 228,
sieve cell 35, 39 243, 298, 303
signal compound 12 susceptible 31, 36, 42, 51, 68, 83-96,
simultaneous attack 50, 56 98, 100, 109, 119, 120, 134, 149,
sink/source regulation 6 165, 178, 190, 192, 204-206, 224-
Sitka spruce 33, 106, 107, 109, 111, 227, 229, 246, 249, 251, 252, 255,
113-116, 118-120, 122, 124 256, 265, 266, 271, 273, 275, 277,
slow growth-high mortality 16 293, 294, 296-299, 301-305
solitary strategy 59 susceptible genotype 10, 114, 249, 300
soluble phenol 33, 36 susceptible plant 4, 16, 112, 149
spatial distribution 112 synchrony 8, 79, 86, 117, 125
specialist 6, 15, 132, 153-156, 176, synergistic interaction 11
302 synthetic hypothesis 38
specialized insect 9, 17, 176 synthetic pathway 45
spore 52, 61, 63, 65 systemic 12, 138, 240, 245, 279
spruce budworm 80-101, 105, 116, systemic induced defense 245
180 systemic induction of resistance 43
staining fungi 53 systemic resistance 138
starch 254, 257
starvation 80, 114 tannin 6, 8, 154, 155, 159, 164, 202,
stem gall 142 249, 254, 257, 288, 295, 300, 302
stilbene aglycons 46 temperature 67, 106, 112, 206, 246,
stilbene syntase 45, 52, 270, 275 304
stimulation 37, 44, 45, 51, 52, 55, temporal variation 112
58, 62, 63, 80, 245 temporal window 9
stone cell mass 33, 59 terpene 35, 38-40, 44-47, 51, 52, 55,
stress effects on insect resistance 64, 83, 95, 96, 98, 109, 113, 114,
226 123, 228, 243, 244, 249, 255, 273,
stress experiment 16 274
stress hypothesis 16, 225 terpene synthase 45, 121
stress response 16 terpenoid 5, 6, 18, 121-125, 133
stress, abiotic 19, 171, 172, 224 terpenoid synthase gene 123
stress, biotic 19, 171, 172, 224 thick bark 3
stressed host plant 132 third trophic level 17, 258
322 KEYWORD INDEX
thorn 107 tree defense strategies 49

three-trophic-level interaction 82, tree genetic factor 64
83, 100, 101 tree killing 183
threshold of attack density 50, 51, tree phenology 108, 116
56, 61-63, 65, 66, 251 tree recovery 80
threshold response 154 tree resistance 1, 2, 16, 20, 32, 34, 35,
timber beetle 132 38, 43, 45, 47, 50, 51, 53-59, 61, 64-
timber worm 132 68, 80, 82, 88, 111, 131, 134, 169-
tip moth 131, 228 171, 176, 178, 189, 190, 226-229,
tissue restoration 42-44 239, 240, 245-249, 251, 253, 254,
tolerance 2, 3, 6, 57, 59, 80, 86, 256-258, 265, 270, 272, 277, 290,
100, 101, 134, 137, 171, 172, 281, 300
174, 178, 208, 225, 266, 268, tree response 36, 43, 44, 47-49, 52, 56,
276, 292, 295, 298, 299, 302 248, 250
tough leaves 7, 80 tree strategy 48
tough needle 80, 101 tree vigor 80, 86, 100, 225, 228, 229,
toughness 7, 9, 80, 81, 88, 89, 100, 251, 254, 255, 258, 306
101, 292 tree/insect interaction 18, 82, 100
toxic 35, 46, 47, 108, 122, 124, trichome 3, 7, 9, 107
195, 200, 202, 244, 268 tri-trophic interaction 18, 82, 100
toxic chemical 3, 5, 202 tri-trophic level effect 16
toxic effect 154, 243 trophic relationship 116
toxic metabolite 139 tropical forestry plantation species 294
toxicity 46, 110, 115, 119, 125, tunnelling insect 58
194, 200, 202 tussock moth 79, 277
toxin 2, 50, 54, 63, 81, 195, 200- twig borer 131, 203, 277
202, 206, 252, 266, 268, 275
trade-off 8, 9 undifferentiated tissue 7
transduction 139, 270 unsuitable food 137
transformation technique 14
transformed woody plant 14 vapor 46, 48
transgenic Bt 200, 201 vertical galleries 34, 49, 57
transgenic poplar 266, 268 vertical resin duct 49, 255
transgenic tree 14, 195, 201, 219, vigor gradient 57
252 virulence gene 12
translocation 37, 39 virus 138
transversal galleries 58 volatile 17, 18, 108
traumatic resin 108, 109, 114, 115, volatile chemical 134
117, 120-124, 279, 281 volatile compound 17
traumatic resin duct 13, 41-45, 48, volatile induction 17, 18
56, 59, 244, 245, 277, 279-281 volatile terpenoid 122, 123
traumatic resinosis response 121
tree death 50, 52-55, 58, 59, 63 walking stick 79
KEYWORD INDEX 323
water stress 64, 134, 226, 227, 250,

255
water stressed tree 134, 226
weevil 105-115, 117-121, 124, 125,
132, 206, 222, 226, 228, 240,
243, 297, 305
western spruce budworm 82-85, 87-
101
white pine weevil 105-109, 115,
117, 119—121, 124, 125, 226,
228
white spruce 43, 80, 106, 107, 111,
113, 117-120
willow 7, 10, 17, 153-158, 164,
165, 174, 182, 192, 193, 265
winding galleries 49, 58
window of susceptibility 80, 124
within-plant resistance 112
within-plant variation 112
wood boring life history strategies
131
wood wasp 131, 133
wood-boring insect 131, 132, 266
wound periderm 40-44, 274
wound reaction 39, 40, 42, 44
wound response 44, 109
wounding 13, 14, 33, 36, 37, 39, 40,
42-44, 47, 51, 52, 58, 62, 108,
120-122, 244
xylem resin canal 117, 120-123

xylem tissue 132
xylophagous insect 49, 245
young larvae 105, 109, 117, 124,

277, 280, 281
zinc 94
Species Index
Abies 35,43,58, 119 Batocera horsfieldi 265, 268, 269

Abies concolor 35 Batocera lineolata 265, 268
Acacia 182, 88, 289, 299, 306 Bauhinia brevipes Vog. 138, 140, 141,
Acacia crassicarpa 299 142, 144, 147, 149
Acacia mangium 298, 299 Betula 157, 164, 220
Acacia mearnsii 288 Betula pubescens 13
Acacia Senegal 288 Betula maximowiczinana 223, 224
Acacia spp. 220 Betula nigra 223, 224
Acer 220 Betula papyrifera 223, 224
Acer freemanii 220 Betula pendula 222, 223, 233
Acer rubrum 220 Betula platyphylla 224
Acer saccharum 226 Betula platyphylla var. japonica 223
Adelges abietis 241, 242, 245 Betula platyphylla var. szechuanica
Adelges laricis 251 223
Adelges picae Ratzeburg 41 Betula populifolia 224
Adelges piceae 183 Betula populifolia Whitepire 223
Adelges tsugae 183 Betula pubescens 223
Agonoxenidae 131 Betula spp. 222
Agrilus anxius 220, 222 Bignoniacaea 143
Agrilus sexsignatus 298 Bostrichidae 132
Agrobacterium 252 Bowdichia virgilioidis 143, 144
Agrobacterium tumefaciens 201, 268, Brachyderes incanus 241
298 Brentidae 132
Alsophilia pometaria 221 Bupalus piniarus 13, 258
Anaglyptus subfasciatus 277 Buprestidae 132
Anisota senatoria 221 Bursaphelenchus xylophilus 266, 271
Annona coriaceae 143 Byrsonima verbascifolia 143, 144
Annonaceae 143
Anobiidae 132 Cupressus arizonica 299
Anoplognathus porosus 302 Cupressus funebris 299
Apocheimia cinerarius 265 Cupressus. torulosa 299
Apochina cinerarius 268 Calliteara argentata 277
Apocynaceae 143 Casuarina 288
Apriona japonica 265, 299 Cecidomyiidae 138, 141-144, 156,
Arabidopsis thaliana 14 277
Argyresthia cupresssella 221, 222 Cedrela odorata L. 294, 295
Argyresthiidae 131 Cedrus 35, 119
Aspidosperma tomentosum 143 Cedrus atlantica 67
Asteraceae 143 Cephalcia abietis 241
Atta sexdens rubropilosa 304 Cephidae 131
Australes 270 Cerambycidae 132-134, 277, 296
Ceratocystis polonica 244, 249, 250,
Baccharis dracunculifolia 143 251
Bacillus thuringensis 195, 252, 304 Chaitophorus poplicola 226
325
326 SPECIES INDEX
Choristoneura 79 Dalbergia sisso 288

Choristoneura conflictana 202 Danaidae 195
Choristoneura fumiferana 80 Danaus plexippus L. 195
Choristoneura fumiferana Clem. Dasineura marginemtorquens 10
180 Dasineura rosaria 158, 165
Choristoneura occidentalis 82 Davilla regusa 143
Choristoneura spp. 105, 116 Dendroctonus brevicomis 57
Chrysomela populi 200 Dendroctonus frontalis 34, 49, 53, 58,
Chrysomela scripta F. 193, 194, 183
195, 196, 197, 198, 199, 200, 201, Dendroctonus micans 33, 34, 49, 50,
203, 205-207 53, 59, 60
Chrysomelidae 156-158, 193, 200 Dendroctonus pondorosae 35, 44, 49,
Cinara cupressi 294, 299 50, 53, 57
Clethrionomys rufocanus 266, 272 Dendroctonus punctatus 53, 59, 60
Cocos 288 Dendroctonus terebrans 60
Coffea arabica 304 Dendroctonus valens 60
Coffea robusta 304 Diaphnocoris chlorionis 221
Coleoptera 79, 105, 131, 133, 134, Dilleniaceae 143
141, 142, 157, 193, 200, 277, 296, Dioryctria 296
298, 299, 302 Dioryctria spp. 296
Combretaceae 143, 144 Dioryctria sylvestrella 241, 243, 249,
Contarinia 144, 147, 149 250
Contarinia sp. 138, 141, 142 Diprion pini 241, 243, 244, 245, 247,
Contortae 271 249, 250
Coptotermes curvignathus 299 Diprionidae 79
Cornus 220 Diptera 79, 131, 144, 148, 141, 142,
Cornus florida 227 277
Corythucha cydoniae 220, 221 Dothideales 204
Cossidae 131
Cotoneaster 220 Elatobium abietinum 242, 243, 251
Crepidodera fulvicornis Fabr. 156, Empoasca fabae 220
158 Epinotia granitalis 277
Cronartium quercuum Berk. 177 Epinotia tedella 256
Cronartium rubicola 43 Epirrita autumnata 13
Cryphonectria cubensis 183 Eucallipterus tilliae 222
Cryptococcus fagisuga 242, 257 Eucaluptus camaldulensis 297, 298
Cryptomeria japonica 266, 277 Eucaluptus deglupta 298
Cupressocyparis leylandii 299 Eucaluptus grandis x E. urophylla
Cupressus 306 298, 299, 303
Cupressus lusinatica 294, 299 Eucalyptus 133, 134, 181-183, 190,
Curculionidae l41, 142, 297 227, 287-289, 297, 306
Cylindrocopturus 105 Eucalyptus amygdalina 302
Eucalyptus blaklyi 7
SPECIES INDEX 327
Eucalyptus grandis 298, 302, 303 Hymenoptera 131, 156, 207

Eucalyptus haemastoma 132 Hypsipyla 294, 295, 306
Eucalyptus japonicus 277 Hypsipyla grandella Zeller 294
Eucalyptus risdonii 302 Hypsipyla robusta Moore 294
Eucalyptus tereticornus 297
Eucalyptus urophylla 298, 302 Ilex spp. 221
Eucosma tedella 241 Imperata cylindrica 299
Euonymus spp. 221 Ips 35, 49
Eurosta 140 Ips acuminatus 33, 57, 60, 241
Eutectona machaeralis 296 Ips cembrae 62
Ips pini 47
Fagus sylvatica 144, 239, 241, 257 Ips sexdentatus 44, 69, 62, 241
Fraxinus pennsylvanica 227 Ips typographus 35, 42, 49, 54, 57,
60-62, 240, 241, 244, 246, 249
Galerucella lineola 154 Isoptera 299
Galerucinae 157 Iteomyia capreae 158
Gaylussacia 182
Gelechiidae 131 Juniperus spp. 221
Geometridae 141, 297
Gilpinia hercyniae 241,256 Khaya ivorensis 294
Gleditsia triacanthos 221 Khaya myasica 294
Gmelina arborea 288, 289 Khaya senegalensis 294
Goniptera scutellanus 297 Khaya spp. 294
Graellsia isabellae 244, 247
Gympsonoma hiambachiana 203, Larix 3, 57, 119, 243
204 Larix decidua 245, 252
Larix eurolepsis (Larix decidua x
Halticinae 156, 158 Larix leptolepsis) 276
Hamameliste spinosus 220 Larix gmelini var. japonica 276
Hartigiola anulipes Htg. 144 Larix gmelini var. japonica x
Heliothis 11 L.leptolepsis 276
Helopeltis spp. 299 Larix leptolepsis 276
Hempitera 299 Larix occidentalis 34
Hepialidae 131, 132 Larix spp. 265
Heteropsylla cubana 301 Lasiocampidae 202
Heteropsylla cubana Crawford 294 Leguminosae 138, 143, 144
Hevea 288 Lepidoptera 79, 131, 132, 141, 142,
Hevea braziliensis 304 193, 195, 202, 203, 277, 296, 297
Homadaula anisocentra 221 Leptographium 57
Homoptera 294, 301 Leptographium wingfieldii 52, 57, 58,
Hyadaphis tataricae 221 60, 61, 63, 248, 250, 251
Hyblaea puera 295, 296 Leptographium yunnanesis 57
Hylobius abietis 241, 243, 249, 250 Leucaena 301, 306
328 SPECIES INDEX
Leucaena collinsii 301 Miridae 299

Leucaena diversifolia 301, 302 Momphidae 131
Leucaena leucocephala 294, 301, Monochamus alternartus 270
302 Morus alba 226
Leucaena leucophala x L.
diversifolia 301 Naupactus lar 141, 142
Leucaena pallida 302 Neodiprion sertifer 241
Leucopholis irrorata 298 Neodiprion autumnalis 81
Liquidambar 182, 190 Neodiprion fulviceps 80
Liquidambar styraciflua 219 Neodiprion sertifer 18, 19
Lochmaea caprea 154, 157, 164 Neodipron 79
Lochmaea caprea L. 157 Neophasia menapia 79
Lochmeae 157 Nepticulidae 131
Loganiaceae 143 Nicotiana attenuata 17
Lonicera spp. 221 Noctuidae 131, 296
Lyctidae 132
Lygaeonematus abietinus 242 Ochniceae 143, 144
Lymantria dispar 79, 193, 202, 203, Oocarpae 270
219-222, 240, 241, 244, 265, 268 Ophiostoma 46, 53, 64
Lymantria monacha 241, 242, 254, Ophiostoma brunneo-ciliatum 60, 61
257 Ophiostoma ips 60
Lymexylidae 79, 132, 193 Ophiostoma novo-ulmi 183
Ophiostoma polonica (cum) 42
Magdalis 105 Ophiostoma polonicum 51, 60, 61,
Malacasoma americanum 221 255
Malacasoma disstria Hübner 202, Ormograptis scribula 132
203, 205 Orseolia oryzae 140
Malpighiaceae 143, 144 Orthoptera 79
Malus spp. 221 Otiorhynchus sulcatus 222
Matsucoccus feytaudi Duc. 240 Ouratea floribunda 143, 144
Matsucoccus feytaudii 242, 243
Melampsora 204, 208 P. euramericana 267
Melampsora spp. 174 P. hondurensis 296
Melampsora larici-populina 248 P. pyrameidalis x P. cathayana 267
Melampsora medusae Thuem. 204 P. simonii x (P. pyramidalis + Salix
Melampsoraceae 204 matsudana) 267
Melamspora sp. 155, 156-159, 163, P. simoniix P. nigra 267
165 P. simoniix P. nigra var. italica 267
Melasoma populi 252 P. tomentosa var. henan 267
Melicia regia 300 P. tomentosa var. jiangan 267
Mikolia fagi Htg. 144 P. tomentosa var. jieye 267
Milicia 300, 301, 305 P. tomentosa var. jinxi 267
Milicia excelsa 300 P. tomentosa var. taxin 267
SPECIES INDEX 329
P. tomentosa var. xiaoye 267 Pinus contorta 35, 44, 47, 50, 246,
P. tomentosa var. yixian 267 249, 272
P. virginiana 270 Pinus densiflora 266, 270, 271, 276
P. yunnanenis 49 Pinus densiflora 272, 274, 275, 276
Pailga machoeralis 296 Pinus edulis 82
Panthomorus sp. 141, 142 Pinus eliotti 251, 272
Paraserianthes falcataria 288 Pinus engelmannii 272
Paropsis atomaria 7 Pinus engelmannii Parry ex. Engelm.
Paulownia 182 107
Phasmida 79 Pinus exelsa 272
Phellinus weirii 43 Pinus greggii 272
Phoracantha semipunctata 296 Pinus khasya 272
Phoracantha semipunctata F. 133, Pinus koraiensii 272
134 Pinus leiophylla 272
Phratora vitellinae 17, 155 Pinus massoniana 272
Phratora vulgatissima 154, 193 Pinus merkusii 296, 304
Phyllaphis fagi 242 Pinus michoacana 272
Phyllocolpa 156 Pinus monticola 43, 272
Phyllotachys 182 Pinus mugo 273
Phylloxera vastatrix 140 Pinus muricata 272
Phytolyma lata 300, 305 Pinus nigra 273
Picea 33, 57, 119, 243 Pinus oocarpa 272
Picea abies 13, 33, 34, 35, 36, 42, Pinus palustris 272
239-241, 244, 245, 248, 249, 250, Pinus patula 288, 296
251, 254, 255, 256, 257 Pinus pentaphylla 272
Picea abies L. Karst 120 Pinus pinaster 240, 241, 243, 249,
Picea glauca 43, 80, 106 250, 273
Picea sitchensis 106, 243, 251 Pinus pondorosae 80, 249, 270
Picea spp. 105 Pinus pseudostrobus 272
Pieridae 79 Pinus radiatus 272
Pinus 5, 33, 57, 190, 243, 288, 289, Pinus radii D. Don 181
304 Pinus resinosa 47, 272
Pinus nigra var. therestig x P. Pinus rigida 266, 270, 272
simonii 267 Pinus rigida x P. taeda 266
Pinus nigra x P. maximowiczii 203 Pinus rigi-taeda 266
Pinus spp. 105 Pinus rudis 272
Pinus banksiana 47, 228, 272 Pinus spp. 250, 265
Pinus bungeana 272 Pinus strobes 272, 275
Pinus caribaea 296, 298, 301 Pinus strobiformis 272
Pinus caribaea subsp. Hondurensis Pinus strobus L. 106
296 Pinus sylvestris 5, 19, 35, 38, 44, 54,
Pinus caribaea var. bahamensis 296 228, 239-241, 243, 245, 248-250,
254, 255, 257, 273
330 SPECIES INDEX
Pinus tabulaeformis 272 Populus deltoides x P. maximowiczii

Pinus taeda 37, 53, 58, 226, 266, 203
272, 274 Populus deltoides x P. nigra 197
Pinus taeda L. 180 Populus deltoides x P. nigra 198, 200,
Pinus taiwanensis 272 203
Pinus thunbergii 266, 270, 271 Populus tremula x P. tremuloides 198,
Pinus thunbergii 272, 274, 275 200
Pinus thunbergii x P. densiflora 276 Populus tremuloides 174, 182, 198,
Pinus thunbergii x P. massoniana 226
275 Populus trichocarpa 197
Pinus yunnanensis 272 Pristiphora abietina 241, 251
Pinus. thunbergii x P. masoniana Prosapia bicincta 221
266 Pseudaulacaspis pentagona 225
Pissodes 105 Pseudoacacia 182
Pissodes harcynae 241 Pseudotsuga 33, 119
Pissodes notatus 241 Pseudotsuga menziesii 43, 67, 293,
Pissodes strobi 43, 109, 111, 113, 304
114, 115, 117-119, 120, 124, 226, Pseudotsuga menziesii var. glauca 82
245 Psylla uncaitoides 220
Pissodes strobi Peck 105 Psyllidae 294, 301
Pissodes strobus 226 Pteromalidae 207
Pityogenes chalcographus 32 Pterophoridae 131
Plagiodera versicolora 155, 226 Pulvinaria regalis 225
Plagiodera versicolora Laicharting Pyracantha spp. 221
200 Pyralidae 131, 296
Platanus 190 Pyrrhalta luteola 222
Platypodidae 132
Pondorosae 20 Quercus alba 226
Pontania 156 Quercus cerris 244
Pontania bridgmanii 158, 164, 165 Quercus ilex 240
Pontania pedunculi 158, 164 Quercus petraea 239, 240, 244, 249
Popillia japonica 220-222 Quercus pubescens 240
Populus 157, 164, 182, 189, 190, Quercus robur 239, 240
193-207, 219 Quercus spp. 221, 241
Populus deltoides 197, 198, 203, Quercus suber 240
226
Populus nigra 252, 268 Reeseliella odai 277, 278
Populus alba 197, 200 Rhinotermitidae 299
Populus alba x P. grandidentata 199 Rhizophora 182
Populus alba x P. grandulosa 266 Rhodondendron spp. 221, 222
Populus deltoides 203, 267, 268 Rhyacionia 246, 296
Populus deltoides x P. deltoides 203 Rhyacionia buoliana 241, 249, 250
Rhyacionia frustrana 228
SPECIES INDEX 331
Rhynchaenus fagi 241 Stephanotis pyrioides 221

Rhyscionia buoliana Schiff. 105 Strepsicrates rothia 297
Rhytisma salicinum 165 Strichnos pseudoquina 143
Rosa spp. 222 Swietenia 288
Rubus bogotensis 9 Swietenia macrophylla 289, 304
Swietenia macrophylla var. Jacq.
Sacchiphantes abietis 256 289, 295
Salix 157, 164, 182, 190, 197, 205 Sylvestris 270
Salix aurita 154, 156, 157, 158, 164 Synanthedon scitula 220, 277
Salix caprea 154, 156-158, 163-165
Salix caprea x Salix aurita 159 Tabebuia ochracaea 143
Salix caprea x Salix repens 159 Taphrorychus bicolor 241
Salix cinera 164 Tectonia grandis 288, 289, 295, 304
Salix dasyclados 155, 193 Tenthredinidae 131, 156, 242
Salix eriocephala 155, 164 Terminalia brasiliensis 143, 144
Salix gracilistyla 198 Terminalia ivorensis 288
Salix pentandra 154 Terminalia superba 288
Salix phylicifolia 156, 157, 164, 165 Thaumetopoea pinivora 241
Salix purpurea 193 Thaumetopoea pityocampa 68
Salix repens 154, 156-159, 163-165 Thaumetopoea pityocampa 68, 240,
Salix repens Sm. L. 156 241, 244, 247
Salix sericea 155, 164 Thaumetopoea processionea 241
Salix spp. 156, 174, 265 Thecodiplosis japonensis 266, 269.
Salix tiandra 154 270
Salix viminalis 10, 154, 155 Thecodiplosis japonicus 266
Sapindaceae 143, 144 Theobroma cacao 304
Scarabaeidae 302 Thuja spp. 222, 299
Scarabidae 298 Thyrididae 131
Schizonatus latus Walker 207 Thyridopteryx ephemeraeformis 221
Sciopithis obscurus 222 Thyrinteina arnobia 297
Scolytidae 132, 299 Tilia spp. 222
Scolytus intricatus 241 Tomicus 35
Scolytus ventralis 35, 49, 58 Tomicus minor 49
Semanotus japonicus 277, 278, 279, Tomicus piniperda 38, 44, 49, 52-55,
280 57, 58, 60-63, 67, 241, 246, 248,
Septoria 204, 208 256, 257
Septoria musiva Peck 204 Toona ciliata 294
Serjania lethalis 143, 144 Tortricidae 131, 202, 203, 297
Sesiidae 131 Tortrix viridana 240, 241, 242, 246,
Siricidae 131 258
Solidago altissima 140 Totricidae 277, 296
Sphaerioidaceae 204 Totricidae 79
Spodoptera litura 296 Tsuga 35
332 SPECIES INDEX
Ulmus 182
Ulmus americana L. 183
Ulmus spp. 222
Unaspis euonymi 221
Uredinales 204
Vaccimium angustifolium 174

Vaccinium 182
Vatairea macrocarpa 143
Xiphydriidae 131
Xyleborus spp. 299
Xylosandrus 299
Yponomeutidae 132
Zeiraphera canadensis 116

Zeiraphera diniana 245

Mechanisms and Deployment of Resistance in Trees To Insects

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Mechanisms and Deployment of Resistance in Trees to Insects

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KLUWER ACADEMIC PUBLISHERS

©2002 Kluwer Academic Publishers

Print ©2002 Kluwer Academic Publishers

All rights reserved

Created in the United States of America

Visit Kluwer Online at: http://kluweronline.com

Chapter 1 Resistance in trees to insects – An overview of mechanisms and

Chapter 2 Mechanisms of resistance in conifers and bark beetle attack

Chapter 3 Mechanisms of resistance in trees to defoliators 79

Chapter 4 Mechanisms of resistance in conifers against shoot infesting

Chapter 5 Host tree resistance to wood-boring insects 131

Chapter 6 Plant resistance against gall-forming insects: the role of

Chapter 7 The resistance of hybrid willows to specialist and generalist

Chapter 8 Deploying pest resistance in genetically-limited forest

Chapter 9 Deployment of tree resistance to insects in short-rotation

Chapter 10 Strategies for Deployment of Insect Resistant Ornamental

Chapter 11 Possibilities to utilize tree resistance to insects in forest pest

Chapter 12 Deployment of tree resistance to pests in Asia 265

Chapter 13 Using resistance in tropical forest plantations ... 287

Keyword Index 311

This book is the result of an international symposium that was held in

The authors gratefully acknowledge the generous support of Northern

RESISTANCE IN TREES TO INSECTS – AN

Department of Entomology, Swedish University of Agricultural Sciences, Box 7044,SE-750 07

last two decades have seen an impressive development of conceptual models on

2. CONCEPTS AND DEFINITIONS

3.1 PRIMARY METABOLITES

3.2. SECONDARY METABOLITES

Secondary metabolites can be constitutive, i.e. always present in the plant, or

3.3. PHYSICAL FACTORS

3.5. THE IMPORTANCE OF TRADE-OFFS IN DETERMINING LEVEL OF

idiosyncracies and that it will be difficult, if possible at all, to formulate universal

6. ENVIRONMENTAL MODIFICATIONS OF RESISTANCE

7. RESISTANCE IN THE CONTEXT OF COMPLEX INTERACTIONS

modifier of insect-caused plant damage in a particular environment will be difficult

8. RESISTANCE AND INSECT POPULATION DYNAMICS

a multitude of approaches, including long-term monitoring of plant and insect,

MECHANISMS OF RESISTANCE IN CONIFERS

2. LEVELS OF TREE RESISTANCE

2.1 PREFORMED DEFENSES

2.1.1. Constitutive defense

Nevertheless, although absolutely passive, this constitutive defense may influence

2.1.2. Preformed induced defense

the already existing rows, by differentiation of axial parenchyma cells or by division

2.2. INDUCED DEFENSES

2.2.1. Induced resin flow

2.2.2. Hypersensitive reaction

The hypersensitive reaction is completed by the formation of a wound periderm

2.2.3. Delayed resistance

Nonetheless, wound periderm is worth mentioning because it may contribute to

The phenomenon of induced protection has been recently discovered and

3. MECHANISMS OF INDUCED DEFENSE

3.1.1. Induction by mechanical wounding

3.1.2. Non specificity of tree responses

3.1.3. Role of phloem parenchyma cells

3.2. BIOCHEMICAL CHARACTERISTICS OF THE RESPONSE

3.3. ORIGIN OF THE ENERGETIC COMPOUNDS USED IN THE INDUCED

3.4. MODE OF ACTION UPON THE AGGRESSORS

4. ROLE OF THE DEFENSE SYSTEMS

1995a,b). Histological changes in the PP cells were considerable at 12 days

4.2. RELATIVE ROLE OF THE PREFORMED AND INDUCED DEFENSES: A