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The selection, testing and application of terrestrial insects as bioindicators

MELODIE A. McGEOCH

Biological Reviews of the Cambridge Philosophical Society / Volume 73 / Issue 02 / May 1998, pp 181 - 201
DOI: null, Published online: 08 September 2000

Link to this article: http://journals.cambridge.org/abstract_S000632319700515X

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MELODIE A. McGEOCH (1998). The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews
of the Cambridge Philosophical Society, 73, pp 181-201

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Biol. Rev. (1998), 73, pp. 181–201 Printed in the United Kingdom # Cambridge Philosophical Society 181

The selection, testing and application of

terrestrial insects as bioindicators
MELODIE A. McGEOCH
Department of Zoology & Entomology, University of Pretoria, Pretoria 0002, South Africa

(Received 4 September 1996 ; revised 3 November 1997 ; accepted 4 November 1997)

ABSTRACT

Although the uses and merits of terrestrial insects as indicators have been extensively discussed, there is a lack
of clear definition, goal directedness and hypothesis testing in studies in the field. In an attempt to redress
some of these issues and outline an approach for further studies, three categories of terrestrial insect
indicators, corresponding to differences in their application, are proposed, i.e. environmental, ecological and
biodiversity indicators. The procedures in terrestrial insect bioindicator studies should start with a clear
definition of the study objectives and proposed use of the bioindicator, as well as with a consideration of the
scale at which the study is to be carried out. Bioindication studies are conducted at a variety of spatial and
temporal scales within the context of earth-system processes, but the objectives of the study will largely
determine the scale at which it would be optimally conducted. There is a tendency for studies to be
conducted below their space-time scaling functions, giving them apparent predictability. The selection of
potential indicator taxa or groups is then based on a priori suitability criteria, the identification of predictive
relationships between the indicator and environmental variables and, most importantly, the development
and testing of hypotheses according to the correlative patterns found. Finally, recommendations for the use
of the indicator in monitoring should be made. Although advocating rigorous, long-term protocols to identify
indicators may presently be questionable in the face of the urgency with which conservation decisions have
to be made, this approach is critical if bioindicators are to be used with any measurable degree of confidence.

Key words : bioindicators, biodiversity indicators, environmental indicators, ecological indicators, monitoring,
terrestrial insects.

CONTENTS

I. Introduction.............................................................................................................................. 182
II. Definitions................................................................................................................................. 183
(1) Environmental indicators ................................................................................................... 183
(2) Ecological indicators .......................................................................................................... 183
(3) Biodiversity indicators ........................................................................................................ 184
(4) Definition : biological indicator .......................................................................................... 185
(5) Monitoring ......................................................................................................................... 185
III. The objectives of terrestrial insect bioindicator studies............................................................. 186
(1) Environmental indicators ................................................................................................... 186
(2) Ecological indicators .......................................................................................................... 186
(3) Biodiversity indicators ........................................................................................................ 187
(4) Monitoring ......................................................................................................................... 188
IV. Methodology............................................................................................................................. 188
(1) Preliminary approach ........................................................................................................ 188
(2) Scale................................................................................................................................... 189
182 M. A. McGeoch

(3) Criteria for the selection of potential indicator species ...................................................... 189
(a) General criteria............................................................................................................ 189
(b) Individual species and species groups as bioindicators ................................................ 193
(4) Data collection and interpretation ..................................................................................... 195
(5) Hypothesis testing .............................................................................................................. 195
(6) Status quo............................................................................................................................. 195
V. Conclusion – ‘ Catch-22 ’ ........................................................................................................... 197
VI. Acknowledgements.................................................................................................................... 197
VII. References................................................................................................................................. 197

I. INTRODUCTION taxa against this list of a priori selection criteria.

Insects constitute a substantial proportion of ter-
restrial species richness and biomass, and play a
significant role in ecosystem functioning. This re-
alisation has led to extensive discussion and evalu-
ation of the use of terrestrial insects as bioindicators,
and the concept has been applied to a variety of
taxa, habitats and environmental scenarios
(Holloway, 1980 ; Rosenberg, Danks & Lehmkuhl,
1986 ; Kremen et al., 1993). Studies have included
the use of single species, higher taxa, assemblages
and communities of, for example, dragonflies,
ground beetles, tiger beetles, moths, butterflies,
sawflies and ants, in habitats such as forests,
grasslands, sand dunes, soils, urban areas and mine-
sites.
In spite of the apparent wide range of terrestrial
insect indicator studies, little attention has been
given to the definition or implicit goals of ‘ bio-
indication ’ using terrestrial insects. The term is often
used loosely and has been adopted in a broad range
of contexts, including the indication of habitat
alteration, destruction, contamination and rehabili-
tation, vegetation succession, climate change and
species diversity (and even to non-conservation
related issues such as indicating past climates :
Coope, 1979 ; Coope & Lehmdahl, 1996).
Questions concerning the protocols that should be
used to identify indicator taxa and whether or not
they can be designated objectively have also been
raised (Stork & Samways, 1995). On more than one
occasion it has been suggested that the basis for
insect indicator selection is often merely favoured or
convenient taxa (Soule! & Kohm, 1989 ; Woiwod &
Thomas, 1993 ; Williams & Gaston, 1994). Nu-
merous authors have listed a priori criteria for the
selection of potentially effective insect indicator taxa
and many studies have applied these to justify the
suitability of particular taxa as indicators (e.g.
Holloway & Stork, 1991 ; Pearson & Cassola, 1992 ;
Pearson, 1994). However, there is little to be gained
from ‘ testing ’ the suitability of potential indicator
Guideline criteria merely minimize the chance from
the outset of spending time and energy studying
species that are unlikely to be successful candidates.
Whatever the criteria for selection used, once
identified as potentially suitable, taxa have seldom
been formally tested for indicator value, let alone
applied as such, and only very recently have more
rigorous studies begun to appear. There is thus an
imbalance between the considered ‘ potential value ’
and well-propounded a priori criteria for suitable
terrestrial insect indicator taxa, and the actual
testing and application of these taxa as indicators.
Bioindication is essentially a subdiscipline of
conservation biology, and its primary goal is,
therefore, the application of scientific knowledge to
the management of ecological relationships, i.e. to
maintain particular relationships between species
and their distributions and abundances (Caughley
& Gunn, 1996). Research is not conservation biology
if it has no practical implications for conservation
(Murphy, 1990, 1992) and, likewise, studies on the
relationships between terrestrial insects and biotic
and abiotic variables are not bioindication unless the
potential applications of these relationships are
elucidated. As a result of undefined endpoints to
indicator identification and selection (i.e. failure to
identify and elucidate the specific applied value of a
nominated indicator), there has often been a lack of
rigorous testing of hypotheses and of the implicit
assumptions made when a species, or group, of
terrestrial insects is selected as a bioindicator.
The use of bioindication in terrestrial systems,
particularly using invertebrate indicators, has only
gained momentum within the last two decades
(Holloway, 1980). Aquatic macroinvertebrates, how-
ever, have frequently been highly recommended as
indicators of water quality (Hellawell, 1986). The
recommendation and use of aquatic invertebrates in
both freshwater and marine systems dates back a
number of decades and the literature in this field is
extensive (see e.g. Hellawell, 1986 ; Rosenberg &
Resh, 1993). Although biological indicators have
Terrestrial insects as bioindicators
been used for far longer and far more extensively in
aquatic than in terrestrial systems, the significant
differences between aquatic and terrestrial eco-
systems to some extent divide the fields of aquatic
and terrestrial bioindication. Terrestrial systems
tend to be more complex (e.g. have greater species
richness) and variable, and terrestrial abiotic factors
(e.g. air pollution, humidity) are often more difficult
to quantify than aquatic abiotic ones (Steele, 1991).
Nevertheless the basic principles and methods used
in terrestrial bioindication have their origin in the
aquatic literature (e.g. Winner, Boesel & Farrell,
1980 ; Hellawell, 1986 ; Rosenberg & Resh, 1993 ;
Clarke & Warwick, 1994 ; Chessman, 1995).
Thus, although the definitions and problems
discussed here may have broader application, for
example to the use of other taxa as bioindicators (see
e.g. Landres, Verner & Thomas, 1988), and may in
some instances stem from aquatic bioindication
literature, I have sought to answer the following
questions in an attempt to redress the lack of
definition and direction in the field of terrestrial
insect bioindication : what is a bioindicator in the
context of terrestrial insect fauna, what are the
immediate and ultimate goals of the identification
and use of terrestrial insects as bioindicators, and
what steps are necessary for the rigorous advance-
ment of the field, i.e. the use of terrestrial insects in
bioindication ?
II. DEFINITIONS
The Oxford Dictionary of Zoology (Allaby, 1992)
defines an ‘ indicator species ’ as ‘ a species that is of
narrow amplitude with respect to one or more
environmental factors and that is, when present,
therefore indicative of a particular environmental
condition or set of conditions ’. The original usage of
the term ‘ biological indicator ’ in aquatic systems
referred to the detection and monitoring of change in
biota to reflect changes in the environment (e.g.
Wilhm & Dorris, 1968). More recently, and in
terrestrial systems, the concept has been used in ways
that include a far broader range of applications for
the term ‘ bioindicator ’. There has also been a
proliferation of synonyms and related terms (see, for
example Spellerberg, 1991 ; Hammond, 1994 ; New,
1995). However, bioindication, and the variety of
terms used in relation to the concept, can be
apportioned into three categories corresponding to
the three main applications of bioindicators. These
183
are environmental indicators, ecological indicators
and biodiversity indicators.
(1) Environmental indicators
An environmental indicator is a species or group of
species that responds predictably, in ways that are
readily observed and quantified, to environmental
disturbance or to a change in environmental state
(see e.g. Hellawell, 1986 ; Paoletti & Bressan, 1996).
This would include, for example, the types of
indicators distinguished and defined first by Jenkins
(1971) and later by Spellerberg (1991) as follows : (i)
Sentinels : sensitive organisms introduced into the
environment, for example, as early-warning devices
or to delimit the effect of an effluent. (ii) Detectors :
species occurring naturally in the area of interest and
which may show a measurable response to en-
vironmental change, e.g. changes in behaviour,
mortality and age-class structure. (iii) Exploiters :
species whose presence indicates the probability of
disturbance or pollution. (iv) Accumulators : organisms
that take up and accumulate chemicals in measur-
able quantities. (v) Bioassay organisms : selected
organisms used as laboratory reagents to detect the
presence and}or concentration of pollutants, or to
rank pollutants in order of toxicity.
(2) Ecological indicators
Indicator taxa are now used far more frequently to
demonstrate the effects of environmental change
(such as habitat alteration and fragmentation and
climate change) on biotic systems, rather than
functioning merely as gauges of changes in en-
vironmental state. Meffe & Carroll (1994) discuss
the necessity of focusing on the ‘ management of
indicator species that act as surrogates for the larger
community ’. In this context they refer to ‘ species
that are known to be sensitive to habitat frag-
mentation, pollution, or other stresses that degrade
biodiversity ’. These species represent the response of
at least a subset of other organisms to such stresses
and thus are, as defined here, ecological indicators
(Noss, 1990). Meffe & Carroll (1994) define an
indicator species as ‘ a species used as a gauge for the
condition of a particular habitat, community, or
ecosystem ’. As pointed out above, ecological in-
dicators are, however, more than ‘ gauges ’ of
environmental state, because the response and
condition (e.g. population decline or size, changes in
spatial distribution) of the ecological indicator itself
is of intrinsic conservation interest or concern. The
184
second part of Meffe & Carroll’s (1994) definition is
more in line with what is meant here by an ecological
indicator, i.e. ‘ a characteristic or surrogate species
for a community or ecosystem ’ (see also Dufre# ne &
Legendre, 1997).
An ecological indicator is thus a characteristic
taxon or assemblage that is sensitive to identified
environmental stress factors, that demonstrates the
effect of these stress factors on biota, and whose
response is representative of the response of at least a
subset of other taxa present in the habitat.
(3) Biodiversity indicators
Insect indicator taxa have also been used recently in
a third context, namely as ‘ indicators of biodiversity ’
(e.g. Noss, 1990 ; Gaston & Williams, 1993 ; Flather
et al., 1997 ; Prendergast, 1997) (also sometimes
termed ‘ surrogates of biodiversity ’, see e.g. Vane-
Wright, Smith & Kitching, 1994). Indeed, the
current literature is dominated by discussion of this
category of bioindication. A biodiversity indicator is
a group of taxa (e.g. genus, tribe, family or order, or
a selected group of species from a range of higher
taxa), or functional group, the diversity of which
reflects some measure of the diversity (e.g. character
richness, species richness, level of endemism) of other
higher taxa in a habitat or set of habitats (Gaston &
Blackburn, 1995 ; Gaston, 1996 a). Here, the species
richness (or other diversity measure) of a particular
indicator taxon or functional group is used to
estimate the species richness of other (closely and
sometimes even distantly related) taxa (Noss, 1990 ;
Ryti, 1992 ; Gaston & Blackburn, 1995 ; Vane-
Wright, 1996). Williams (1996) describes bio-
diversity indication as the use of species, higher
taxon richness, or environmental or habitat classifi-
cation as a surrogate of character (genetic) richness
(see also Margules & Redhead, 1995). Biodiversity
can thus be evaluated at a number of levels of
organisation including genetic (character), species
or ecosystem levels (Noss, 1990). Energy-flux and
ecosystem approaches have also been used as
predictors of biodiversity (see e.g. Turner, Gatehouse
& Corey, 1987 ; Currie, 1991), but these approaches
are not based primarily on taxic measures (Vane-
Wright et al., 1994). Kremen (1994) discusses ‘ target
taxon analysis ’ which involves the inventory of
‘ biogeographically informative ’ taxonomic groups
that are likely to represent environmental gradients
and the distribution patterns of species in other
unrelated taxonomic assemblages. Hammond (1994)
makes a further distinction between groups of
M. A. McGeoch
biodiversity indicators, based on their application,
from which ratio-based extrapolations are made,
that he defines as follows : (i) Reference group, used as
a basis for extrapolation to a group for which less full
data are available. (ii) Key group, whose principal
role is to provide a focus for efforts made to document
and estimate species richness in a given arena. (iii)
Focal group, performs a ‘ reference ’ role, but rep-
resents a subset of a larger group of interest selected
specifically for its qualities as a predictor set (see also
Ryti, 1992). Somewhat different uses of this term are
found in, for example, Kitching (1996) where
according to the definitions provided here,
Kitching’s groups would be ‘ target groups ’ rather
than ‘ focal groups ’. Lambeck (1997) uses ‘ focal
species ’ to mean those species that encapsulate the
needs of other species. Lambeck’s (1997) ‘ focal
species ’ are conceptually similar to umbrella species
(Murphy & Wilcox, 1986), and in the scheme
provided here ‘ ecological ’ rather than ‘ biodiversity ’
indicators. (iv) Target group, merely a group that is
under investigation or the object of attention [a
somewhat different definition to Kremen’s (1994)
‘ target taxa ’].
The term ‘ biodiversity indicator ’ has been used
when referring to measurable parameters, or vari-
ables, of biodiversity (Noss, 1990 ; Reid et al., 1993 ;
Meffe & Carroll, 1994). These included, for
example, species richness and endemism, genetic
parameters (such as allelic diversity and hetero-
zygosity), population-species parameters (such as
population dynamics factors and community com-
position variables), community-ecosystem par-
ameters (such as diversity and distribution range),
and landscape parameters (such as patch size and
shape and rates of energy transfer). These variables
are certainly indicative measures of biodiversity (in a
similar way to which market indicators reflect the
state of an economy). However, the original defi-
nition, and more common use, of the term indicator
in biology refers to taxa as the unit of bioindication,
and uses measurable variables associated with the
bioindicator to establish baseline value systems and
to monitor changes in them. The hierarchy of
measures presented by Noss (1990) and the list
recommended by Reid et al. (1993) provide an
extremely useful approach to measuring biodiversity.
However, to avoid possible semantic confusion I
recommend that these parameters, or measurable
variables, of biodiversity be referred to as such and
that the term bioindicator be used to refer to the
taxon or group of taxa for which these variables are
to be measured.
Terrestrial insects as bioindicators 185

INDICATOR CATEGORY ALTERNATIVE FUNCTIONS

Indicator used to:
detect a change in environmental state
Environmental
monitor changes in environmental state

demonstrate the impact of a stressor

on biota
Ecological
monitor longer term stressor-induced
changes in biota

identify diversity of taxa in a specified

area
Biodiversity
monitor changes in biodiversity

Fig. 1. The functions of bioindicators in each category of bioindication.

(4) Definition : biological indicator With respect to bioindication, monitoring is thus

A loose, all-encompassing definition of a biological
indicator would therefore be a species or group of
species that readily reflects : the abiotic or biotic state
of an environment ; represents the impact of en-
vironmental change on a habitat, community or
ecosystem ; or is indicative of the diversity of a subset
of taxa, or of wholesale diversity, within an area.
(5) Monitoring
A term often used in close association with ‘ in-
dicator ’ is ‘ monitoring ’ (e.g. Kremen, Merenlander
& Murphy, 1994 ; Pearson, 1994). Although the
term ‘ monitoring ’ is often used in a very broad
sense, a clear definition of the term is necessary to
facilitate the design of monitoring programmes
(Hellawell, 1991). Hellawell (1991) makes the
following distinctions between monitoring and re-
lated activities : (i) Survey : an exercise in which a set
of qualitative or quantitative observations are made,
usually by means of a standardized procedure and
within a restricted period of time, but without any
preconception of what the findings ought to be (see
also Haila & Austin, 1996). (ii) Surveillance : an
extended programme of surveys undertaken in order
to provide a time series, to ascertain the variability
and}or range of states or values which might be
encountered over time (but again without pre-
conception of what these might be). (iii) Monitoring :
intermittent (regular or irregular) surveillance car-
ried out in order to ascertain the extent of compliance
with a predetermined standard or the degree of
deviation from an expected norm.
the repeated application of bioindicator taxa to
provide information on the environmental con-
ditions, or effects thereof, to which they were initially
identified as suitably sensitive and for which baseline
standards, thresholds or relationships have already
been determined. Hawksworth & Ritchie (1993)
actually define biomonitors (‘ species in which
changes in numbers or distribution over time are
studied and compared with baseline data ’ (Hawks-
worth, 1993)) as being distinct from bioindicators,
which they refer to merely as organisms that indicate
(usually qualitatively) environmental state.
Monitoring is usually, although it need not
necessarily be, the endpoint of all categories of
bioindication studies. Bioindicators can be used for
single, once-off assessments or, repeatedly, for longer
term monitoring of the scenario of interest (Fig. 1).
Hinds (1984) makes a useful distinction between
what he terms ‘ biological ’ and ‘ ecological ’ moni-
toring. Biological monitoring uses taxa as ‘ surrogate
filters to be analysed to indicate environmental
quality ’, whereas ecological monitoring is the ‘ pur-
poseful and repeated examination of the state or
condition of specifically defined biotic groups in
relation to external stress ’ (Hinds, 1984). This
distinction compares well with the difference drawn
here between the traditional interpretation of the
term ‘ bioindicator ’ (referred to above as an en-
vironmental indicator) that would be used in
‘ biological monitoring ’ programmes and the more
recent application of bioindicators (referred to above
as an ecological indicator) in ‘ ecological moni-
toring ’.
186
The different uses of insects (or other biota) in
bioindication and monitoring programmes as en-
vironmental, ecological or biodiversity indicators
can thus be included in a single, clearly defined
concept of biological indication (bioindication), and
the taxa used collectively referred to as ‘ bio-
indicators ’.
III. THE OBJECTIVES OF TERRESTRIAL
INSECT BIOINDICATOR STUDIES
Article 7 of the Convention on Biological Diversity
(1992), to which over 157 countries are signatory,
states that each contracting party shall, as far as
possible and as appropriate identify components of
biological diversity important for the long-term
conservation and sustainable use of biodiversity
(Glowka et al., 1994). Among the recommended
categories of such listed components are those with
‘ importance for research into the conservation and
sustainable use of biological diversity, such as
indicator species ’.
Independently of the mandate set by the Con-
vention, bioindicators have in the past and continue
to be used today to determine the state of en-
vironmental health and to be tested as potential
predictors of biodiversity and of the impact of
environmental change on natural systems.
(1) Environmental indicators
The traditional approach to indicator studies, where
the indicator taxon is monitored so that changes in
environmental condition can be detected (i.e. en-
vironmental indication), has most commonly been
applied using soil invertebrates as bioindicators of
soil fertility and pollutant levels (such as pesticides,
heavy metal and acidic pollutant levels) (see Paoletti
& Bressan, 1996). In comparison with aquatic
environmental indication, this approach has seldom
been applied using insects in terrestrial systems, with
the exception of the use of pedofauna (Paoletti &
Bressan, 1996).
Possible reasons for the above include that the
type and degree of environmental change (such as
air pollution, habitat alteration and fragmentation,
invasions of exotic organisms) is commonly known
prior to investigation in terrestrial insect indicator
studies (e.g. Jones, 1987 ; Kroupa, Spitzer & Novak,
1990 ; Davies, Davidson & Port, 1992 ; Steenkamp &
Chown, 1996). Using biota to indicate changes in
physical or chemical environmental conditions, or
M. A. McGeoch
vegetation, when the changes can be measured
directly and far more accurately using instrumen-
tation, or by other means, is futile (Kremen, 1992).
Also, when subtle, complex environmental changes
occur, direct measurement of the stressor is often
more useful because it may be difficult to distinguish
biotic changes as being either a direct consequence of
anthropogenic influence or merely part of the
inherent dynamics of the system being examined
(Underwood, 1989 ; Stork & Samways, 1995).
In certain instances, however, insect indicators
remain potentially useful as signallers of change in
environmental state (Zonneveld, 1983). Direct meas-
urement of disturbance often requires sophisticated
procedures and equipment that are expensive to
purchase and run. Environmental indicators may
then be a more feasible alternative. In other
instances, environmental changes in terrestrial eco-
systems may be subtle and a result of complex
interactions between abiotic and biotic components
that cannot be measured directly (e.g. Zonneveld,
1983 ; Spellerberg, 1992 ; Stewart-Oaten, 1993 ;
Worthen, Mayrose & Wilson, 1994). Occasionally,
environmental changes can also be detected in biota
long after physical or chemical traces of the impact
are no longer directly measurable, or the biological
indicator may reflect more accurately the presence
and extent of a disturbance (e.g. Dallinger, Berger &
Birkel, 1992 ; Spellerberg, 1992).
(2) Ecological indicators
Using species or groups of taxa as indicators of the
impact of environmental stressors on biotic com-
munities (ecological indicators) is arguably perhaps
the more critical objective in the field of bio-
indication. Ecological understanding of anthropo-
genically induced effects on biota is essential if an
attempt is to be made to ameliorate the impact of
human activity and conserve biodiversity. This
should be the primary goal of all conservation
efforts. Studies on the impact of particular en-
vironmental stressors generally focus on single
species, single assemblages or communities, or single
groups of closely related taxa. Such bioindication
studies serve two purposes. They indicate that a
particular stressor does (or does not) have a biotic
impact, and they provide critical information for the
conservation of the indicator taxa or group, par-
ticularly when the species are known to be rare and
endangered (e.g. Butterfield, et al., 1995). However,
only restricted, indicator-related interpretations can
be made from the results of single taxon or
Terrestrial insects as bioindicators
assemblage studies. The utility of ecological indi-
cators would be substantially greater if their represen-
tativeness of other taxa could be demonstrated
(Noss, 1990 ; Dufre# ne & Legendre, 1997). Further
relational studies are thus required to determine
whether the sensitivities demonstrated by the in-
dicator reflect trends in related and unrelated taxa
within the ecosystem or habitat. Few studies have
progressed to this stage and there is presently little
evidence to suggest that any taxon or group of
organisms can be expected to qualify as an ecological
indicator in this sense. Indeed, although groups of
terrestrial taxa have been identified as potential
indicators of climate change (Holloway, 1990 ;
Holloway & Stork, 1991 ; Kremen, 1992), evidence
shows that the response of late Quaternary plant
communities to global warming was individualistic
and that communities of species did not shift as
tightly linked assemblages in response to this change
in environmental state (Woodward, 1987 ; Graham
& Grimm, 1990). Perhaps Hammond’s (1994)
‘ shopping basket of taxa ’ approach may prove
successful here if the responses of carefully selected,
different taxa, which each represent the response of
a limited set of other taxa (perhaps most closely
taxonomically or functionally related taxa, rather
than communities), are investigated. In combi-
nation, the taxa in this ‘ shopping basket ’ may then
provide an adequate representation of the response
of the community, habitat or ecosystem of interest to
the stressor of interest. While the urgency of taking
conservation measures may demand that decisions
be made on the basis of single taxon, limited-
relational studies, such action should not deter
biologists from extending studies by this further step
to determine the representativeness of selected
ecological indicators.
(3) Biodiversity indicators
The urgent need for the prioritization of areas for
conservation has been necessitated by intense com-
petition for land by agriculture, industry and urban
development. Areas for conservation are prioritized
by identifying optimal sets of viable but threatened
areas for maximizing overall diversity (Margules,
Nicholls & Pressey, 1988). Our knowledge of the
taxonomy and distribution of invertebrates is, how-
ever, poor and we are thus unable to provide
detailed systematic evaluations of the group (Vane-
Wright et al., 1994). The only alternative is to use
taxa (groups of invertebrates or other organisms)
that are better known and that will, with some
187
predetermined degree of accuracy, represent whole-
sale biodiversity (Savage, 1982 ; Vane-Wright et al.,
1994 ; Williams, Gaston & Humphries, 1997). This
concept may then be applied by using biodiversity
indicator groups to identify priority areas for
conservation. Biodiversity indicators save the time
and expense that would be necessary for com-
prehensive biodiversity surveys (if such surveys were
at all possible).
The identification of priority areas for conser-
vation based on bioindicator testing and application
has been and continues to be dealt with extensively
in the literature (see e.g. Humphries, Williams &
Vane-Wright, 1995). Here, I merely extract the
principal objectives of biodiversity indication and
highlight some of the key literature.
Several studies, including both insect and other
taxa, have examined the possible indicator value of
particular taxa for predicting the richness of one or
more other taxa (Gaston, 1996 a, b ; Williams, 1996).
An example is the study by Beccaloni & Gaston
(1995) where the Ithomiinae (Nymphalidae, Lepi-
doptera) were identified as a biodiversity indicator
on the basis of their representativeness of the diversity
of forest-dwelling neotropical butterflies. Conversely,
Prendergast et al. (1993), using high species richness
and rare species as criteria for site selection, found
low coincidence of species-rich areas (hot-spots) and
areas harbouring rare species for either plants, birds,
butterflies or dragonflies. These studies (see also
Oliver & Beattie, 1996) are based on the so-called
‘ hot-spot ’ approach (Mittermeier, 1988) and do not
address the critical issue of complementarity that has
been recognized as an integral component for
markedly improving the efficiency of site-selection
procedures (Kirkpatrick, 1983 ; Ackery & Vane-
Wright, 1984 ; Collins & Morris, 1985 ; Vane-
Wright, Humphries & Williams, 1991).
Considering complementarity, Vane-Wright
(1996) summarizes the objectives of biodiversity
indicator studies as being founded on the following
three principles : (i) Complementarity and efficiency.
Efficiency is achieved by maximising complement-
arity, defined as the degree to which a single area or
subset of areas represents the total number of
attributes found in the whole system, or adds
unrepresented attributes to one or more specified
areas. Here, the identity of component biodiversity
attributes is critical, without which area selection
based on minimum taxon sets cannot be optimised.
(ii) Vulnerability. Action (i.e. selection of areas for
conservation) should be directed at areas that are
most threatened and at the same time that are most
188 M. A. McGeoch

likely to benefit from the action taken. (iii) Viability. biodiversity predictor sets (Cousins, 1991 ; Gaston,
Areas chosen for conservation action should not only 1996 c).
contain the optimal attributes for conservation
determined according to the previous two principles (4) Monitoring
but, based on ecological principles of viability, must
The objectives of monitoring programmes are to
be capable of sustaining their biodiversity subsets in
evaluate the changes over time in habitat structure,
the forseeable future.
function and composition in response to natural
Complementarity analysis is thus a component of
factors, human activity or management practices
site-selection procedures (e.g. Nicholls & Margules,
(Noss, 1990 ; Spellerberg, 1991) (Fig. 1). Hellawell
1993 ; Pressey et al., 1993 ; Margules, Creswell &
(1991) defines three general categories that sum-
Nicholls, 1994). An assessment of complementarity,
marize the motivations for instituting a biological
in terms of reserve selection, requires the identity of
monitoring programme and that are relevant here to
species to be known. Biodiversity indicator measures
the use of bioindicators : (i) assessing the effectiveness
(e.g. species richness of taxon or groups) may,
of policy or legislation, e.g. long-term survival of rare
however, be used in complementarity analyses. The
or endangered species in designated conservation
complementarity value of an area is given by the
areas ; (ii) regulatory (performance or audit func-
number of so-far unrepresented indicator species,
tion), e.g. monitoring levels of soil pollutants ; (iii)
and the objective of maximum-coverage complemen-
detecting incipient change (‘ early warning ’), e.g.
tarity methods is to find the smallest possible set of
effects of development on biodiversity (see Kremen et
areas, or total land area, that represents each of the
al., 1994).
indicator species a prescribed number of times
To date, few terrestrial insect bioindicators have
(Vane-Wright et al., 1991 ; Church, Stoms & Davis,
been used in monitoring, and the potential for their
1996 ; Faith & Walker, 1996). The complementarity
future application rests on the outcome of bio-
value for an effective biodiversity indicator group
indicator selection procedures. Approaches to and
will predict that the set of areas species-rich for the
methods for these procedures are discussed below.
indicator group is species-rich in general (Faith &
Walker, 1996 ; although here a non-taxic approach is
IV. METHODOLOGY
adopted using environmental pattern as the in-
dicator).
To fulfil the objectives of the three types of
The primary objective of biodiversity indication is
indication, and to reduce uncertainty concerning the
thus the use of insect indicator taxa in conservation
utility of terrestrial insects as bioindicators, a series of
planning (Pressey & Nicholls, 1989 ; Brown, 1991 ;
rigorous procedural steps for the selection of bio-
Kremen et al., 1993 ; Lees, 1996). During the
indicators is recommended (Table 1).
selection and design of nature reserves and the choice
of areas to be given conservation status, insect groups
(1) Preliminary approach
are used as biodiversity indicators to highlight areas
of maximum collective diversity (Humphries et al., Efforts directed towards sustainable development
1995 ; Lees, 1996), and are expected or hoped to be and the conservation of biodiversity arise from
indicative of total (unknown, unnamed or wholesale) common societal values (Williams, 1996). Irres-
biological diversity. pective of whether a society holds utilitarian or
General patterns are not evident from the bio- intrinsic values on attaining conservation objectives,
diversity indicator studies that have been conducted the bioindication of environmental disturbance,
and relationships found differ between taxa, region stress effects on biota, or of biodiversity, necessitates
and spatial scales (Gaston, 1996 c). Although the this shared appreciation for bioindication objectives.
relationships found between the species richness of Hereafter, the initial steps in a bioindication study
different taxa are mostly positive, statistically strong must involve a clear definition of the objectives and
correlations between taxa are rare (Gaston, 1996 b). endpoint of the proposed bioindicator selection
Further investigations of biodiversity indicator value process (Steps 1 and 2, Table 1). If the objectives
are necessary (such as those conducted by Balmford, and endpoint are not clearly defined, the field of
Green & Murray, 1996 a, and Balmford, Jayasuriya bioindication at best provides improved ecological
& Green, 1996 b) across both taxa and scales, as well understanding of the system and information for the
as investigations of the use of functional groups, or conservation of the chosen indicator or, at worst,
sets of diverse taxa, rather than taxonomic groups, as meaningless correlations of poorly defined variables.
Terrestrial insects as bioindicators
(2) Scale
The selection of potential bioindicators, the design of
sampling procedures and experiments, and the
analytical methods chosen to test relationships
between indicators and abiotic or biotic environ-
mental parameters are not only dependent on the
objectives of the study, but also on the scale at which
it must be undertaken to achieve these objectives. All
anthropogenically induced environmental changes
take place within the context of natural earth systems
(Fig. 2 A). To distinguish human-induced from
natural processes, and to conduct indicator iden-
tification and selection studies at appropriate scales,
it is necessary to view environmental changes in this
context (Levin, 1992 ; Weaver, 1995 ; Gaston, 1996 b)
(Fig. 2 B).
On a temporal scale, stressors, or disturbances,
have a time of incidence followed by a period during
which the impact of the stressor is experienced by the
biota that are exposed to it. The incidence of a
stressor may be a single rapid event (e.g. an
accidental pollutant spill), episodic, intermittent or
continuous (e.g. climate change), and the temporal
scale relevant to bioindication studies therefore
ranges from seconds to periods of over a century
(Fig. 2 B) (e.g. Lancia, Adams & Lunk, 1986).
Because larger-spatial-scale stressor effects are
inclusive of the scales below them, stressors operating
at the greatest spatial scale can, potentially, be
experienced by organisms at all lower scales. Thus,
the impact of a stressor may be evident at the
smallest level of a single habitat unit of an individual
organism, in which case bioindication procedures
may be macro-molecular or organ-based (e.g. heavy-
metal contents of insect tissues or numbers of
ovarioles in female individuals : Kroupa et al., 1990)
(Fig. 2). When stressors operate at larger local,
regional or global scales, bioindication procedures
may also involve the measurement of parameters
associated with species (population), communities or
higher level taxonomic groups (Noss, 1990). The
influence of spatial scale on species richness relation-
ships is pervasive and biodiversity indication studies
cannot afford to ignore scaling effects (Hammond,
1994 ; Rykken, Capen & Mahabir, 1997). The
spatial scaling restrictions on the choice of a
bioindicator are thus the distribution of the species
or group and the presence of suitable habitat within
the area in which it is required as an indicator. The
objective of bioindicator selection is then to identify
the organism or group of organisms below this scale
of stressor incidence, and at the scale of interest, that
189
readily respond to the stressor (or in the case of
biodiversity indicators reflect the diversity of other
taxa).
Bioindication studies can thus be conducted at a
variety of spatial and temporal scale combinations
(Fig. 2 B). Biodiversity indication studies, for ex-
ample, are conducted at all but the smallest spatial
scales, and may yield utilisable results in the short
term so that, for example, urgent reserve-selection
decisions can be made. Alternatively, they may be
conducted on a long-term basis to monitor bio-
diversity turnover and the impact of landscape
alteration and other stresses on biodiversity patterns.
However, at least initially biodiversity indication
tends to demand a higher spatial to temporal scale
ratio approach than either ecological or environ-
mental indication (Fig. 2 B). Conversely, environ-
mental indication studies are most usefully con-
ducted at local and smaller spatial scales, but over
short to indefinitely long time periods (Fig. 2 B).
Long-term monitoring will of course shift all in-
dicator studies along the temporal axis of Fig. 2 B.
Ecological indication studies may span any of these
scales (Fig. 2 B), although they should preferably fall
within Wiens’ (1989) space-time scaling zone. As the
spatial scale of examination increases, the time scale
of relevant mechanistic processes also increases
(Wiens, 1989). Indicator studies conducted within
this space-time scaling zone (see shaded area of Fig.
2 B) will thus have high predictive power. Below, I
will show that this is one of the essential elements of
a successful bioindication study. In the face of the
current urgency of conservation actions and the
present structure and financing of research pro-
grammes, ecological indicator studies tend to be
executed well below their appropriate space-time
scaling functions (May, 1993 ; Root & Schneider,
1993), giving them only apparent high predictability
(Wiens, 1989). Therefore, focusing on the objective
of the envisaged study, the scale at which the stressor
in question operates and the scale at which it is likely
to have an effect on the potential indicator taxon or
group chosen, will reveal the most appropriate
scaling zone within which the study should be
conducted.
(3) Criteria for the selection of potential
indicator species
(a) General criteria
After clarification of the objectives, endpoint and
scale at which the bioindication study is to be
conducted (Table 1, Steps 1 & 2), potential
190
Table 1. Procedural steps in bioindicator studies involving terrestrial insects beginning with the categorization of the
objective of the study as being either environmental, ecological or biodiversity indication (Step 1)
Step 1. Determine broad
objective
Step 2. Refine objectives and
clarify endpoint
Step 3. Select potential indicator
based on accepted a
priori suitability criteria
Step 4. Accumulate data on
indicator (for
approaches see, e.g.
Margules & Austin,
1991 ; Schneider &
Gurevitch, 1993 ;
Margules & Redhead,
1995)
Step 5. Collect quantitative
relational data
Step 6. Establish statistically the
relationship between
the indicator and the
relational data (see, e.g.
Margules & Austin,
1991)
Step 7. Based on the nature of
the relationship, either
accept (preliminarily)
or reject the species,
higher level taxon or
assemblage as an
indicator
Environmental Ecological indication
indication
To detect and identify To determine and be
the nature of able to predict the
disturbances or changes impact of disturbance
in environmental (pollution, habitat
quality or state (e.g. alteration, climate
pollutants, habitat change) on biota
alteration, vegetation (communities, habitats,
successional stage) ecosystems) using an
using an indicator indicator
Select a species, higher Select a species, higher
level taxon, assemblage level taxon, assemblage
or community (decision or community (decision
partly scale dependent) partly scale dependent)
Determine the response Establish pollutant
of the indicator to concentrations in the
disturbance organism, species
(environmental state) presence}absences,
abundance}s, richness,
biomass, productivity,
interactions, temporal
changes of indicator
Measure levels of Measure levels of
disturbance : pollutant disturbance : pollutant
concentrations, altered concentrations, altered
habitat parameters habitat parameters,
climatic variables
Establish the relationship Establish the relationship
between the between the
disturbance disturbance and the
(environmental state) contamination level,
and the contamination composition, structure,
level, composition, or function of the
structure or function of indicator
the indicator
Are there significant, Are there significant,
strong correlations strong correlations
between the between the
disturbance disturbance and
(environmental state) measured qualities of
and measured qualities the indicator ? YES :
of the indicator ? YES : continue to step 8. NO :
continue to step 8. NO : either conclude that the
repeat procedure from disturbance has no
step 3. impact on the biota or
repeat procedure from
step 3.
M. A. McGeoch
Biodiversity indication
1. To identify
biodiversity hot-spots
using an indicator.
2. To assess and be able
to predict biodiversity
in selected areas using
an indicator
Select a higher level
taxonomic group, or a
group containing an
array of selected taxa
Define geographic
boundaries within
which biodiversity is to
be assessed and
quantify the diversity
(richness and
abundance) of the
selected indicator group
in selected subset areas
(scale dependent)
Determine the diversity
(richness and
abundance) of selected
taxa other than the
indicator group in the
subset areas
Establish the relationship
between the diversity of
the indicator group and
the diversity of other
taxa
Is there a significant,
strong, positive
correlation between the
diversity of the
indicator group and the
diversity of other taxa
in the area ? YES :
continue to step 8. NO :
repeat from step 3.
Terrestrial insects as bioindicators 191

Step 8. Establish the robustness Ho : there is no Ho : there is no Ho : there is no

of the indicator by
developing and testing
appropriate hypotheses
under different
conditions (see, e.g.,
Murtaugh, 1996)
Step 9. If the null hypotheses
are rejected make
specific
recommendations,
based on the original
objectives, for the use of
the indicator.
significant relationship
between the
disturbance
(environmental state)
and measured qualities
of the indicator in other
areas or at different
times
Use the indicator to Use the indicator to
detect and monitor the
presence and level of a
disturbance (or
condition of an
environmental state).
"
significant relationship significant, strong,
between the positive relationship
disturbance and between the diversity of
measured qualities of the indicator group and
the indicator in other one or more other taxa
areas or at different in different
times. Ho : the geographical areas
#
relationship between
the disturbance and
other taxa is different
to the relationship
discovered in the
previous step
Use indicator group to
monitor and predict the estimate or to monitor
impact of disturbance biodiversity in selected
on communities, regions.
habitats and
ecosystems.

indicators are selected according to appropriate
characteristics of the species or group that are known
a priori (Table 1, Step 3 ; Table 2). Although the
characteristics of a good indicator are almost entirely
dependent on the objectives of the environmental
issue being addressed, as well as on the spatial and
temporal scale of the latter, suitable and effective
indicators must generally fulfil criteria in two broad
categories. First, economic and logistic suitability
(including financial cost, time efficiency and per-
sonnel requirements) and second, biological efficacy
(including taxonomic, distributional, reliability, rep-
resentation and sensitivity criteria). It is essential
that any bioindication or monitoring programme
require the minimum time expenditure and be
financially viable, particularly if it is to be executed
on a long-term basis (Table 2, no. 1). The cost of an
indicator selection or monitoring programme has to
be weighed against the potential cost of failure to
achieve the stated objectives (Noble & Norton,
1991). Financial, personnel and time constraints will
determine both the likelihood of the adoption of such
a programme, as well as its long-term continuation.
Methods for reducing the cost of invertebrate
biodiversity indication surveys have been suggested,
e.g. the use of higher taxa (Balmford et al., 1996 b ;
Williams, 1996) and morphospecies (Oliver &
Beattie, 1996). However, there is an inevitable
compromise between reducing expenses and the loss
of resolution as a result of using taxonomically coarse
data (Balmford et al., 1996 a ; Williams, 1996).
Therefore, cost–benefit analyses that consider the
stated objectives of individual bioindication pro-
grammes have to be conducted prior to their
implementation (Noble & Norton, 1991). In some
instances, the use of bioindicators is advocated for
the very reason that expenditure is lower when using
a bioindicator than when using more direct or
comprehensive analytical procedures (e.g. Paoletti
& Bressan, 1996).
Numerous authors have discussed biological and
practical criteria for the selection of bioindicators
(see e.g. Lenhardt & Witter, 1977 ; Holloway, 1980 ;
Hellawell, 1986 ; Noss, 1990 ; Brown, 1991 ;
Holloway & Stork, 1991 ; Spellerberg, 1991 ;
Kremen, 1992 ; Pearson & Cassola, 1992 ; Kremen et
al., 1993 ; Hammond, 1994 ; Pearson, 1994) and
these criteria are listed in Table 2. Some of the
criteria are obviously applicable to either only one,
or more, categories of bioindication, whereas others
are scenario-specific, or optional. For example, it is
vital in all categories of bioindication that the
taxonomy of bioindicator species or higher taxa is
sound and stable. The single greatest limitation to
the use of terrestrial insect groups as indicators is the
state and difficulty of practical identification of
insect taxa (Vane-Wright et al., 1994) (Table 2, no.
6). As a further example, the wider the geographic
range and the more diverse the habitat types
occupied by a bioindicator taxon or group, the
broader the range of experimental design and
comparison that can be made (Table 2, no. 28).
However, this criterion is not obligatory. Also, in
environmental and ecological indication, infor-
192 M. A. McGeoch

(A)
Global Carbon-dioxide Origin of
variations earth & life

10 000 km Climate
Glacial
periods
Speciation
1000 km
Soil Extinction events
Soil moisture development
variations

100 km Seasonal
vegetation
cycles

10 km Nutrient
cycles
Atmospheric
convection

1 km Atmospheric
turbulence
Local
Second Minute Day Year Century Ten One One
thousand million billion
Spatial scale

years years years

(B)

Global Climate
change

BIODIVERSITY
INDICATION ECOLOGICAL
INDICATION

Single event, Habitat alteration and destruction

point-source Pollutants
disturbance
Local ENVIRONMENTAL
INDICATION
Second Minute Century
Temporal scale
Fig. 2. The space-time scales (A) of earth-system processes (modified from National Aeronautics and Space Admin-
istration, 1988), and (B) at which bioindication studies of particular environmental states and changes are conducted.
The shaded area is the space-time scaling zone within which investigations will produce relationships that are likely
to have high predictive power (after Wiens, 1989).

mation on the life-history characteristics of species
and measured variables of a bioindicator group or
community should be easily accessible (if not already
known), quantified and analysed to facilitate the
rapid collection of large and reliable data sets that
can then be interpreted in relation to the changes
being indicated and later monitored (Table 2, no.
11). This criterion is not always essential in bio-
diversity indication (Kremen, 1992). Suitability
criteria are also not always assessable prior to
sampling or testing (Table 2).
Following guidelines such as these for the initial
selection of a potential bioindicator will minimise the
chance of proceeding with a study where the species
or group chosen is rejected as a suitable bioindicator
subsequent to a large capital and human resource
investment. In addition, if these guidelines are
considered beforehand and the study proves suc-
cessful, the chosen indicator will have comparatively
low budgetary demands when later used in bio-
indication programmes. Nonetheless, individual cri-
teria, such as those listed in Table 2, may be adopted
Terrestrial insects as bioindicators 193

Table 2. Suggested criteria for the selection of bioindicators. En, environmental indicators ; Ec, ecological indicators ; B,
biodiversity indicators. Criteria with an asterisk may be, or are usually, possible to determine before the selection of a
potential bioindicator. Other criteria are usually only assessable after testing the suitability of the selected potential
bioindicator. Ticks represent obvious criteria for consideration under each category of bioindication

Criterion En Ec B

1.* Cost efficient and effective (time, funds, personnel) (e.g. Noss, 1990) h h h
2.* Sampled and sorted easily (e.g. Hellawell, 1986) h h h
3.* Adequate representation in samples (e.g. Hammond, 1994) h h h
4.* Be abundant (e.g. Jenkins, 1971) h h h
5.* Ease and reliability of storage (e.g. Hammond, 1994) h h h
6.* Taxonomically well-known group, readily identified, taxonomic expertise readily available h h h
(e.g. Stork, 1994)
7.* Sampled individuals expendable (e.g. New, 1995) h h h
8.* Spatial and temporal distribution predictable to ensure long-term continuity (Holloway & h h h
Stork, 1991)
9. Relatively independent of sample size (e.g. Noss, 1990)
10. Changes visible by remote sensing (e.g. Jenkins, 1971)
11.* Baseline data on biology available (e.g. New, 1995) h h
12.* Abundant autecological data (e.g. Hellawell, 1986)
13.* Low genetic and functional variability (e.g. Hellawell, 1986) h
14. Sufficiently sensitive to provide early warning (e.g. Noss, 1990) h
15. Able to differentiate between natural cycles and trends and those produced by h h
anthropogenic stress factor (e.g. Noss, 1990)
16. Representative of critical components, functions and processes (e.g. New, 1995) h h
17. Show a well-defined response, i.e. either
(a) die or decrease,
(b) change or mutate,
(c) replace or be replaced by other species (e.g. Jenkins, 1971). h h
18.* Be non-target species if to be used to monitor pesticides (e.g. Jenkins, 1971) h h
19. Readily accumulate pollutants (e.g. Hellawell, 1986) h
20.* Easily cultured in the laboratory (e.g. Hellawell, 1986) h
21. Capable of providing continuous assessment over a wide range of stress (e.g. Noss, 1990) h
22.* Recognised importance to agriculture, environment etc. (e.g. Stork, 1994)
23.* Economic importance as a resource or pest (e.g. Hellawell, 1986)
24. Representative of all trophic levels and major functional guilds (e.g. Stork, 1994) h
25. Matching with target group (e.g. Hammond, 1994) h
26. Representative of related and unrelated taxa (e.g. Pearson & Cassola, 1992) h h
27.* Full range of body sizes and growth forms (e.g. Stork, 1994)
28.* Tend to be distributed over range of habitats or environments (e.g. Faith & Walker, 1996) h
29. Information rich : representative distribution (Kremen, 1994) h
30.* Group should have species that are disjunct, and environmentally dispersed, in their h
distributions (e.g. Ryti, 1992)
31.* Representatives from low-, medium- and high-diversity groups (e.g. Stork, 1994) h
32.* Wide range of host-specificities (e.g. Stork, 1994)

or disregarded in accordance with their relevance to
the particular bioindication programme being con-
ducted.
(b) Individual species and species groups as bioindicators
The levels of organization used as bioindicators
include individual species as well as groups of species.
Indeed, one of the first applications of the bio-
indicator concept was to the lists of aquatic
organisms, rather than single species, character-
istically found under conditions of varying degrees of
water pollution (Kolkwitz & Marsson, 1908).
Kremen et al. (1993) also use a group-based
definition of a bioindicator : ‘ suites of species that
194
respond to environmental change in ways that are
easily measured or observed ’.
The choice between the selection of a single
indicator species versus a group of taxa is relevant
only to environmental and ecological indication.
Biodiversity indication necessarily uses groups of
taxa because the variables of indication are always
numbers of species, numbers of functional groups,
etc. In environmental or ecological indication, the
indication variables may, in contrast, be morpho-
logical, physiological or population characteristics of
single species.
Groups of bioindicators may also be selected on
either a taxonomic or functional basis, or on some
combination of both. This therefore includes
‘ natural groups ’, in the taxonomic sense such as
Kremen’s (1994) monophyletic ‘ target taxa ’, or
subjectively delineated functional groups, or com-
binations of sets of diverse taxa.
Taxonomic groups include groups of species that
may not necessarily have any taxonomic affinity
(Hammond, 1994), as well as higher level taxonomic
groups, e.g. tribes, genera, assemblages (e.g.
Kremen, 1992 ; Samways & Steytler, 1996), families
(e.g. Luff & Woiwod, 1995) or even whole orders.
Functional groups include, guilds, trophic levels and
communities, e.g. the suggestion by Holloway &
Barlow (1992) that the proportion of tree-feeding
versus herb-feeding Lepidoptera families may be
indicative of forest disturbance. There are, however,
potential problems with the delineation of groups at
levels of organization higher than species (e.g. Block,
Brennan & Gutierrez, 1986). It has been shown, for
example, that species may be far better indicators of
total diversity than higher taxa (Prance, 1994).
Clear-cut or fixed boundaries for delineating these
units of biodiversity do not always exist, particularly
when such units incorporate complex arrays of
interactions between their members (Reid et al.,
1993 ; Williams et al., 1997). Hammond (1994)
advocates the use of ‘ shopping baskets ’ of suitable
taxa when, as may often be true, it is difficult to
identify a single taxon that fulfils all the criteria
necessary for the required bioindicator. In bio-
diversity indication, the choice thus lies between
target (higher monophyletic) taxa or some sum-
mation of not necessarily monophyletic groups of
species or higher taxa (Vane-Wright et al., 1994). As
an example of the latter, Humphries & Vane-Wright
(1992) suggest the use of 100 or more genera, tribes
or families (each of which should include approxi-
mately 200 species) of widely differing organisms for
a global biodiversity analysis. This is based on the
M. A. McGeoch
rationale that the summation of different, well-
known, taxa may prove a better surrogate of total
diversity than the use of a single target taxon (Vane-
Wright et al., 1994).
The advantages of using groups of species (i.e. in
environmental and ecological indication) rather
than single species have been stated as ‘ providing
improved resolution and scale of inventory and
monitoring ’ (Kremen et al., 1994). Groups of taxa
represent a wider array of taxonomic, functional and
habitat diversity and increase the number and types
of environmental responses that are perceived
(Kremen et al., 1994). Twenty years of ecosystem
research on the effects of chemical stressors on lakes
showed that the most sensitive biotic variables were
species diversity, food-chain length, proportion of r
strategists (selected for maximizing their biotic
potential) and the sizes and life spans of organisms
(Schindler, 1990). These include firstly and pre-
dominantly community and assemblage parameters.
In addition, attention is increasingly being directed
towards the effects of disturbance and environmental
change on interactions between species and it is on
these interactions that climate-change effects are
predicted to have a major impact (Sugden, 1992 ;
Carpenter et al., 1993 ; Ives & Gilchrist, 1993).
Cousins (1991) also highlights the potential use of
functional group variables as biodiversity measures,
e.g. size-based diversity distributions, species-rich-
ness relationships between trophic levels, correlations
between numbers of species in different guilds and
measurements of taxonomic distinctiveness. Here,
the distinction is again made between bioindicators,
and variables, or measures, of ecological function or
diversity (see above discussion of the definition of
biodiversity indicators). Di Castri, Robertson-
Vernhes & Younes (1992) recommend the incor-
poration of representatives of all major functional
guilds into biodiversity indicator programmes.
Williams (1996) also suggests that one of the
advantages of using higher taxonomic level indi-
cators (or ‘ surrogates ’) is the inclusion of a wider
range of functional relationships.
The use of higher level taxa rather than species is
frequently also advocated because of the cost of
expert assistance with identification and the frequent
lack of taxonomic expertise (see e.g. Oliver &
Beattie, 1996 ; Paoletti & Bressan, 1996). Iden-
tification of bioindicator organisms to lower taxo-
nomic levels also does not always improve the
resolution of the results obtained using higher
taxonomic level determinations (Oliver & Beattie,
1996). Furthermore, Oliver & Beattie (1996) showed
Terrestrial insects as bioindicators
that acceptably accurate assessment of terrestrial
invertebrate biodiversity may be achieved with the
use of morphospecies (see further arguments by
Goldstein, 1997 ; Oliver & Beattie, 1997). However,
the quality of the data on which bioindicator
predictions and conservation decisions are made is
ultimately fundamental to their accuracy
(Hammond, 1994 ; Vane-Wright, 1996). The out-
come of monitoring activities could also be com-
promised if morphospecies are not assigned in the
same way during serial surveillance. This ultimately
necessitates a species-level taxonomy.
Although the use of groups of taxa rather than
individual species has apparent potential advan-
tages, the choice between a single species or group of
taxa, as well as the particular type of group of taxa,
depends entirely on : (i) the category of indication
being conducted (i.e. environmental, ecological or
biodiversity), (ii) the specific objectives of the study,
and (iii) the finding, after adequate testing, that the
particular species or group is suitably sensitive and
tractable to provide the information required.
(4) Data collection and interpretation
Once the potential indicator taxon, or taxa, has been
chosen, sampling procedures are designed to identify
relationships between the indicator and the en-
vironmental or biotic variables of interest (Steps 4
and 5, Table 1). The essence of bioindication is these
‘ correlative complexes’ that exist as a result of direct
or indirect causal relationships between environ-
mental parameters and the state and behaviour of
biota (Zonneveld, 1983). These relationships have to
be identified and their robustness, or causal nature,
demonstrated (Steps 6–8, Table 1).
The utility of bioindicators lies in their predictive
ability, i.e. to accurately predict (or indicate) the
presence and extent of a disturbance (environmental
indicator), the impact of a stressor on biota (eco-
logical indicator), or the diversity of other taxa in an
area (biodiversity indicator) (Noss, 1990 ; Hum-
phries et al., 1995 ; Faith & Walker, 1996). An
indicator’s predictive value is determined by its
sensitivity, specificity and by the prevalence of the
response, or of the relationship, that it demonstrates
(Murtaugh, 1996 ; Dufre# ne & Legendre, 1997).
Therefore, the presence of significant correlations
between indicators and the variable of interest is, in
itself, insufficient to be of practical value (Gaston,
1996 b ; Flather et al., 1997). Statistically strong
correlations are usually necessary to provide pre-
dictive relationships (although see Hammond, 1994,
195
p. 126). The predictive value of the relationship will
even then often depend on the variability of the
relationship around the value of the predictor
(considering also that the data are usually trans-
formed prior to analysis reducing apparent varia-
bility) that is to be used in the prediction (Gaston,
1996 a ; Flather et al., 1997).
(5) Hypothesis testing
The initial relational patterns found between the
potential indicator and the stressor, or other taxa,
must then be used to develop hypotheses on the
response of the indicator to an environmental state,
or on the relationship between the indicator and
other taxa in the community or habitat under
examination (Treweek, 1996). The hypothesis is
then tested and the bioindicator selected or rejected
based on the outcome of formal experimental design
procedures, or testing on an independent data set
(Step 8, Table 1) (see e.g. Green, 1979, 1993 ;
Hurlbert, 1984 ; Underwood & Peterson, 1988 ;
Underwood, 1991, 1993). This step will thus
establish the robustness of the correlative relation-
ships. The need for ground-truthing biodiversity
indicators is not always as critical as it is for
environmental and ecological indicators because of
the small variance around many multi-taxon species-
richness relationships and because of the large size of
data sets used in biodiversity studies (Williams &
Gaston, 1994).
Once an indicator has been accepted on the basis
of these procedures, concrete suggestions can be
made for its use, and it will yield results with a
known degree of confidence when used in bio-
indication and monitoring programmes (Step 9,
Table 1) (e.g. Margules & Austin, 1994).
(6) Status quo
Although guidelines for comprehensive planning
approaches to the collection of ecological and
biodiversity data exist (e.g. Margules & Austin,
1991 ; Hawksworth & Ritchie, 1993 ; Reid et al.,
1993 ; Margules & Redhead, 1995), the majority of
publications on the utility of terrestrial insects as
bioindicators are either largely anecdotal, or pre-
scriptive (for example, Holloway, 1980 ; Rosenberg
et al., 1986 ; Brown, 1991 ; Holloway & Stork, 1991 ;
Stork & Eggleton, 1992 ; Kremen et al., 1993).
Of those studies that are broadly experimental,
many do not progress beyond the point of estab-
lishing the form of the relationship between the
196
potential indicator and other biotic or abiotic
variables (i.e. Step 6, Table 1). For example,
Mossakowski, Frambs & Baro (1990) claim indicator
status for carabid beetles based on a loose, qualitative
comparison of habitat quality and carabid diversity
data (i.e. Step 5, Table 1). Other studies claiming
indicator status for taxa (e.g. Majer, 1983 ; Maelfait
& Desender, 1990 ; Maelfait, Desender & Baert,
1990) reach Step 6 (Table 1) but no further attempt
is made to establish the robustness, or the represen-
tativeness, of taxa before giving indicator status to
the species or group involved.
Pearson & Cassola (1992) conducted a wide-
ranging evaluation of the potential suitability of
tiger beetles (Coleoptera : Cicindellidae) as environ-
mental, ecological and biodiversity indicators based
on published a priori criteria for indicator selection.
Their study fails to make the distinction between
selecting ‘ apparently ’ appropriate indicators and
actually formally testing the validity of these hy-
potheses. Although Pearson & Cassola (1992) find
weak, positive large-scale correlations between tiger
beetle species richness and bird and butterfly species
richness (Step 6, Table 1), they conclude merely by
stating that giving conservation status to certain
endemic cicindelid species will ‘ bring protection to
other invertebrate and vertebrate species associated
with the habitats ’. These weak correlations were
later found to be explained by the general pattern of
increasing diversity towards lower latitudes (Flather
et al., 1997). Although the documentation of large-
scale patterns certainly has a place (May, 1993), the
large-scale comparisons used in Pearson & Cassola’s
(1992) study (land area squares of 275–350 km per
side) are likely to reveal relationships that may
disappear at finer scales (Wiens, 1989 ; Curnutt et al.,
1994), i.e. the weak, broad correlations between
tiger beetle and bird and butterfly species richness
may not hold under locally heterogeneous conditions
within the borders of conservation areas where
bioindicators are likely to be used. The majority of
reserves and areas of land under conservation
management, and those areas likely to become so,
are far smaller than the spatial scales used in Pearson
& Cassola’s (1992) study. This again emphasizes the
importance of formulating bioindicator study ob-
jectives with appropriate regard to the scales at
which they are to be conducted.
A number of studies on the use of Lepidoptera as
bioindicators (Erhardt, 1985 ; Erhardt & Thomas,
1991 ; Woiwod & Thomas, 1993) also only reach
Step 6 (Table 1). Erhardt & Thomas (1991) do not
go as far as formally testing the robustness of the
M. A. McGeoch
relationship between Lepidoptera diversity and
grasslands under different management regimes.
Although Woiwod & Thomas (1993) progress little
further, they acknowledge their study as being
preliminary and rather than claiming indicator
status for their study taxa, they choose to illustrate
the importance of using both local and regional data
to understand patterns of distribution and abun-
dance. Kremen (1992) and Luff & Woiwod (1995)
progress to Step 7 (Table 1) in their studies of the
indicator properties of, respectively, a Lepidoptera
assemblage and moths and ground beetles. Kremen
(1992) acknowledges the preliminary status and lack
of statistical tests in her analysis of the indicator
properties of the Rhopalocera (Lepidoptera) in
Madagascar. However, the suggestion is made that
the Rhopalocera may be useful ecological indicators
of climate change because of their significant
response, with no measure of the strength or
predictive value of the response, to topographic and
moisture gradients. Their correlation with plant
species richness and diversity was also poor. Once
again, therefore, the potential utility of an ecological
indicator as being representative of the responses of
other taxa to the same stressor is not examined or
acknowledged. This programme to document
patterns of Madagascan butterflies and other fauna
is, however, ongoing and has well-defined, long-term
goals and in future is likely to provide the more
quantitative and directed approach to the selection
and use of bioindicators that is advocated here
(Kremen, 1992 ; Lees, 1996).
The studies mentioned above, and others like
them, nonetheless provide valuable information for
the conservation of their so-called ‘ indicator taxa ’.
They also provide invaluable baseline information
for further studies that wish to confirm, or reject, the
utility of the particular taxon or group as an
indicator (Steps 7–9, Table 1). Although successful
bioindication studies, particularly environmental
indication studies (which have followed procedures
along the lines of those outlined here, Table 1), have
been carried out using other terrestrial invertebrates
(e.g. Dallinger et al., 1992), similarly successful
examples are far less prevalent in the terrestrial
insect indicator literature.
A number of more recent publications, however,
adopt the rigorous testing approach that has been
advocated here [e.g. Paoletti, Schweigl & Favretto,
1995 (environmental indication) ; Samways &
Steytler, 1996 and Dufre# ne & Legendre, 1997
(ecological indication) ; Balmford et al., 1996 a, b
(biodiversity indication)].
Terrestrial insects as bioindicators
Balmford et al. (1996 a, b) provide a good example
of a well-planned and executed biodiversity in-
dication study with explicit objectives. Rykken et al.
(1997) actually reject the use of ground beetles as
indicators of land-type diversity in Vermont after
the outcome of ordination and classification analyses.
Samways & Steytler’s (1996) study on the use of
Odonata species and assemblages as ecological
indicators of land-use types along a river also
provides clear objectives for the selection and use of
the proposed bioindicators, as well as documented
and tested species and assemblage patterns. The only
potential addition to this study would be a general-
ization of the results found (by testing on an
independent data set) and the provision of a
geographical range estimate within which the selec-
ted bioindicators may be used. The latter also
applies to an otherwise comprehensive environ-
mental indication study by Paoletti et al. (1995) that
identifies soil organisms sensitive to heavy metals
and organochlorine residues in orchards.
The examples highlighted in this section show that
clear definition of the objectives of bioindicator
studies, formal testing of the robustness of insect
indicators, and making recommendations for their
use in detection and monitoring are the steps
necessary to improve the utility and establish the
credibility of terrestrial insects as bioindicators.
V. CONCLUSION – ‘ CATCH-22 ’
The risks of applying a strict set of methods to the
identification and selection of bioindicators, such as
those outlined above, are twofold. First, the primary
advantage of using bioindicators is to provide a cost-
and time-effective route to answering some of the
most pressing conservation questions. Exhaustive
hypothesis testing to determine the degree of ro-
bustness therefore appears almost self-defeating. This
is nevertheless critical for the future utility of
bioindication as a conservation tool ; the dangers of
ad hoc approaches to conservation have been demon-
strated previously (Pressey, 1994). Second, given the
urgency in many instances of making conservation
decisions and taking conservation action, protocols
that prescribe long-term and costly assessments
become redundant.
The status quo of terrestrial insect indication, no
matter what the extent of its potential value to
conservation, is conceptual, and the ratio of data to
theory is extremely low. The selection and testing of
bioindicators remains difficult, and progress slow,
because of inventory problems, problems associated
197
with the choice and testing of appropriate bio-
indicators and variables, and the continual need to
consider scaling issues during the planning of
programmes and the interpretation of results
(Flather et al., 1997). There are few cases where
ecologists can provide decision-makers with tried
and tested terrestrial insect indicators as tools for
conservation assessment and planning. To avoid the
indefinite continuation of this dilemma we should
not allow the urgency of conservation crises to
dishearten or blind us to the importance of medium-
to long-term research investments and a rigorous
research approach to support (or refute) the utility
and application of terrestrial insects as either
environmental, ecological or biodiversity indicators.
VI. ACKNOWLEDGEMENTS
I thank S. L. Chown, A. S. van Jaarsveld and S. Freitag
(University of Pretoria), and K. J. Gaston (University of
Sheffield) for their suggestions and comments on the
manuscript, and P. Barnard (The Natural History
Museum, London) for help with literature access. The
manuscript was substantially improved by the refereeing
of R. I. Vane-Wright (The Natural History Museum,
London). Financial assistance from WWF-South Africa
and Research Support, University of Pretoria, is gratefully
acknowledged.
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