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Annu. Rev. Entomol. 1999. 44:291–315

Copyright °c 1999 by Annual Reviews. All rights reserved

HYPERPARASITISM: Multitrophic
Ecology and Behavior
Daniel J. Sullivan
Department of Biological Sciences, Fordham University, Bronx, New York 10458;
e-mail: sullivan@murray.fordham.edu

Wolfgang Völkl
Department of Animal Ecology, University of Bayreuth, 95440 Bayreuth, Germany;
e-mail: wolfgang.voelkl@uni-bayreuth.de

KEY WORDS: biological control, facultative, heteronomous, habitat specificity, sex ratio,
foraging behavior

ABSTRACT
Hyperparasitoids are secondary insect parasitoids that develop at the expense
of a primary parasitoid, thereby representing a highly evolved fourth trophic
level. This review evaluates multitrophic relationships and hyperparasitoid ecol-
ogy. First, hyperparasitoid communities of various taxa of phytophagous and
predacious insects are described. Second, specific patterns of hyperparasitoid
community organization and hyperparasitoid ecology are described in detail, us-
ing the aphid-parasitoid–hyperparasitoid food web as a model system. Aphid
hyperparasitoid communities consist of ecto- and endohyperparasitoids, with ec-
tohyperparasitoids being less host specific than endohyperparasitoids. Lifetime
fecundity and intrinsic rate of increase of hyperparasitoids are generally lower
than those of their primary hosts. Aphid ectohyperparasitoids search randomly for
hosts and do not use specific cues, whereas endohyperparasitoids gain information
that originates from host plants or hosts for long-range search. Interactions with
adult primary parasitoids do not influence hyperparasitoid searches, but aphid-
attending ants typically prevent successful hyperparasitoid foraging. Impact of
hyperparasitism on biological control is reviewed.

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PERSPECTIVES AND OVERVIEW

Multitrophic ecology and the related behavior of the phytophagous and ento-
mophagous insects interacting as a food-web “community” was pioneered by
Askew & Shaw (4, 5). Many ecologists such as Price et al (86) have continued
this exciting research over more than 30 years. In emphasizing the “bottom-up”
effects of hosts on their parasitoids, the first trophic level shows that both inter-
and intraspecific plant variation can influence the ecology and behavior of the
second trophic level of phytophagous insects, which, in turn, is one of the major
determinants of the third trophic level of insect parasitoids (21). Insect “hyper-
parasitism” can be defined as a highly evolved fourth trophic level relationship
that exists between entomophagous insects. It refers to the development of a
secondary insect parasitoid or hyperparasitoid at the expense of a primary insect
parasitoid. The primary parasitoid attacks an insect host that is usually phy-
tophagous, but which could also be a predator or scavenger. Hence, an insect
hyperparasitoid attacks another insect that is or was developing in or on another
insect host, and this sometimes impacts on biological control of a pest insect.
Hyperparasitoids may have a considerable influence on the “top-down” con-
trol of terrestrial herbivorous arthropod populations by parasitoids (90), and
their action may have shaped the evolution of parasitoid foraging strategies
(61, 118, 129). The structure of hyperparasitoid communities, representing the
fourth trophic level, has been studied for a representative spectrum of phy-
tophagous hosts (39, 41), and the degree of resource utilization in the field is
known for most systems of economic importance. In contrast, there is only
limited knowledge of life-history parameters and of foraging behaviors of hy-
perparasitoids. Both factors are of crucial importance for the understanding of
the role of hyperparasitism in natural populations as well as in pest control (104).
Information about hyperparasitoid life history may help in understanding basic
interactions and may give rough estimates about their general capability to influ-
ence primary parasitoid populations (15a, 104). The analysis of hyperparasitoid
foraging behavior may give us an idea of the factors that influence the hyperpar-
asitoid’s foraging success and may thus contribute explanations for the levels
of hyperparasitism observed in the field. There are two multitrophic systems
with a well-studied hyperparasitoid ecology: (a) the heteronomous hyperpar-
asitoids of the genus Encarsia attacking scale insects and whiteflies (33) and
(b) the aphid-parasitoid-hyperparasitoid community (104, 105, 120). In both
systems, the involved phytophages are worldwide pests. Furthermore, they are
easy to keep in the laboratory, and the knowledge of hyperparasitoid ecology is
of basic importance for the design of biological control programs. However, in
heteronomous hyperparasitoids or adelphoparasitoids, only males develop as
hyperparasitoids, attacking females of their own or another parasitoid species
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(33, 68, 82, 84, 104, 117, 134, 136). But aphid hyperparasitoids generally
develop as obligate hyperparasitoids (104, 105). In this review, we first re-
port on the structure of hyperparasitoid communities in various taxa of host
parasitoid systems and on levels of resource utilization. Concerning ecology
and behavior, we focus on obligate hyperparasitoids. We use the aphid hyper-
parasitoid community as a model system to show typical patterns of selected
life-history aspects and foraging strategies at the fourth trophic level.

TERMINOLOGY
“Obligate” hyperparasitoids are always secondary parasitoids: Their progeny
can develop only in or on a primary parasitoid. A subcategory includes both
“true” hyperparasitoids, which attack the primary parasitoid through the her-
bivore, and “pseudohyperparasitoids,” which attack the primary parasitoid in
the cocoon stage after it has emerged from the host (39). “Facultative” hy-
perparasitoids have progeny that can develop either as primary or as secondary
parasitoids. Endophagous hyperparasitoids have larvae that feed inside the host,
whereas ectophagous species feed externally. Another feeding-related distinc-
tion is between koinobionts, which allow their hosts to continue development
after oviposition, and idiobionts, which paralyze or kill their hosts in the process
of oviposition (4, 29). “Direct” hyperparasitoids attack the primary parasitoid
directly by ovipositing in or on it. “Indirect” hyperparasitoids attack the primary
parasitoid’s phytophagous host and thus only attack the parasitoid itself indi-
rectly. In this case, the female hyperparasitoid oviposits into the phytophagous
host whether it is parasitized or not (31).

EVOLUTION
Hyperparasitism has evolved in only three insect orders: Hymenoptera (17
families) and perhaps in a few species of Diptera and Coleoptera (33). Only
Hymenoptera are treated here.

Evolution of Hyperparasitism in Hymenoptera

PRIMARY PARASITISM The recent review by Whitfield (131) suggested that
parasitism arose once, in the common ancestor of the Orussoidea (parasitic
wood wasps) and the monophyletic Apocrita (narrow-waisted wasps). The ori-
gin of the Apocrita, and therefore parasitism in the Hymenoptera, dates to the
Jurassic period, about 135 million years ago (88). This precursor specialized
in larval feeding within tunnels in wood and at least partly upon fungi (intro-
duced and/or promoted by secretions from the adult female wasp at the time of
oviposition). Ectoparasitism probably evolved before endoparasitism, with the
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294 SULLIVAN & VÖLKL

parasitoid egg deposited near or perhaps on the host rather than in it. Hence,
these ectoparasitoids usually attacked concealed hosts, often within galleries
in wood or plant galls. The use of venom apparently developed very early and
produced physiological changes in the host. While the venom of the more an-
cestral ectoparasitoids resulted in idiobiosis (permanent paralysis or death), the
venom of the more specialized endoparasitoids tended toward koinobiosis (tem-
porary or nonlethal paralysis). However, it is not clear whether endoparasitism
preceded koinobiosis or vice versa (33). Of related interest is the evolution
of teratocytes or “giant cells” with nutritive and secretory functions that some-
times cause pathologies, then viruses and virus-like particles that can overcome
immune responses, and finally polyembryony, in which many embryos develop
from a single egg.
HYPERPARASITISM According to Godfray (33), “facultative” hyperparasitism
perhaps evolved from ectoparasitism because no special adaptations are needed
to oviposit and feed on a primary parasitoid as well as the primary’s host.
“Obligate” hyperparasitism has a wide taxonomic distribution and could have
evolved in at least two ways: (a) via facultative hyperparasitism as an oppor-
tunistic trade-off to utilize primary or secondary hosts, and/or if the hyper-
parasitic species frequently encounters already parasitized hosts; or (b) by a
host shift from a primary parasitoid of one host to a secondary parasitoid of
another species. This host transfer is facilitated if the old primary and new
secondary hosts share physiological and/or ecological attributes. Finally, some
hyperparasitoids are ectoparasitic whereas others are endoparasitic, and some
are idiobionts whereas others are koinobionts (10).

NON-APHID HYPERPARASITISM
This section reviews hyperparasitism in insect hosts other than aphids and is
presented in descending order of literature citations by major taxa with selected
examples of current research on more common multitrophic relationships and
interesting behaviors, with special reference to the impact of hyperparasitism
on biological control.
Lepidoptera
GYPSY MOTH Lymantria dispar (Lymantriidae) is an exotic insect defoliator
of trees in North America, against which classical biological control has been
used over many years. It is attacked by a number of introduced hymenopterous
primary parasitoids, such as Cotesia (= Apanteles) melanoscela (Braconidae),
Brachymeria intermedia (Chalcididae), and Ooencyrtus kuvanae (Encyrtidae).
In the case of C. melanoscela, their cocoons in turn are attacked by as many
as 16 indigenous hyperparasitoid species, sometimes resulting in an average of
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50–90% primary mortality, which can interfere with biological control (11, 24).
A nondiapausing Asian strain decreases its exposure time and, hence, reduces
its vulnerability to hyperparasitism (78, 132, 133). A tachinid fly, Ceranthia
samarensis (Diptera:Tachinidae), was imported into Canada from Europe and
is the predominent parasitoid in low-density populations of gypsy moths while
suffering 7–16% hyperparasitism (69).
LEAFMINERS Phyllonorycter crataegella (Gracillariidae) on pin cherry and
Phyllonorycter propinquinella on black cherry have parasitoid fauna similar to
that of apple leafminers (62). However, of the parasitoids that emerged from
these leafminers, nine species were primary parasitoids, and seven were facul-
tative hyperparasitoids. Both cherry leafminers are alternate hosts for parasitoid
species that attack economically important apple leafminers, but obligate hy-
perparasitoids do not seem to be important.
GREEN CLOVERWORM In the soybean canopy, the green cloverworm, Plathy-
pena scabra (Noctuidae), is parasitized by Cotesia marginiventris (Hymenop-
tera: Braconidae), which is hyperparasitized by Mesochorus discitergus (Hyme-
noptera: Ichneumonidae). The hyperparasitoid must hang by its tarsi from the
edge of the leaf from which the larva is suspended, and then it reels in the
caterpillar by pulling upward on the caterpillar’s silken thread. Hyperparasitoid
pupation occurs within the cocoon spun by the primary parasitoid (137a).
CABBAGE BUTTERFLY Pieris rapae (Pieridae) is attacked by the gregarious
parasitoid, Cotesia glomerata (Hymenoptera: Braconidae). Emergence of adult
hyperparasitoids, Eurytoma sp. (Hymenoptera: Eurytomidae), from the oldest
cocoon clusters was found to be strongly male biased, while the sex ratio from
young cocoons was in favor of females (108).
SPRUCE BUDWORM An extensive study was done by Huber et al (48) on 28
genera representing 10 families of at least 50 chalcidoid parasitoids and hy-
perparasitoids recorded from Choristoneura fumiferana (Tortricidae) and other
Choristoneura spp. in New Brunswick, Canada. Primary parasitoids belonging
to the Ichneumonidae, Braconidae, and Tachinidae were recorded from 10 of
the 16 Nearctic Choristoneura spp., but chalcidoid hyperparasitoids were from
only 4 of the 16 species.
STEM BORERS Tetrastichus howardi (Hymenoptera: Eulophidae) is a gregar-
ious endoparasitoid introduced into South Africa as a biological control agent
against stem borers. Chilo partellus (Pyralidae) and Helicoverpa armigera
(Noctuidae) were preferred by T. howardi and so behaved as a polyphagous
facultative hyperparasitoid rather than as an obligate hyperparasitoid on their
primary parasitoids. When one lepidopteran pupa was parasitized by a single
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T. howardi female, about 55 progeny emerged, of which 94% were females

(70, 71).

EUCALYPTUS MOTH In South Australia, Uraba lugens (Noctuidae) on several

species of eucalyptus was attacked by 11 primary parasitoids and 10 hyperpar-
asitoids (one of which was facultative). Of these hyperparasitoids, many were
gregarious and polyphagous, and all but one species parasitized the pupae of the
primary parasitoids. Hyperparasitism and the presence of many polyphagous
primary parasitoids in the complex perhaps contributed to the low levels of
parasitism of U. lugens (2).

TRIGONALYID WASPS Weinstein & Austin’s (127, 128) studies of the relation-
ship of the enigmatic trigonalyid wasps (Hymenoptera: Trigonalyidae) with
their hosts indicated that most species appear to oviposit on a wide variety of
plants. Their eggs are ingested in most cases by lepidopteran or sawfly larvae,
and they then develop as obligatory hyperparasitoids in tachinid or ichneumonid
primary parasitoids or in vespid or eumenid wasp larvae. Vespidae are the most
commonly recorded secondary hosts, perhaps via lepidopteran primary hosts
provisioned into nests.

TUFTED APPLE BUD MOTH Platynota idaeusalis (Tortricidae), a pest in apple

orchards, has 41 primary parasitoids, with Exochus atriceps (Hymenoptera:
Ichneumonidae) as the most common. Only two hyperparasitoid species emer-
ged with no major impact noted (9).

SCALE INSECTS AND WHITEFLIES Scale insects and whiteflies are phytopha-
gous pests in the order Homoptera. They are often hosts in an unusual relation-
ship of multitrophic ecology and behavior unique to the hymenopterous family
Aphelinidae, which had been reviewed by Viggiani (116).

HETERONOMOUS HYPERPARASITISM Heteronomous hyperparasitism is also

called facultative autoparasitism and adelphoparasitism. Females develop nor-
mally as primary endoparasitoids of Homoptera, whereas males develop hy-
perparasitically in primary endoparasitoids, including their own conspecific
females (68, 117, 134). Abnormal behavior or deviant male ontogeny is as-
sociated with sex differentiation in the host relations of some species in such
genera as Aneristus, Coccophagus, Coccophagoides, Euxanthellus, Encarsia,
Lounburyia, Physcus, and Prococcophagus. This highly evolved mode of de-
velopment results in linkage with progeny sex ratio. Field sex ratios of het-
eronomous hyperparasitoids can fluctuate dramatically depending on changes
in the relative availability of male and female hosts (136).
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SCALE INSECTS Second instar scales of Filippia gemina are the preferred
hosts for the larvae of the female aphelinid Coccophagus atratus. Late larval
instars and prepupae of the conspecific C. atratus are the preferred hosts of
male C. atratus larvae. Variable population sex ratios observed in C. atratus
apparently result from the behavior of individual females, in which brood sex
ratios are dependent on the relative availability of hosts for males and hosts for
females (23).
When another aphelinid, Encarsia tricolor, was offered pupae of Encarsia
inaron or conspecific pupae, E. tricolor showed a distinct preference to exploit
E. inaron for male production (134). In complexes of parasitoids containing
a heteronomous hyperparasitoid and one or more conventional species, in the
majority of cases, the heteronomous hyperparasitoid was the most important and
dominant species. Hence, caution is necessary when using such parasitoids in
classical biological control programs (135). Three forms of Encarsia perniciosi
are recognized by Stouthamer & Luck (102) based on their mode of reproduction
and host choice: a thelytokous form parasitizing California red scale, Aonidiella
aurantii, and both a thelytokous and an arrhenotokous form parasitizing San
Jose scale, Quadraspidiotus perniciosus. The arrhenotokous E. perniciosi is a
heteronomous hyperparasitoid, and it had been suggested that the arrhenotokous
form would become thelytokous in one generation when cultured under constant
temperatures in the laboratory. However, this was not found to be the case in four
cultures under constant temperatures after 2, 3, 11, and 19 generations (102).

WHITEFLIES A tritrophic model of heteronomous hyperparasitism was used

in a cotton–whitefly-parasitoid system by Mills & Gutierrez (68). Male aphe-
linid parasitoids develop at the expense of conspecific females or competing
parasitoid species. The unresolved question is whether such heteronomous
hyperparasitism is compatible with the goals of biological control. Three aphe-
linid parasitoids were considered: (a) a typical primary parasitoid (where both
males and females develop on whitefly hosts), (b) an obligate autoparasitoid
(where males develop only on conspecific females), and (c) a facultative au-
toparasitoid (where males develop on all other parasitoids including conspecific
females). Results indicate that the combination of a primary parasitoid and an
obligate autoparasitoid provides the greatest suppression of cumulative whitefly
abundance. In contrast, the addition of a facultative autoparasitoid disrupts the
control potential of the other parasitoids. Hence, the indiscriminate introduction
of aphelinid parasitoids in biological control programs should be avoided when
some are facultative autoparasitoids. Encarsia formosa (Hymenoptera: Aphe-
linidae) is a parasitoid used worldwide for the biological control of whiteflies
on vegetables and ornamental plants grown in greenhouses (43). It is hyper-
parasitized by Signiphora coquilletti, Encarsia pergandiella, and E. tricolor
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298 SULLIVAN & VÖLKL

(6, 15, 137). Models suggest that the efficacy of biological control is reduced if
heteronomous hyperparasitoids (such as E. pergandiella, E. tricolor) are used
together with primary parasitoids such as E. formosa (69; see also 82, 84; see
AC Bellotti et al, this volume).
Mealybugs
CASSAVA MEALYBUG The history and success in Africa of a classical biolog-
ical control program to protect cassava (Manihot esculenta) from the South
American mealybug (Phenacoccus manihoti) has been reviewed by Herren
& Neuenschwander (42). The most effective of the primary parasitoids was
Apoanagyrus (=Epidinocarsis) lopezi (Hymenoptera: Encyrtidae), which was
introduced from Paraguay into Nigeria in 1981. Even some defensive behavior
by the cassava mealybug involving encapsulation and melanization of the wasp’s
eggs and larvae did not prevent biological control of this pest (106). At least
10 indigenous hymenopterous hyperparasitoids adapted to this new exotic pri-
mary in Africa: Chartocerus hyalipennis (Signiphoridae) and Prochiloneurus
insolitus were the most common hyperparasitoids, followed by Prochiloneurus
aegyptiacus (Encyrtidae), Tetrastichus sp. (Eulophidae), and Marietta leopar-
dina (Aphelinidae) (1, 80). The rate of hyperparasitism varied considerably
(20–90%). Yet, in spite of sometimes high hyperparasitism, no detrimental ef-
fect on the control efficiency of A. lopezi was noticed (51, 79). Special field and
laboratory studies on the biology and impact of Chartocerus and Prochiloneu-
rus spp. confirmed that these hyperparasitoids did not significantly reduce
A. lopezi’s success (34, 35).
MANGO MEALYBUG In the early 1980s, the mango mealybug, Rastrococcus
invadens, was accidentally introduced into Togo, causing serious damage on
mango (Mangifera indica), citrus, other fruit, and even shade trees. As part of
a biological control program, a primary parasitoid was introduced from India,
Gyranusoidea tebygi (Hymenoptera: Encyrtidae), and became established in
Togo and most of West Africa (79). Although, at times, 50–60% of G. tebygi
mortality was attributable to eight species of hyperparasitoids, this still did not
seem to prevent successful control of the mango mealybug (65).
DIPTERA The recent review of Diptera as parasitoids by Feener & Brown (29)
compared them with the Hymenoptera and pointed out that the Diptera use
a wider array of hosts (22 orders across five phyla) than any other group of
parasitoids. In contrast, hosts of the more diverse parasitic Hymenoptera are
restricted to 19 orders, all within the single phylum Arthropoda. Most dipteran
parasitoids are koinobionts and endoparasitoids. Superparasitism (ovposition
in a host already parasitized by a female of the same species) appears to be both
widely distributed across dipteran species and common within populations, as
reported in Conopidae, Phoridae, and Tachinidae.
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GALL-MAKERS Hawkins & Goeden (40), Hawkins & Sheehan (41), and Craig
(21) have pointed out that multitrophic ecology and the related behavior of
the phytophagous and entomophagous insect community are especially well
demonstrated with dipteran gall-makers. In Florida, Stiling & Rossi (101)
studied the dipteran midge Asphondylia borrichiae (Cecidomyiidae), which
induces the formation of galls on three different plant species: sea oxeye daisy
(Borrichia frutescens), marsh elder (Iva frutescens), and beach elder (Iva imbri-
cata). The dipteran gall-maker is attacked by four main species of hymenopteran
parasitoids. Two of these parasitoids, Torymus umbilicatus (Torymidae) and
Galeopsomyia haemon (Eulophidae), are ectoparasitic and facultatively hy-
perparasitic (Figure 1). They were the dominant species because the two other
parasitoids are primaries only and endoparasitic: Rileya cecidomyiae (Euryto-
midae) and Tenuipetiolus teredon (Eurytomidae). As endoparasitic primaries,
they are available for attack by the two ectoparasitoids when behaving as facul-
tative hyperparasitoids. However, gall size is also important in the further com-
petition between these two ectoparasitic and facultative hyperparasitoids. One

Figure 1 Multitrophic ecology and behavior of the parasitoids and hyperparasitoids associated
with the dipteran gall-maker Asphondylia borrichiae. Redrawn from Stiling & Rossi (101), with
permission from Oxford University Press.
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300 SULLIVAN & VÖLKL

of these, G. haemon, displaces the other hyperparasitic species, T. umbilicatus,

in small galls. But T. umbilicatus has a much longer ovipositor than G. haemon,
enabling it to oviposit later as galls grow in size. As a result, T. umbilicatus has
a competitive advantage in larger galls.

LEAFMINERS The dipteran honeysuckle leafminer, Chromatomyia suikasurae

(Agromyzidae), in a natural forest in Kyoto, Japan, was found to have a com-
plex of primary parasitoids, of which 3 were koinobiont (all larval-pupal soli-
tary) and 22 idiobiont species (11 larval solitary, 9 pupal solitary, and 2 pupal
gregarious). Although competition among these primaries contributed to low
emergence rates of parasitoids at high host densities, these primary parasitoid
rates were also reduced at low host densities, probably by inter- and intraspecific
hyperparasitism (54).

DROSOPHILIDAE A facultative hyperparasitoid, Pachycrepoideus vindemiae

(Hymenoptera: Pteromalidae), attacks both as a primary parasitoid on Droso-
phila melanogaster and as a hyperparasitoid on the primary Asobara tabida
(Hymenoptera: Braconidae) (85).

BOMBYLIIDAE Unlike most of the dipteran parasitoids, bombyliids are ec-

toparasitoids. Hyperparasitism on dipteran parasitoids as hosts seems uncom-
mon, but there are some records of hyperparasitism by bombyliid parasitoids
(in genera of Anthracinae) on primary hosts (138). However, all bombyliids
recorded as hyperparasitoids do not appear to have evolved in any close associa-
tion with the primary host and are best termed “pseudohyperparasitoids”—with
both facultative and obligate hyperparasitic behaviors existing.

Wasps and Bees

CYNIPID GALL-MAKERS The wasp pest Dryocosmus kuriphilus (Hymenoptera:
Cynipidae) induces galls in chestnut orchards in Japan. An imported parasitoid,
Torymus (= Syntomaspis) sinensis (Hymenoptera: Torymidae), was released in
1982 in Kumamoto Prefecture, but disappointingly, the population had not in-
creased at the rate expected. As a result, the density of the host cynipid pest
has not yet decreased but instead continues to fluctuate at too high a level. Two
factors were suggested to have delayed the success of the introduced para-
sitoid: the low female sex ratio and high mortality rate due to native facultative
hyperparasitoids (75, 76).

LEAFCUTTER BEES The fly Physocephala vittata (Diptera: Conopidae) is a

pest of beneficial pollinating alfalfa leafcutter bees, Megachile rotundata
(Hymenoptera: Megachilidae), in the former Yugoslavia. A hyperparasitoid,
Habrocytus eonopidarum (Hymenoptera: Pteromalidae), emerged from pupae
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of P. vittata in the laboratory, indicating that biological control of this fly pest
is a possibility (67).

SAWFLIES Sometimes sawflies’ primary parasitoids in Australia (127, 128)

and in Eurasia (87) are in turn attacked by facultative hyperparasitoids.

Psyllids
PEAR PSYLLA Psylla pyri (Homoptera: Psyllidae) is the key pest in pear
orchards in France and many European countries. Trechynites psyllae (Hy-
menoptera: Encyrtidae) is the main primary parasitoid regulating the pest from
the first generation. Hyperparasitism, essentially due to Syrphophagus mami-
tus (Hymenoptera: Encyrtidae), appears later on another host species, Psylla
pyrisuga, which acts as a relay species for primary parasitoids between the
first and second generation of P. pyri. Five other hyperparasitoids appear even
later. Because hyperparasitism is not recorded on the first generation of P. pyri,
early release of primary parasitoids should be successful in reducing pest
populations (3).

HAWTHORN PSYLLIDS Ant attendance on larval parasitism was studied in

three species of hawthorn psyllids (Cacopsylla peregtina, Cacopsylla mela-
noneura, Cacopsylla crataegi). All three psyllid species had low parasitization
rates by two encyrtid primaries. However, the ant-attended C. crataegi was
almost exclusively parasitized by only one primary: Prionomitus mitratus. The
two other psyllid species that were not ant attended were attacked mainly by
Prionomitus tiliaris. In addition, the dominant hyperparasitoid, Pachyneuron
muscarum (Hymenoptera: Pteromalidae), was most successful on the two psyl-
lid species unattended by ants. Hence, the primary parasitoid benefited from
ant attendance of its psyllid host, C. crataegi, since honeydew-collecting ants
provided it with protection from hyperparasitoids (81).

Coleoptera
COCCINELLID BEETLES The European ladybird beetle, Coccinella septem-
punctata, was introduced into the eastern United States during the 1970s. The
literature and recent North American collection records indicate that at least 16
species of insects (ca 14 Hymenoptera from six families, and 2 Diptera from
two families) are now known as primary parasitoids and hyperparasitoids, such
as Tetrastichus spp., Pachyneuron spp., etc (91).

WEEVILS Two weevil stem borers (Curculionidae) on Rumex crispus differed

in their feeding position. Apion miniatum inhabited the lower 10% of the stem,
while Apion violaceum occurred all along the stem, thus exploiting distinctly
different feeding positions, partly owing to differences in time of oviposition.
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302 SULLIVAN & VÖLKL

A. miniatum suffered less parasitization than A. violaceum because its feeding

position in basal, thick parts of the stem constitutes a refuge as the stem diameter
increases. Koinobiont endoparasitoids attack the weevils before they enter the
stem (unlike idiobiont ectoparasitoids), and they benefit from the refuge itself
by avoiding hyperparasitism (32).
BRUCHID BEETLES Two species of beetles, Callosobruchus maculatus and
Bruchidius atrolineatus (Bruchidae), are attacked by two solitary primary ec-
toparasitoids: Dinarmus basalis (Hymenoptera: Pteromalidae) and Eupelmus
vuilleti (Hymenoptera: Eupelmidae). In behavioral contrast to D. basalis,
E. vuilleti concentrates ovipositions on hosts already parasitized by the former
and aggressively kills eggs and larvae of D. basalis by thrusts of the ovipos-
itor, resulting in ovicide and larvicide. However, E. vuilleti can also act as a
facultative hyperparasitoid on older larvae of D. basalis (110).

HYPERPARASITISM IN APHID PARASITOIDS

Primary aphid parasitoids are found in two families of Hymenoptera: the Aphi-
diidae (=Braconidae: Aphidiinae) (all genera of this family) and the Aphe-
linidae (genus Aphelinus and related genera). They in turn are attacked by a
species-rich community of hyperparasitoids (104, 105). The members of this
community belong to different hymenopteran subfamilies [Cynipoidea (Al-
loxystidae: Alloxysta, Phaenoglyphis, Lytoxysta), Ceraphronoidea (Megaspili-
dae: Dendrocerus), and Chalcidoidea (Pteromalidae: Asaphes, Pachneuron,
Coruna, Euneura; Encyrtidae: Syrphophagus = Aphidencyrtus)] (66, 104, 105,
109) and represent various life-history strategies. Alloxysta, Lytoxysta, and
Phaenogplyphis spp. develop as koinobiont endohyperparasitoids and para-
sitize the primary parasitoid larva within the living aphid (37, 63, 64, 95, 96,
104, 105). Syrphophagus (= Aphidencyrtus) aphidivorus develops also as a
koinobiont endohyperparasitoid, but females display a dual oviposition behav-
ior by attacking parasitoid larvae both within living aphids and also inside aphid
mummies (53, 105). Dendrocerus spp. and all pteromalid species develop as
idiobiont ectohyperparasitoids. Females attack parasitoid prepupae and pupae
inside the empty aphid cuticle, which is called an aphid mummy (8, 10, 16, 55,
103, 104).
Reproductive Potential
The few studies on life-table characteristics of aphid hyperparasitoids suggest
a relatively low lifetime fecundity when compared with those of primary par-
asitoid species. Singh & Srivastava (97) reported that females of Alloxysta
pleuralis, a hyperparasitoid of Trioxys indicus via Aphis craccivora, laid on
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HYPERPARASITISM: ECOLOGY–BEHAVIOR 303

average 113 eggs, with a daily maximum of about 30 eggs. Dendrocerus car-
penteri females produced on average 75 offspring, with a daily maximum of 10
eggs, with Aphidius ervi via Acyrthosiphon pisum being the host (125). By con-
trast, the fecundity of Asaphes species seems to be somewhat higher. Asaphes
suspensus females laid on average 432 eggs, with a maximum of 16 mum-
mies per day when the host was Aphidius uzbekistanicus via Sitobion avenae
(19). Lifetime fecundity and longevity reported for Asaphes vulgaris varied for
different host species. Estimates range from 51 offspring per female, a daily
maximum of 9 eggs, and an average longevity of 14 days [host: Lysiphlebus
cardui via Aphis fabae (61)] to 265 offspring per female, a daily maximum of
10 mummies per day, and an average longevity of 47 days [host: A. uzbekistan-
icus via S. avenae (19)] and 1433 offspring per female, 20 mummies per day,
and an average longevity of 46 days [host: Aphidius nigripes via Macrosiphum
euphorbiae (13)].

Sex Ratio and Offspring Sex Allocation

Offspring sex allocation and sex ratio variation was intensively studied for
D. carpenteri. Mated females are able to produce “precise” sex ratios by ad-
justing the sequence of male (=unfertilized) and female (=fertilized) eggs laid
during a single oviposition bout (18). In laboratory studies, the first egg to be
laid was fertilized if the host was of high quality (=large mummies) but un-
fertilized if the host was of low quality (=small mummies). The second egg
usually had the opposite sex. Later ovipositions varied with host quality, with
more fertilized eggs being laid in high quality hosts (18). This pattern may ex-
plain sexual size dimorphism. Although immatures of both sexes gain weight
at the same rate, males of D. carpenteri are generally smaller than females
(60, 83). Thus, it should be advantageous for D. carpenteri females to allocate
more female progeny in large hosts, which provide more resources for develop-
ment. Female age had apparently no effect on sex allocation (125). The results
of these laboratory studies are consistent with field collections, where the pro-
portion of females depended also on host size, varying between approximately
50% in small A. pisum mummies and 75% in large A. pisum mummies (59).
By contrast, there is only very little information about sex ratios in other aphid
hyperparasitoids. Singh & Srivastava (98) reported for Alloxysta pleuralis a sex
ratio of approximately 60% females, which was independent of the number of
eggs laid. In Asaphes vulgaris, the proportion of male progeny increased with
the age of females (13). Across host species, the sex ratio of A. vulgaris seems
to be a result of host size. Field studies revealed a female biased sex ratio in
large host species, while there was an extreme male bias in small host species
(Table 1), as has been reported for many other species of Hymenoptera.
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304 SULLIVAN & VÖLKL

Table 1 Sex ratio (proportion of females) in field samples of the aphid ectohyperparasitoid
Asaphes vulgaris collected near Bayreuth, Bavaria, Germanya

Primary parasitoids Aphid species Sex ratio

(mummy size) (number mummies) Host plant (females)

Small
Lysaphidus arvense Coloradoa tanacetina (89) Tanacetum vulgare 0.12
Lysiphlebus cardui Aphis fabae (312) Cirsium arvense 0.14
Trioxys angelicae Aphis fabae (122) Evonymus europaeus 0.19
Lysiphlebus hirticornis Metopeurum fuscoviride (76) Tanacetum vulgare 0.22
Trioxys falcatus Periphyllus sp. (38) Acer campestre 0.26
Medium
Euaphidius setiger Periphyllus sp. (26) Acer platanoides 0.35
Aphidius funebris Uroleucon jaceae (116) Centaurea jacea 0.38
Aphidius absinthii Macrosiphoniella absinthii (58) Artemisia vulgaris 0.41
Aphidius absinthii Macrosiphoniella tanacetaria (77) Tanacetum vulgare 0.45
Large
Aphidius rosae Macrosiphum rosae (156) Rosa sp. 0.58
Aphidius funebris Uroleucon cirsii (56) Cirsium arvense 0.64
Aphidius ervi Acyrthosiphon pisum (32) Trifolium pratense 0.69
Pauesia picta Cinara pinea (77) Pinus sylvestris 0.83
a
Primary parasitoids are divided according to mummy size into small-, medium-, and large-sized hosts
(W Völkl, unpublished data).

Host and Habitat Specificity

Generally, externally feeding idiobiont ectohyperparasitoid species need less
physiological adaptations for survival on a living host (such as a mechanism
to overcome the host’s immune system) than koinobiont endohyperparasitoid
species do. Host specificity is much more pronounced in endoparasitic species
than in ectoparasitoid species, and species richness is also higher in endopar-
asitoids (for reviews, see 33, 39, 88). The aphid hyperparasitoid community
presents an excellent example for this general pattern and is discussed below.
In Europe, the genera Dendrocerus (6 spp.), Asaphes (2 spp.), Pachyneuron
(4 spp.), Coruna (1 spp.), and Euneura (2 spp.) comprise altogether 15 species
developing as ectohyperparasitoids of aphids. Of these, 11 species have a very
broad host range and attack various aphidiid genera and species, independent
of the aphid host (22, 30, 36, 99, 105). Only Pachyneuron gibbiscuta and
Euneura laeviuscula are host specific, each of them having been reported up
to now from only a single primary parasitoid species (72, 74). Two other species,
Dendrocerus liebscheri (the only gregarious aphid hyperparasitoid) and
Euneura augarus, seem to be habitat specific, having been reported only from
field samples of conifer lachnids (30, 57, 77, 99, 120).
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HYPERPARASITISM: ECOLOGY–BEHAVIOR 305

By contrast, endohyperparasitic species are much more numerous: more than

50 described species and a number of undescribed or cryptic species, especially
within the genus Alloxysta (26, 27, 44). There are only a few species attacking a
broad range of unrelated aphid and primary parasitoid hosts, such as Alloxysta
victrix and Phaenoglyphis villosa (25). The vast majority of the species, how-
ever, seem to be host specific, attacking either a specific aphid host independent
of the primary parasitoid or a single primary parasitoid genus independent of
the aphid host. An example of the first strategy is from Phaenoglyphis stricta,
which is restricted to various aphidiid parasitoids of the genus Uroleucon on
various host plants (124). Examples for primary parasitoid–specific alloxystid
species are Alloxysta circumscripta, a hyperparasitoid of various Praon spp. on
different aphid hosts and host plants; Alloxysta pallidicornis, a hyperparasitoid
of Pauesia spp. via Cinara spp.; Alloxysta darci, a hyperparasitoid of Apheli-
nus spp.; and Alloxysta castanea, which attacks Praon volucre via Hyalopterus
pruni (17, 25, 26, 28, 120).
This host specificity is also reflected by the composition of faunistic com-
plexes. In native systems, host-specific alloxystid wasps are usually the most
abundant hyperparasitoids, while generalist ectohyperparasitoids, especially
Asaphes spp. or D. carpenteri, are dominant in exotic systems that have been
established after the introduction of a primary parasitoid (73, 100, 107, 111,
112, 118, 124, 139–141).

Foraging Behavior
Little information is available on foraging behavior and the cues involved in
host location. Generally, aphid honeydew may represent an unspecific cue pro-
viding information on the presence of aphids on the particular host plant after
the female’s arrival. Honeydew accumulation leads to increased residence times
in females of A. victrix, P. villosa, and D. carpenteri (14) and might be respon-
sible for an increase in hyperparasitoid foraging effort and foraging success on
contaminated plants.
The majority of the alloxystid species are host specific, and a cue like hon-
eydew may provide only limited information. There are two possible strate-
gies that might be applied that are not mutually exclusive. First, females may
search for primary parasitoid females. Indeed, females of Alloxysta fuscicor-
nis (= Alloxysta brassicae) responded positively in olfactometer experiments
to the presence of females of their host, Diaeretiella rapae (89). This strat-
egy would assure that females arrive in patches with an available resource but
may confront the alloxystid female with the problem of arriving too early; the
primary’s progeny will be available for oviposition only 3–4 days after ovipo-
sition, a time interval exceeding by far the known patch times of alloxystid
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306 SULLIVAN & VÖLKL

females, both in the presence and absence of primary parasitoid females (121,
123). Thus, this foraging strategy by such an endohyperparasitoid might not be
very successful in the field. Second, females may search for host plant volatiles
and use them, potentially in combination with the presence of aphid honeydew,
as reliable information about the potential occurrence of hosts. After the arrival
in an aphid colony, the female would have to acquire information about (a)
the kind of aphid host and (b) the presence of parasitized individuals. Singh
& Srivastava (94) showed that A. pleuralis females were attracted to foliage
extracts of potential host plants. After the arrival on a host plant, females distin-
guished between host (=parasitized) and nonhost aphids by ovipositor contact
(93, 95, 96). This strategy might explain some extreme host specificities, such
as in A. castanea, which attacks only P. volucre via H. pruni only on the winter
host, Prunus spinosa. A simple searching strategy restricted to cues arising
from the host plant, which is not attacked by other hosts of P. volucre, might
explain why A. castanea does not attack P. volucre on reeds, the summer host of
H. pruni.
By contrast, ectohyperparasitoids with a broad host range depend less on
specific cues for foraging, since their hosts may occur on a broad variety of
host plants. A. vulgaris is obviously using kairomones arising from the silky
cocoon of aphidiid primary parasitoids for host finding (20), and probably
females may use this cue also for locating mummies on a given host plant.
Since larvae of aphelinid species (the other hymenopterous family of aphid
primary parasitoids) do not produce silk for pupation, the low incidence of
hyperparasitism in Aphelinus spp. by Asaphes spp. (45) may be explained by
the missing kairomone (20).
D. carpenteri, the most polyphagous aphid hyperparasitoid species, does
not seem to respond to any cues from hosts or host plants. Females did not
respond to differently colored or differently shaped mummies (18), except for
Praon mummies (18a). They searched with the same efficiency during nocturnal
and diurnal conditions (122) and were only slightly influenced by insecticide
residues (58). Furthermore, residence times did not differ significantly between
differently structured plants without aphid mummies and between mummy-free
and mummy-containing plants, as long as no hosts were found (56, 92). Females
are searching at random on a host plant, a behavior also known for some other
parasitoid species with a broad host or host plant spectrum (113, 114). The
strategy of random search might be successful, since the hosts of D. carpenteri
may occur on a broad variety of differently structured host plants where their
density and distribution is unpredictable (74).
In petri dishes, hyperparasitoid foraging may also be influenced by encoun-
ters with primary parasitoids that are also foraging in aphid colonies (46, 47).
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HYPERPARASITISM: ECOLOGY–BEHAVIOR 307

By contrast, females of the primary parasitoids Aphidius funebris and L. cardui

did change their behavior after encounters with Alloxysta brevis, A. victrix, and
D. carpenteri when foraging in aphid colonies on plants (but the reverse was
not observed), which suggests that the proximate effect on oviposition behavior
and resource exploitation of aphidiids is negligible (123). However, as one of
the most important mortality factors, it is likely that hyperparasitism may have
had an ultimate effect on the evolution of the foraging strategies of aphidiid
wasps (7, 61, 129).
Also, the behavior of parasitized aphids to leave the aphid colony before
mummification has been suggested as an example of host manipulation by the
primary parasitoid to reduce the risk of hyperparasitism after mummy formation
(12). However, most primary parasitoids suffered less from hyperparasitism
within aphid colonies than outside (74). Therefore, alternative explanations are
more likely to explain this behavior (33, 74).

Ants and Hyperparasitism

Aphid colonies are often attended by honeydew-collecting ants, which defend
their carbohydrate source against colony intruders (126). Like many other in-
sect species, foraging females of all aphid hyperparasitoid species are heavily
attacked and regularly killed by ant workers (50). The presence of ants leads
to a significant reduction in hyperparasitoid foraging success, thereby providing
a kind of “enemy-free” space for the primary parasitoid (81, 119, 120). There
are several strategies among aphid hyperparasitoids to escape ant aggression.
Alloxystid species have evolved a chemical defense, which enables specialized
species to exploit ant-attended resources to a certain degree. A. brevis releases
a mandibular gland secretion, which contains 6-methyl-5-hepten-2-one, actini-
din, and unidentified iridoids in response to an attack of the ant Lasius niger
(121). This secretion functions both as a measure of self-defense if the female is
seized by an ant worker and as a repellent that prevents ant attacks during sub-
sequent encounters. It enables A. brevis females to hyperparasitize ant-attended
aphids that constitute a major proportion of their hosts and significantly reduces
mortality by ectohyperparasitoids (103, 121). D. carpenteri can avoid ant con-
tacts by quick and flexible movements, thereby mainly using visual cues. This
strategy is very successful against Myrmica laevinodis but less effective during
interactions with L. niger (50). Obviously, D. carpenteri is also able to change
its behavior after an aggressive ant contact. Females that survived an attack by
L. niger recognized ant workers by their odor and avoided any contacts with
them during the next few hours (49). The benefit of this “avoidance learn-
ing” may be sought in the nocturnal activity of this species, when neither
hyperparasitoid nor ant is able to respond to visual cues in their environment.
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308 SULLIVAN & VÖLKL

Syrphophagus aphidivorus, Pachyneuron aphidis, A. vulgaris, and Euneura

stomaphidis possess jumping ability and were hardly exposed to mortality risks
in experimental studies (50, 52).

CONCLUSIONS
Hawkins (39) notes that evolution at the fourth trophic level often measures
hyperparasitoid species richness based on the number of species per herbi-
vore species. A positive relationship between the numbers of hyperparasitoid
species and primary parasitoids is not surprising, and species richness at these
trophic levels is therefore dependent on the biological and ecological charac-
teristics of the herbivores. In fact, the difficulty in sampling many ecosystems
probably results in an underestimation of the hyperparasitoid species. For in-
stance, most of the data come from rearings of phytophagous insects, with fewer
rearings of field-collected parasitoid cocoons that may have been attacked or
will be attacked by hyperparasitoids. Hence, a hyperparasitoid larva or pupa
could be developing in these uncollected cocoons, resulting in an undercount
of species diversity. Despite these shortcomings, the emerging patterns suggest
that hyperparasitoid community structure seems to follow the same organiza-
tion patterns as primary parasitoid communities. Many parasitoids are attacked
by generalist ectohyperparasitoids, and by more host-specific endoparasitoids.
Furthermore, host-specific hyperparasitoids seem to be generally more abun-
dant than unspecialized generalists, a pattern that is also found in primary
parasitoid communities (33, 39, 41, 88).
In contrast to hyperparasitoid community organization, more information on
hyperparasitoid foraging and on oviposition decisions might contribute to a bet-
ter explanation of the patterns of resource utilization. Most of our knowledge
comes from studies on a small-scale range, i.e. on patch level (14, 19, 46, 47,
49, 56, 83, 93, 121, 123), while there are virtually no studies that analyzed
hyperparasitoid foraging on a larger scale, for example, between patches on the
same plant, between plants, or between habitats (91a). Studies on a small-scale
range suggest, together with field data from biological control measures (61,
104, 112), that the impact of hyperparasitism on primary parasitoid popula-
tion dynamics may be overestimated, although hyperparasitoids can be clearly
identified as an important host mortality factor (90). Although there is no clear
evidence for density dependence at the patch level, we have no information
about such processes on a larger spatial scale. Studies on this topic should com-
bine field studies with an experimental laboratory approach, for example, by
using “microcosmos” systems, and should also include detailed examinations
of the cues involved in habitat and host location and of the importance of in-
teractions with adult primary parasitoids and with hyperparasitoid predators at
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HYPERPARASITISM: ECOLOGY–BEHAVIOR 309

the habitat level (61, 90, 104, 120). In general, such an analysis may help to
better understand individual patterns of resource utilization, which are one key
factor of hyperparasitoid population dynamics and its role in pest control.
Finally, as was mentioned in a review published in this series in 1987 by
Sullivan (104), it is standard quarantine procedure in biological control pro-
grams to exclude exotic obligate hyperparasitoids. Whether or not exotic fac-
ultative hyperparasitoids should be imported and released must be evaluated
separately for each candidate species depending on the availability of conven-
tional natural enemies and the seriousness of the insect pest problem. Most
researchers urge caution and advise a conservative policy in biological control
programs in order to exclude exotic facultative hyperparasitoids (130). Indige-
nous hyperparasitoids, on the other hand, already exist in the ecosystem and
usually cannot be eliminated even if they interfere (in varying degrees) with
biological control by exotic primary parasitoids.
ACKNOWLEDGMENTS
We thank G Hübner, P Kranz, and U Schwörer for sharing unpublished data and
P Stiling and AM Rossi (101) for permission to use their drawing (Figure 1),
as well as the editors (BA Hawkins and W Sheehan) and Oxford University
Press for use of this copyright material. M Romstöck-Völkl, G Hübner, M
Mackauer, and K Dettner provided helpful comments on the manuscript. The
German Research Council provided financial support to WV (DFG Vo 628/3-1).
Visit the Annual Reviews home page at
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