21 Oct 2003 20:38 AR AR208-EN49-02.tex AR208-EN49-02.

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10.1146/annurev.ento.49.061703.153618

Annu. Rev. Entomol. 2004. 49:27–49

doi: 10.1146/annurev.ento.49.061703.153618
Copyright °c 2004 by Annual Reviews. All rights reserved
First published online as a Review in Advance on July 16, 2003

FUNCTIONAL ECOLOGY OF IMMATURE

PARASITOIDS
Jacques Brodeur1 and Guy Boivin2
1
Département de Phytologie, Université Laval, Quebec, Canada G1K 7P4;
email: jacques.brodeur@plg.ulaval.ca
2
CRDH, Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, Quebec,
Canada J3B 3E6; email: boiving@em.agr.ca

Key Words host-parasitoid relationship, life history, host selection,

gregariousness, host behavior
■ Abstract Recently, there has been exciting progress in our understanding of the
behavioral and evolutionary ecology of immature parasitoids. Developing parasitoids
face a diversity of ecological constraints, and parasitism success involves decisions
and responses made by immature parasitoids to find a host and solve conflicts with five
potential antagonists: host, mother, siblings, competitors, and natural enemies. In this
review we synthesize and interpret results from studies on (a) the convergent evolution
of host selection behavior of first-instar larvae and females in hymenopteran, dipteran,
and coleopteran families; (b) the competitive interactions between larval parasitoids and
the evolution of gregariousness; (c) the susceptibility of parasitized hosts to predation;
and (d) the ability of parasitoids to manipulate the behavior of the host. We discuss how
ecological interactions between juvenile parasitoids and their hosts, competitors, and
natural enemies influence the evolution of parasitoid life-history strategies, and why
the integration of functional aspects of the ecology of immature parasitoids provides
a reliable framework for effective host-parasitoid population models and formulation
of biological control solutions.

INTRODUCTION

Successful parasitism by insect parasitoids is a complex achievement. The par-

asitoid must locate and evaluate the host, evade or overcome the host immune
response, and adapt to or regulate a constantly changing host environment to sat-
isfy the metabolic, nutritional, and ecological needs of the immature parasitoid.
Parasitoids from diverse origins have evolved a variety of strategies to exploit their
host, and understanding the underlying mechanisms, the ecological consequences
of host-parasitoid relationships, and the evolutionary processes has intrigued sci-
entists from different disciplines.
Host selection and progeny allocation by the female parasitoid have been in-
tensively investigated for decades, and we now have strong evolutionary and
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28 BRODEUR ¥ BOIVIN

mechanistic explanations for aspects of the reproductive strategy and foraging

behavior of adult parasitoids (43, 118, 122, 122a). Similarly, the molecular, bio-
chemical, and physiological interactions between host and parasitoid have been
the subject of considerable research and several recent reviews (9). Immature para-
sitoids are exploitative organisms that live in continuous, intimate association with
their host, and important advances have been achieved that characterize patterns
of parasitoid preimaginal development (71), notably optimal resource allocations
to adult body size and development time (50, 67, 111, 114), hormonal interactions
with the host (8, 9), and adaptations that promote parasitoid virulence (44).
Relatively few studies have focused on the behavioral and evolutionary ecology
of immature parasitoids. The paucity of information contrasts with the need to
understand the ecological interactions between juvenile parasitoids and their hosts,
competitors, and natural enemies. Obviously, immature parasitoids are more than
passive, saprophytic consumers of host tissues. They feed, grow, molt, fight, and
monopolize space in the host environment. Immature parasitoids are therefore
expected to have evolved morphological, ontogenic, and behavioral responses to
ecological constraints.
We restrict our review to four aspects of the functional ecology of immature par-
asitoids: the convergent evolution of host selection behavior of first-instar larvae
and females in hymenopteran, dipteran and coleopteran families; the competi-
tive interactions between larval parasitoids and the evolution of gregariousness;
the susceptibility of parasitized hosts to predation; and the strategies evolved by
immature parasitoids to avoid mortality by natural enemies. These aspects are
significant, as they comprise the major tasks and conflicts faced by juvenile para-
sitoids. Throughout, we have attempted to present both theoretical and empirical
work and to suggest some of the most rewarding directions for future research.

IMMATURE PARASITOIDS: AN OVERVIEW

Parasitoids occur in six holometabolous orders of insects with more or less com-
plex life cycles: Hymenoptera, Diptera, Coleoptera, Lepidoptera, Trichoptera, and
Neuroptera (43, 90). Hagen (48) remains a key reference for the morphological as-
pects of immature stages, providing a detailed description of egg, larval, and pupal
stages of the most common groups of parasitoids and suggesting adaptive functions
for some of the structures. Within the context of this review, first-instar larvae are
particularly fascinating, as their roles include host location, host evaluation, inges-
tion, respiration, competition, and protection. For other aspects of the morphology
of developmental stages of parasitoids we refer the reader to Quicke (90).
Most parasitoid females lay their eggs directly into or on the host, although
some lay eggs near the host. In the latter, parasitism may occur either when the egg
is consumed by the host or when the larva actively enters or is carried to the host by
phoresy (43). Consequently, parasitoid larvae may develop on (ectoparasitoids) or
in (endoparasitoids) their host, the latter is usually considered the derived condition
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ECOLOGY OF IMMATURE PARASITOIDS 29

(40). Furthermore, parasitoids may be classified as either solitary or gregarious if

one or several individuals develop within a given host, respectively.
The literature is peppered with specialist terminology describing unique aspects
of the biology and life history of parasitoids. One of the most useful functional
classifications is the idiobiont-koinobiont dichotomy, which describes alternative
modes of development (5, 47). Koinobiont parasitoids allow their host to continue
to feed, grow, and function after parasitism, whereas hosts attacked by idiobiont
parasitoids cease development immediately upon being parasitized or shortly there-
after. Idiobiont parasitoids include ectoparasites that permanently paralyze or kill
their hosts, as well as egg and pupal endoparasitoids. In contrast, koinobiont par-
asitoids typically develop as endoparasites of free-moving larval and adult hosts
and are physiologically constrained by the host in which they live, and their devel-
opment is finely tuned to that of the host. Several morphological, physiological,
and behavioral attributes of parasitoids correlate with the idiobiont-koinobiont
life-history strategies (39, 41, 71, 90), and the dichotomy has been especially in-
strumental in developing theories of parasitoid development (67, 111) and host
specificity (5).

HOST SELECTION BY FIRST-INSTAR LARVAE

We review the behaviors of immature parasitoids that have to locate, evaluate, and
enter the host, compare foraging patterns with those of adult female parasitoids,
and discuss the ecological implications of host selection by parasitoid larvae.

Convergent Evolution in Hymenoptera,

Coleoptera, and Diptera
The process of successful parasitism is generally divided into hierarchical steps
consisting of habitat location, host location, host acceptance, and host regulation
(118, 124, 125). For the majority of hymenopteran parasitoids, the first three steps,
and part of the fourth step, are the responsibility of the adult female and these
behaviors are likely to be under strong natural selection, as they determine the
fitness of the female (93). Oviposition decisions are affected by several factors
such as host quality, competition level, the number of eggs available, and the life
expectancy of the female parasitoid (23, 43, 45, 97, 117, 121, 126, 128). Numerous
models have been proposed to explain the relative impact of these factors on female
oviposition decision (20, 21, 49, 68).
For some hymenopteran [Perilampidae, Eucharitidae (Chalcidoidea), and Eu-
cerotinae (Ichneumonidae)] as well as most of the coleopteran, dipteran, lepi-
dopteran, neuropteran, and trichopteran parasitoids, host location and selection
are performed by the first-instar larvae (31, 43). The factors influencing host se-
lection have been considered irrelevant to host-seeking first-instar larvae because
they are unlikely to discover several hosts and therefore express a choice (34).
Although this is generally true, there are some interesting exceptions. In species
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30 BRODEUR ¥ BOIVIN

that parasitize aggregated hosts, host selection capability of first-instar larvae could
be important, as larvae have the possibility to encounter and evaluate several hosts.
Although larvae may face ecological constraints that differ from those of female
parasitoids, in all cases fitness will depend on their capacity to choose the best
host available. Therefore, predictions from models developed for adult parasitoids
could be tested, assuming that host-seeking first-instar larvae are the ecological
equivalent of parasitoid females with a short life expectancy, low mobility, and
only one egg to lay.
In most species where first-instar larvae seek hosts, the female retains some
of its responsibilities. Females may respond to host abundance and even to the
level of habitat exploitation by conspecifics (36). For larvipositing parasitoids the
females deposit larvae in locations likely to harbor potential hosts (34). Ambushing
a host and/or being carried by phoresy to the host are used by some hymenopteran,
dipteran, and coleopteran parasitoids. For example, the females of genera such
as Obeza and Pseudochalcura (Hymenoptera: Eucharitidae) oviposit in habitats
harboring ants. Following eclosion, the planidial larva waits for an ant to pass,
attaches itself, and is carried to the ant nest, where it parasitizes ant larvae and
pupae (54). In groups that evolved from predators, such as the genus Aleochara
(Coleoptera: Staphylinidae) (30), the campodeiform first-instar larva has functional
legs that enable active searching of the habitat for the presence of a host. In Diptera
and Hymenoptera the planidial larvae are legless, but other structures such as setae
and sternal spines have evolved to facilitate host-searching behaviors (34, 90).
Although host-seeking first-instar larvae are mobile, the time available and the
area that can be searched are considerably less than that for an adult female. Thus
the number of potential hosts encountered is lower, and in most cases once a
choice is made it is definitive. In a species such as Aleochara bilineata, campode-
iform first-instar larvae survive an average of five to six days in the laboratory
without feeding, but the probability of finding and entering a host puparium is
less than 50% after four days (99). In rare cases, such as the Bombyliidae Villa
brunnea, planidia can survive up to 25 days while searching for hosts (28). As-
suming that the consequences of choosing a poor host are highly detrimental for
juvenile parasitoids, any mechanisms that increase the capacities of first-instar
larvae to discriminate against inferior hosts should have been favored by natural
selection.
The ecology of host-seeking first-instar larvae rarely has been studied thor-
oughly with the exception of the genus Aleochara, whose first-instar larvae are
solitary ectoparasitoids of aggregated Diptera pupae. Almost all Aleochara species
have a parasitoid life style (31). Studying such species could provide evidence of
convergent evolution. Hymenopteran parasitoids all originate from one acquisition
of the parasitoid lifestyle (30), and therefore it is difficult to document separate
occurrences of a given adaptation to constraints typical of the parasitoid lifestyle.
In contrast, coleopteran and diptera parasitoids result from 14 and up to 100 ac-
quisitions, respectively (30). In these groups, morphological, behavioral, or phys-
iological adaptations similar to those found in hymenopteran parasitoids could be
considered examples of convergent evolution.
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ECOLOGY OF IMMATURE PARASITOIDS 31

Several aspects related to host evaluation and acceptance have been exten-
sively studied in hymenopteran species and are pertinent to the ecology of some
host-seeking first-instar larvae. These aspects include the effect of host quality
(including host discrimination), competition from conspecifics or other species,
age of the searching individual, and optimal time allocation while searching and
evaluating hosts.

Aspects of Host Evaluation and Acceptance

Female parasitoid fitness is correlated with the quality of the hosts in which her
progeny develops (43). Host quality varies according to several factors includ-
ing host species, size, age, sex, parasitization, and nutritional state. Few data are
available on the impact of these factors on host selection by first-instar larvae,
but we would expect that reduced mobility and low encounter rate of parasitoid
larvae diminish the importance of expending resources to evaluate the host. On
the other hand, because a host-seeking larva has only one opportunity of entering
a host and its entire fitness thus comes from a single host, as opposed to parasitoid
females that can spread their fitness gain over several hosts, the cost of choosing
a low-quality host is great. Therefore, host discrimination, which describes the
capacity of parasitoids to recognize parasitized hosts (119, 120), should be under
strong selective pressure and, if present, should rapidly spread in a population. The
campodeiform first-instar larvae of Aleochara species do choose their hosts on the
basis of factors such as the species, size, developmental stage, and parasitism sta-
tus (1, 38, 99). A. bilineata prefers host fly puparia of large to intermediate sizes,
whereas A. bipustulata prefers puparia of small size (1). For each species, there
are specific size limits, below which the larva has insufficient resources to com-
plete its development and over which the larva dies as the unconsumed host tissue
decomposes and the immature parasitoid dies (59).
Host discrimination confers a significant advantage to female parasitoids be-
cause parasitized hosts have a lower fitness value and, by avoiding them when
unparasitized hosts are available, females save both time and eggs (7). Host dis-
crimination by female parasitoids is common in Hymenoptera (119) but rare in
Diptera (34), although it was shown in two tachinid species (65). In host-seeking
first-instar larvae the value of host discrimination depends on the host encounter
rate and on the fitness gain expected from discriminating. When the probability of
encountering another host is lower than the probability of winning a competition
with the first occupant of the host, it is always more advantageous to accept the
first host encountered and host discrimination is not expected to evolve. However,
when hosts are aggregated, the host encounter rate increases and so does the prob-
ability of encountering a second higher-quality host. In such conditions, we would
expect host-seeking larvae to evolve discrimination ability.
Both A. bilineata and A. bipustulata can discriminate unparasitized from par-
asitized pupae (intraspecific host discrimination), and pupae parasitized by con-
specifics from pupae parasitized by other species of Aleochara (interspecific
discrimination). Discrimination is based on chemical cues and partially on physical
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32 BRODEUR ¥ BOIVIN

cues related to the entrance hole in the puparium. Larvae in host-poor habitats,
characterized by low host-encounter rate, showed a higher level of superpara-
sitism (99). The acceptance of parasitized hosts did not result from the absence
of discrimination, as larvae that superparasitize a host exhibit a distinct change
in behavior. The entrance holes of the initial A. bilineata first-instar larvae were
generally found on the dorsal surface of cabbage maggot puparium. However,
when superparasitism occurred, the entrance hole of the second larva was mostly
found on the ventral surface of the puparium. This behavioral change may delay
the encounter with the first larva, providing the second larva with time to feed and
gain energy (98).
Both intra- and interspecific competition influence host acceptance and, for
female parasitoids, the allocation of resources. Although the optimal allocation
of progeny and sex is restricted to female parasitoids, host-seeking larvae can
still allocate varying amounts of time to searching for and evaluating hosts. The
presence of competitors in the habitat can be used as an indication of the probability
of finding already parasitized hosts and may therefore alter the host searching
strategy of a larva. When the population density of searching larvae is high, the
larvae should relax their selection criteria, as seen in A. bilineata (99).
Optimal patch time allocation refers to behaviors associated with the exploita-
tion of host patches. When a female parasitoid enters a host patch, the duration
of the exploitation and therefore the extent to which the patch will be exploited
is one of the key factors determining her foraging success (19, 127). Factors such
as patch quality and travel time between patches are postulated to modulate patch
time residence (19). The concept of a host patch is less relevant to host-seeking
first-instar parasitoid larvae because of their low mobility and the unique host se-
lection event. However, the time spent evaluating host quality is probably under
evolutionary constraints similar to those for patch searching for female parasitoids.
As long as a host-seeking first-instar larva has reserves of time and energy, it can
thoroughly evaluate quality before parasitizing or rejecting a host. When larvae
of A. bilineata age, the amount of time available to find a host decreases and, as
a result, their acceptance of parasitized hosts increases (99). However, the host
evaluation behavior and the impact of travel time have never been studied.

COMPETITION BETWEEN IMMATURES

Once a host has been found, evaluated, and accepted, the immature parasitoid must
secure enough resources to complete development. In cases of superparasitism, this
implies competing with other immatures.
When several immature parasitoids share a host, they compete for the resource
either in a scramble or in a contest mode (88). In gregarious species, competition is
generally restricted to resource exploitation, where immatures rarely are in direct
combat, but when resources are limited, individuals are smaller and have reduced
fitness. When superparasitism occurs in solitary parasitoids, the immatures enter a
contest competition and supernumerary individuals are destroyed either physically
or physiologically (66, 90).
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ECOLOGY OF IMMATURE PARASITOIDS 33

In polyembryonic parasitoids such as the Encyrtidae the embryos give rise

to two morphologically different types of larvae (112). Larvae of the first type
are normal and eventually develop into male and female adults. The second type
consists of precocious larvae that are serpentine, have large mandibles, develop
more rapidly, and are more mobile than larvae of the first type. They never molt
and lack some internal organs. Several roles have been proposed for the precocious
larvae including the breakdown of host tissues for normal larvae (90). However,
they can also be involved in immature competition either as “bodyguards” for the
normal larvae against nonsibling competitors (24) or as “killers” that preferentially
attack male immatures (46) and thus help produce a female-biased sex ratio.

Evolutionary Pathway to Gregariousness:

Tolerance or Movement?
The outcome of competition between immature parasitoids is either one or multiple
larvae sharing a host. The existence of both solitary and gregarious development
represents an important dichotomy in insect parasitoids. In Hymenoptera, solitary
development is considered the ancestral parasitic condition, with gregariousness
having evolved at least 43 times independently in 26 different families (69, 96).
The passage from solitary to gregarious development implies changes of within-
population modalities of aggression.
This dichotomy has major implications for evolutionary ecology. For solitary
species the killing of siblings by aggressive immature larvae prevents the oviposit-
ing female from reaching an optimal clutch size, thereby decreasing her fitness.
This results in a parent-offspring conflict where the genes expressed in the parent
and its immatures have different optima.
The appearance of gregarious development has been explained by an increase
in fitness (42). Even though individuals that develop gregariously in a host are
generally smaller than solitary individuals, their cumulative fitness can be greater
(43). It has been postulated that coexistence of several immatures in a host is made
possible by the presence of a tolerance gene that enables larvae to share a host with-
out fighting. However, tolerant individuals would be killed by nontolerant fighting
individuals; for a tolerant gene to persist, the fitness gain per host must be large
enough to compensate for the destruction of clutches attacked by an aggressive
mutant. This implies that a minimal clutch size is needed for the tolerant gene to be
evolutionarily stable (42). Clutches smaller than three or four eggs are predicted to
be less evolutionarily stable than large ones, as the tolerant population is vulner-
able to invasion by an aggressive mutant, whereas the clutch size necessary for a
tolerant mutant to invade a solitary population is much larger (69, 96). Because of
this threshold difference, the presence of solitary fighting immatures is considered
to be a locally absorbing state, i.e., once a mutant solitary fighting larva appears
in a population, it is unlikely that a mutant tolerant can reverse the situation (52).
Given the strict conditions for gregariousness to invade a solitary population,
one would expect gregarious species with small brood size to be rare. However,
contrary to prediction, 87 gregarious species in 15 families of Hymenoptera have
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34 BRODEUR ¥ BOIVIN

clutch sizes of fewer than four eggs (70). Thus small gregarious broods can be
evolutionarily stable under some circumstances, such as the occurrence of single-
sex broods (96), or being ectoparasitoids and idiobionts (72).
The tolerance model assumes that tolerant individuals do not fight and therefore
would always lose in the presence of aggressive individuals. A factor that could
relax the constraint for the transition from solitary state to gregarious development,
even in small broods, is the degree of movement by the immatures. Aggressive
immatures with reduced or no mobility could develop gregariously in a host, as they
retain the ability to defend themselves against aggressive mobile mutants (11). The
immobility hypothesis provides a less-stringent route from solitary to gregarious
development in parasitoids (82). Anaphes victus and A. listronoti are two closely
related species of mymarid parasitoids of curculionid eggs; however, the first is
solitary and the second is gregarious. When a larva of each species was present in a
host, each had a survival probability of about 50%, indicating that the two species
have similar fighting abilities (11). When the solitary A. victus was present with
varying numbers of A. listronoti immatures, its probability of survival matched
the predictions of the immobility hypothesis where the two types of larvae had the
same fighting abilities but where the immobile immatures did not fight each other
(11). Direct observations of the two types of immatures showed that the solitary
A. victus larvae were much more active than the gregarious A. listronoti larvae.
Gregarious development can evolve in different ways. Solitary species could
increase clutch size, and the presence of several immatures within a host results
in the selection of nonsiblicidal behaviors (either tolerance or immobility) (80).
Alternatively, a species could gain tolerance or lose mobility while still ovipositing
single eggs. In the latter case the evolutionary pressure is on the female, and
individuals depositing multiple-egg clutches would have an advantage over those
depositing only one egg. Because immobile larvae retain their fighting ability and
therefore are less vulnerable to elimination by aggressive individuals, both routes
are plausible (82). Using an analytical genetic model, Pexton et al. (83) showed
that a reduced mobility trait can spread in the population under a wide range of
conditions. The criterion for the spread of a rare immobility allele is independent
of a biased sex ratio and the likelihood of single-sex broods.
In a sense, a decrease in larval mobility and the resulting gregarious develop-
ment can be seen as an evolutionary victory for the female parasitoid in a parent-
offspring conflict. The female achieves the possibility to optimize her fitness gain
per host at the expense of the developing immatures. The immatures, although
more numerous, generally have a lower individual fitness. The occurrence of such
a mechanism in other groups of gregarious species remains to be tested.

THE PARASITIZED HOST: A DISTINCT

ECOLOGICAL ENTITY
Once the host is located, evaluated, and accepted, the immature parasitoid has to
exploit the resource. Parasitized hosts differ biochemically, physiologically, and
ecologically from unparasitized conspecifics (114, 123, 125). They often exhibit
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ECOLOGY OF IMMATURE PARASITOIDS 35

consequential symptoms including altered morphology, development, reproduc-

tion, and behavior that are likely to change over time as the relationship between
the host and the immature parasitoid develops. Parasitism therefore results in the
formation of a dynamic, integrated host-parasitoid complex (114), where both par-
asitoid and host genomes actively influence the outcome of the interaction (25).
For example, competition for resources between the host and the immature para-
sitoid could be related in a complex manner, as parasitoid’s nutritional requirement
stresses the host’s metabolism and, conversely, the nutritional status of the host in-
fluences parasitoid development (114). The outcome of such an interaction might
be a parasitized host that spends more time feeding, displays abnormal locomotory
patterns, or passes through supernumerary larval instars (106, 114).
Altered physiological and ecological patterns in parasitized hosts may be adap-
tations of either the host or the parasitoid or may reflect pathological changes that
are selectively neutral (57, 74). The host-parasitoid relationship has unique aspects
that promote the concept that a host represents an extended phenotype (sensu 25)
of the parasitoid. Likewise, Vinson (123) considered that a parasitized host is no
longer “a member of the host species, but must be viewed as a container for the
parasitoid.” Once the host has been parasitized, and the immature parasitoid has
successfully invaded its host, the host’s fate is permanently modified: The host
has, in most cases, no reproductive future and does not survive the interaction.
Consequently, under this schematic framework, the evolution of host-parasitoid
relationships should be toward the benefit of the parasitoid. However, as we will see
below, there are alternative functional outcomes for changes in parasitized hosts.
Predation risk occuring between oviposition and adult emergence has been
identified as a strong determinant of life-history evolution of parasitoids (16, 51a,
87). This is especially true for immature parasitoids that face a diverse array of
natural enemies when developing in exposed and poorly-defended hosts. In the
next sections, we first examine how susceptibility of host to predation is affected
by parasitism, and then discuss the strategies evolved by immature parasitoids to
reduce predator-induced mortality.

SUSCEPTIBILITY OF PARASITIZED
HOSTS TO PREDATION
Parasite-induced changes in host characteristics commonly alter the response of
the parasitized host to the environment, the most general assertion being that
parasitism weakens the host (114). The developmental and behavioral changes
observed in parasitized hosts include supernumerary larval instars; premature or
arrested pupation; sluggish behavior; selection of specific habitats; and changes
in rate of feeding, period of activity, or foraging patterns (58, 106, 125). Because
immature parasitoid mortality is contingent on that of the host (87, 123), and
because predation is a significant selective force in the evolution of several animal
characteristics (64), natural selection should act to promote parasitoid attributes
that render parasitized hosts less susceptible to natural enemies (12, 37). Very
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36 BRODEUR ¥ BOIVIN

few studies have been primarily designed to examine susceptibility of parasitized

hosts to natural enemies. Nevertheless, some inferences can be drawn (J. Brodeur,
unpublished data).
First, as expected from the diversity of host-parasitoid-predator associations,
patterns of predation rate vary considerably depending on the system, with para-
sitized hosts being less, more, or equally susceptible to predation as unparasitized
ones.
Second, the probability of being detected by predators for unparasitized sessile
hosts is usually similar to that for hosts containing idiobiont parasitoids (55, 89, 94),
but the frequency of attack often varies in relation to parasitoid ontogeny (see
below). A field survey revealed that unidentified predators preferentially attacked
parasitized over unparasitized egg masses of the spruce bud moth (81). Conversely,
in another forest species, the winter moth, Operophtera brumata, pupae parasitized
by a tachinid fly, Cyzenis albicans, are attacked less frequently by staphylinid
beetles than unparasitized pupae are (95).
Third, no clear patterns emerge from the very few studies that examined the
vulnerability of mobile hosts parasitized by koinobiont parasitoids. Tostowaryk
(116) observed that parasitized sawflies were more susceptible to predation by a
pentatomid bug as they were more frequently located at the periphery of the colony
and thus more likely to be attacked by a foraging predator. In a field study, Jones
(60) reported that survival of healthy Pieris rapae caterpillars was higher than those
parasitized by the braconid wasp Apanteles glomeratus, as the latter were more
often captured and killed by ants. A study by Reed et al. (91) showed that Indian
meal moth larvae parasitized by the ichneumonid wasp Venturia interpunctella
suffered higher levels of cannibalism than unparasitized ones. Other experimen-
tal studies concluded that active hosts parasitized by koinobiont parasitoids are
equally susceptible to predation as unparasitized hosts [(110); J. Brodeur, unpub-
lished data]. Parasitism of the tobacco budworm by a braconid wasp did not affect
its susceptibility to predation by lacewing larvae (110). Brodeur (unpublished data)
determined the extent to which parasitism of the potato aphid by the aphid par-
asitoid Aphidius nigripes altered the probability and success of attack by three
species of invertebrate predators characterized by their differences in prey selec-
tivity, feeding type, and foraging strategy. The results indicated that the incidence
of predation by coccinellids, hover flies, and predatory midges was similar for
parasitized and unparasitized aphids.
Fourth, parasitism is a dynamic process and susceptibility to predators may vary
in relation to parasitoid ontogeny. A general trend observed in systems involving
idiobiont parasitoids developing in sessile hosts (egg and pupa) is that newly par-
asitized hosts are as susceptible to predation as unparasitized prey, whereas hosts
containing late-instar larvae or pupae of the parasitoid are less susceptible. For ex-
ample, the coccinellid Delphastus pusillus readily accepts sweetpotato whiteflies or
those parasitized by first-instar aphelinid parasitoids, but avoids feeding on white-
flies containing third-instar and pupal parasitoids (55). For koinobiont parasitoids,
no published studies have tested the effect of parasitoid age on host vulnerability.
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ECOLOGY OF IMMATURE PARASITOIDS 37

However, Brodeur (unpublished data) found no difference in the susceptibility

of unparasitized and parasitized aphids containing either egg, second-, third-, or
late-fourth-instar parasitoid larvae to three species of aphidophagous predators.
These disparate and often anecdotal observations are insufficient to provide a
comprehensive pattern for the relationships between parasitism and host suscepti-
bility to predation. However, the limited experimental evidence suggests that hosts
parasitized by idiobiont and koinobiont parasitoids are usually similar to unpar-
asitized hosts in their vulnerability to invertebrate predators. The picture is even
less clear if one would like to analyze how parasitoid-induced changes in host
physiology and behavior alter the susceptibility of parasitized hosts to pathogenic
infection (18).

STRATEGIES TO REDUCE MORTALITY

FROM NATURAL ENEMIES
Parasitoids may adopt two main strategies to lower predation pressure on the
parasitized host: reliance on host defensive mechanisms and manipulation of host
behavior (12, 17, 86).

Reliance on Host Defense

Dogiel (27) defined parasites as organisms “. . .which use other living animals
as their environment and sources of food at the same time relinquishing to their
hosts, partly or completely, the task of regulating their relationships with the ex-
ternal environment.” Implicitly, survival of immature parasitoids depends on the
performance of the hosts, in particular their ability to avoid other natural ene-
mies prior to successful completion of development by the parasitoid. Therefore,
any alteration on the part of the parasitized host that increases risks of predation
should be prevented until the parasitoid has completed its development. Hosts have
adaptations for avoiding natural enemies, and immature parasitoids should exploit
the host’s defensive mechanisms to promote their own survival (17, 60). Yet, the
conditions are different for idiobiont and koinobiont parasitoids.
Idiobiont parasitoids alter the development and behavior of their hosts at ovipo-
sition or shortly thereafter. The host, which contains a fixed and sufficient amount
of resources for the parasitoid larva, is permanently paralyzed or killed. Keeping
the host in a lethargic state may, therefore, be a mechanism to increase inconspic-
uousness to predators. Along with this strategy, most idiobiont parasitoids attack
concealed hosts (53).
Koinobiont parasitoids depend on the host not only to satisfy their nutritional
and metabolic needs but also to reduce risks of premature death from predation.
Consequently, one would expect an evolution toward a relationship where imma-
tures have minimal stressful effects on the defensive behavioral patterns of the
host (106, 114). Immature parasitoids should not handicap their host’s competitive
ability by monopolizing its energy, mechanically impeding its movements, altering
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38 BRODEUR ¥ BOIVIN

its sensory system, or precociously damaging its vital tissues and organs, as any
parasitoid-induced changes that increase early host mortality would be detrimen-
tal to the parasitoid’s own survival. Most studies on host utilization strategies by
immature koinobiont parasitoids indicate that larvae do not cause significant dam-
age to host tissues and organs during early development [see (90) and references
therein]. Although generalities should be made with caution, two main divergent
patterns of parasitoid feeding have been described (40, 51). Some larvae, mostly
Braconidae, essentially feed by ingesting host hemolymph and emerge from a
still-living but moribund host to pupate externally. Others, mostly Ichneumonidae,
start as hemolymph feeders but switch to host tissue toward the end of larval de-
velopment. They typically consume the entire host and pupate within the host.
Nevertheless, in both cases the parasitoid larva acts as a metabolic sink and, al-
though parasitoid-mediated alterations in host growth may occur, the host remains
functional from parasitoid oviposition to pupation.
Potential reduction of parasitoid mortality through reliance on host defensive
behavior is nicely portrayed by the interaction between the pierid caterpillar Pieris
brassicae and its gregarious braconid wasp Cotesia glomerata. The parasitoid has
evolved several mechanisms to maintain its host in a suitable condition, not only
throughout parasitoid larval development but also during parasitoid pupation. C.
glomerata larvae do not consume >50%–60% of the food assimilated by the host
(105). Host metamorphosis is arrested during the prepupal stage, temporary paraly-
sis favors both parasitoid emergence from the host and spinning of the cocoon, and
host bleeding is prevented by parasitoids leaving their cast integuments as plugs in
the emergence holes (107). Brodeur & Vet (17) subsequently showed that follow-
ing parasitoid emergence, the caterpillar stays on the pupating parasitoids, spins
a web over them, and displays aggressive responses identical to that of healthy
caterpillars when disturbed by natural enemies. They hypothesized that immature
parasitoids exploit, for their own benefit, some components of the host’s behavioral
defense repertoire that remain functional. This hypothesis was supported by Kester
& Jackson (63), who showed in a similar host-parasitoid system that continued
association of parasitoids with their host reduces predation on parasitoid pupae.

Host Behavior Manipulation

The notion that evolution can lead to the manipulation by a parasite of its host’s
behavior has become a familiar concept for parasitologists (75, 85). Host behavior
manipulation probably has multiple independent origins, as reflected by the wide
taxonomic distribution of organisms capable of interfering with the behavior of
their host: virus, fungus, metazoan parasite, nematode, parasitoid. For parasitoids,
theory is a few steps ahead of empirical evidence. The phenomenon of host behavior
manipulation is poorly understood and, consequently, less generally accepted.
In this section, we first examine some evidence of altered behaviors in diverse
host-parasitoid associations and describe how host manipulation relies on timing,
i.e., the onset of behavioral changes in parasitized hosts. Next, we look at three
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ECOLOGY OF IMMATURE PARASITOIDS 39

examples to illustrate the recurring problem of determining the adaptive signifi-

cance, if any, of host behavior manipulation in parasitoids.

TYPE AND TIMING OF ALTERED BEHAVIORS Horton & Moore (58) identified two
main categories of altered behavior of hosts by parasitoids: changes in activity
level and changes in habitat preference. A few conclusive, manipulative experi-
ments showed that host plant preference could be altered in arctiid moths para-
sitized by tachinid flies (62) or in bumble bees parasitized by conopid flies (101).
Parasitism may also alter foraging budget and diurnal/nocturnal activities of hosts.
A braconid wasp induces its nocturnal caterpillar host to become active during the
day (100). Changes in the distribution of unparasitized and parasitized hosts are
the most common behavioral manipulations reported for parasitoids. Parasitized
hosts may move to elevated and exposed sites (14, 15, 103, 109) or select more con-
cealed microhabitats (13, 56, 77, 92). Such differences are often associated with
altered responses to thermal, phototactic, geotactic, and thigmokinetic preference
in parasitized hosts (13a, 58). Another type of atypical behavior was described by
Eberhard (29), who observed that moribund spiders parasitized by an ichneumonid
wasp spin a “cocoon web” that is entirely different from the archetypal one, which
is more resistant to adverse climatic conditions and could favor survival of the
pupating parasitoid.
Parasitoid-induced behaviors are normal components of the host’s behavioral
repertoire but they are expressed inappropriately (17). For example, larvae of a
tachinid parasitoid cause their caterpillar hosts to leave the host plant prematurely
and burrow in the soil before death (92). Parasitism accelerates the onset of wander-
ing and burrowing behavior in caterpillars, two pre-existing behaviors associated
with host pupation. Major gaps exist in our understanding of the mechanisms
for manipulative behavior in parasitized hosts. Thompson (114) recognized that
“. . .the physiological bases for the modified behavior observed in infected hosts
may be elusive because in many cases they merely reflect subtle modifications of
existing mechanisms.” Nevertheless, because behavioral components are directly
linked to neuronal function and because parasitoids have the capacity to modulate
the endocrine and nervous system of the host (8, 9), altered host behaviors are
thought to proceed from modified developmental processes and reflex pathways
induced by chemical or mechanical action of the parasitoid (115).
Host manipulation is needed only when requirements of the immature parasitoid
differ from those of its host. A key component of success is timing. Poulin et al.
(86) hypothesized that koinobiont parasitoids should rely on the host’s normal
behavioral repertoire as long as it is effective, and thereafter should manipulate
some of its components. In most cases, the onset of behavioral manipulation should
coincide with a period of high vulnerability (37), such as the end of parasitoid larval
development, when host defensive capacities are more likely to be impaired.

CASE STUDIES A number of investigators have used aphid parasitoids to exam-

ine the nature, occurrence, and function of microhabitat selection through host
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40 BRODEUR ¥ BOIVIN

behavior manipulation. Aphid parasitoids are solitary koinobiont braconid wasps.

At the end of parasitoid larval development the host is killed and only its cuticle re-
mains. This “aphid mummy” serves as a shelter, within which the parasitoid spins a
cocoon and pupates. Studies have been reported for many different host-parasitoid
associations, including species from six genera (Aphelinus, Aphidius, Ephedrus,
Praon, Trioxys, Lysiphlebus) in two families (Aphelinidae and Braconidae) where
parasitized hosts, just prior to death, cease feeding and leave the aphid colony
to mummify at specific sites. Aphid mummies are often found on the upper leaf
surface or off the host plant (10, 13–15, 56, 79). Brodeur & McNeil (13, 15) also
found that the behavior of parasitized aphids varies in function of the physiological
state of the parasitoid. Mummies containing nondiapausing Aphidius nigripes are
located on the upper surfaces, mainly in the apical stratum of the plant canopy,
whereas aphids containing parasitoid larvae destined to enter diapause frequently
leave the host plant and mummify in concealed microhabitats. In both situations
the host was a nondiapausing individual, so the behavioral differences observed are
due directly to the physiological state of the parasitoid, providing strong support
to the concept that mummification site selection is mediated by the immature par-
asitoid. A different interpretation was proposed by Chow & Mackauer (22), who
studied microhabitat selection of pea aphids parasitized by five species of braconid
wasps under laboratory conditions. They found differences in mummification sites
among parasitoid species, but they concluded that this was an epiphenomenon, a
byproduct of trauma to the host. To account for mummies that were found away
from the aphid colony, they argued that parasitism progressively handicaps the
host, especially its motor control. Moribund hosts that frequently dropped off the
plant were not able to walk back to the feeding site, and thereby mummified in
atypical habitats.
Aphid parasitoids may benefit from induced mummification site selection. In
a field survey, using host plants with different architectures, Brodeur & McNeil
(14, 15) showed that survival of nondiapausing pupal parasitoids was higher on the
upper surface of apical leaves rather than close to the aphid colony due to reduced
levels of hyperparasitism and, to a lesser extent, lower predation. Another study that
examined the relationship between induced habitat selection and hyperparasitism
in 16 species of aphids provided mixed support for the manipulation hypothesis
(79). The authors concluded that the consequences of mummifying away from the
colony in terms of hyperparasitism risk were “very variable and no single pattern
emerged.” A confounding factor in several aphid-parasitoid associations was ant-
attendance, as mummies located within ant-attended colonies were less likely to
be attacked by hyperparasitoids.
Another special case of altered behavior in parasitized aphids deserves attention.
The aphid may retain control of the host-parasitoid relationship by committing
suicide. The host suicide hypothesis postulates that parasitized hosts may benefit
from suicide if it increases their inclusive fitness (108). Pea aphids parasitized by
A. ervi often dropped from the host plant when disturbed, thus increasing risk of
dessication and death (73). This behavior was interpreted as a kin-selected sacrifice
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ECOLOGY OF IMMATURE PARASITOIDS 41

of parasitized individuals with no reproductive potential that serves to decrease

risk of parasitism to related individuals by eliminating the parasitoid contained
within them. This interpretation is not without alternative explanations and has
been criticized (43).
Bumble bees parasitized by conopid flies represent another particularly suitable
example to investigate ultimate causation of host behavior manipulation. Para-
sitized workers reduce their foraging activity, modify their food-collecting pattern
by switching to flowers with shorter corollas (101), exhibit a preference for cold
temperature (78), and tend to abandon their colony (78, 102). The latter altered
behavior was first considered to be adaptive to the conopid flies, as parasitoid
pupae developing in bumble bee nests would be more susceptible to pathogenic
infection than those pupating outside the colony (102). An alternative hypothesis
was proposed by Poulin (84), who argued that a parasitized bumble bee could
increase its inclusive fitness by abandoning the colony and dying away from the
nest, thereby decreasing the probability that the parasitoid it carries would emerge
next spring and parasitize members of its colony. A complementary explanation
was proposed by Müller & Schmid-Hempel (78), who showed that by remaining
outside the colony at night parasitized hosts experience low temperature, which
reduces parasitoid survival and development rate. It was further hypothesized that
the exploitation of cold temperature allows parasitized bumble bee workers to ex-
tend their lifetime and, for those that continue to sporadically return to the nest,
prolong the period of time they collect resources for the colony. Parasitism may
induce another type of altered behavior in bumble bees. At the end of parasitoid
development, moribund bumble bees tend to bury themselves in the soil more often
than control hosts (77). In this instance, the digging behavior increases parasitoid
fitness by providing a suitable overwintering site for diapausing conopid pupae.
Adult flies emerging from overwintering sites in the soil were larger and had fewer
malformed wings than those overwintering on the ground.
A third host-parasitoid model is rewarding to our understanding of altered be-
havior in parasitized hosts. English-Loeb, Karban & Brody (32, 33) observed that
woolly bear caterpillars, Platyprepia virginalis (Arctiidae), may survive and repro-
duce following the emergence of the parasitoid Thelaira americana (Tachinidae).
In the field, they showed that parasitism tends to modify caterpillar host plant
preference from bush lupine to poison hemlock. This parasitoid-induced change
has significant positive consequences for both the host and the parasitoid. Para-
sitized caterpillars were more likely to survive to adulthood and parasitoids were
larger when reared on poison hemlock rather than on bush lupine. Karban &
English-Loeb (62) suggested that host plant selection may be governed not only
by the nutritional quality of the plant and the herbivore’s susceptibility to natural
enemies, but also directly by parasitism. Which protagonist is in control in this
system? We do not know, but both interacting genomes have convergent interests
to select poison hemlock over bush lupine once the parasitized host complex has
been formed. Obviously, the host’s perspective, which is usually ignored when
analyzing altered behavior in host-parasitoid association, has to be restored.
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42 BRODEUR ¥ BOIVIN

ADAPTIVE SIGNIFICANCE OF ALTERED BEHAVIORS Behavioral changes of para-

sitized hosts are most likely to benefit the parasitoid because the host has no re-
productive future. However, there are alternative explanations. Altered behaviors
may have evolved to increase host fitness, either by increasing parasitoid mortality
[e.g., through behavioral fever (61)] or by reducing risk of parasitism to relatives
[e.g., through host suicide (73)]. It is also possible that there are no evolution-
ary explanations for altered behaviors and that they merely reflect mechanistic
consequences of pathologies caused by immature parasitoids.
Studies on parasitoids of aphids, bumble bees, and woolly bear caterpillars illus-
trate how explicit results may lead to different conclusions about the evolutionary
significance of altered behavior. Interpreting the consequence of altered behaviors
in parasitized hosts is challenging because they may (a) be subtle and differ only
quantitatively from the normal behavioral repertoire of the host, (b) change during
the course of infection, or (c) be expressed at specific period during the day or un-
der distinct ecological conditions. Three approaches can be taken to elucidate the
nature and origin of behavioral changes in parasitized hosts: (a) the identification
of the proximate mechanisms and a thorough account of the pathology associated
with damage inflicted by immature parasites, (b) the assessment of fitness benefits
and their variations for both host and parasite, and (c) the study of the influence
of parasitoid and host phylogeny (75, 85). Mechanisms, costs and benefits, and
evolutionary origins of host behavior manipulation have yet to be conclusively
tested for parasitoids.

CONCLUSIONS
Despite decades of discussion about the evolutionary biology of parasitoids, it
is surprising how little is known about the functional aspects of the ecology of
immature stages. In this review we have examined an amalgam of information
from a conceptual rather than descriptive approach. It is evident that only a lim-
ited number of experimental studies have explored each of the aspects discussed,
making a search for patterns rather tenuous. Several factors contribute to this need
for caution: the huge diversity of host-parasitoid associations, the variety of means
by which parasitoids exploit their hosts, and the variability of ecological factors
that modulate host-parasitoid–natural enemy interactions.
We believe that many more patterns of host selection behavior by first-instar
parasitoid larvae, vulnerability of parasitized hosts to predation, and parasitoid-
induced behavioral changes will emerge if they are sought. Accurate observations
of immature parasitoids, especially of endoparasitic species, are intrinsically diffi-
cult. However, adaptation of existing and original experimental techniques devel-
oped to study metazoan parasites, evaluation of new host-parasitoid associations
as research models, and adoption of a comparative approach would help to over-
come some of these difficulties. Parasitoid ecologists tend to underestimate the
occurrence and significance of parasitized individuals in a host population. For
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ECOLOGY OF IMMATURE PARASITOIDS 43

one thing, more attention in the future should be directed to atypical development,
distribution, and behavior exhibited by parasitized and infected hosts under natural
conditions.
The themes considered in this review illustrate the diversity of ecological con-
straints faced by immature parasitoids. Parasitism success involves decisions and
responses made by developing parasitoids to solve conflicts with five potential pro-
tagonists: host, mother, siblings, competitors, and natural enemies. The resolution
of these conflicts can be achieved by several of the strategies discussed above. The
complexity of certain mechanisms evolved by immature parasitoids to find their
host, reduce competition, avoid predation, and, for koinobiont species, minimize
the deleterious effects of parasitism on the host attest to high levels of coevolution
in some associations.
Aspects of the functional ecology of immature parasitoids may also significantly
influence host-parasitoid population dynamics. For instance, changes in levels of
susceptibility of parasitized hosts to natural enemies may be a significant factor in
determining the potential of a parasitoid to regulate host populations. Despite the
widespread occurrence of parasitoids in natural communities and their importance
in biological control, theoretical and empirical studies have largely overlooked
mortality factors that impact parasitized insect hosts. Likewise, it seems paradox-
ical that most models of host-parasitoid population dynamics assume that an egg
laid by a parasitoid is equivalent to an offspring produced (16). Assessing the fate
of immature parasitoids is challenging because distinguishing unparasitized from
parasitized hosts is remarkably difficult to achieve in the field. Effective popula-
tion models and formulation of biological control solutions would benefit from
the careful integration of functional aspects of the ecology of juvenile parasitoids.
This is a critical and ambitious task for ecologists.

ACKNOWLEDGMENTS
We thank J.N. McNeil, J. Trumble, and L.E.M. Vet for valuable comments on var-
ious aspects of this manuscript. This work was supported by the Natural Sciences
and Engineering Research Council of Canada.

The Annual Review of Entomology is online at http://ento.annualreviews.org

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