Content uploaded by Amos Bouskila
Author content
All content in this area was uploaded by Amos Bouskila
Content may be subject to copyright.
The effect of host starvation on parasitoid
brood size in a polyembryonic wasp
Michal Segoli1, Ally R. Harari1,2, Amos Bouskila1
and Tamar Keasar3
1Department of Life Sciences, Ben Gurion University, Beer Sheva, Israel,
2Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel
and 3Department of Biology, University of Haifa – Oranim, Tivon, Israel
ABSTRACT
Hypothesis: Offspring of polyembryonic parasitoid wasps (in which each egg divides clonally
to produce several individuals inside a host body) adjust their numbers according to the host
carrying capacity.
Organism: The polyembryonic parasitoid wasp, Copidosoma koehleri, parasitizes the potato
tuber moth, Phthorimaea operculella.
Methods: We starved parasitized host larvae during the wasp embryonic division phase. We
recorded host mass and the number of wasps in sub-samples of dissected hosts throughout
development and upon pupation and emergence.
Results: Starvation significantly reduced larval host mass but this was largely compensated at
the pupal stage, probably through delayed pupation. Starved hosts tended to harbour fewer
wasps but this effect was marginally non-significant.
Conclusions: Wasp offspring do seem to adjust their numbers in response to host starvation,
but not strongly.
Keywords: brood size, Copidosoma koehleri, host quality, host starvation.
INTRODUCTION
Brood size has important implications for the fitness of both parents and offspring. Since
resources for the production and care of offspring are often limited, offspring number is
traded-off with quality (Lack, 1947). Thus, parents often adjust the number of offspring that
they produce to the carrying capacity of their immediate or anticipated environment.
Examples of this phenomenon include, among others, butterflies that adjust clutch size
to the quality of the host plant (Bergstrom et al., 2006; Kagata and Ohgushi, 2002), burying beetles
that adjust clutch size to the size of the carcass (Nagano and Suzuki, 2007), and Siberian jays that
reduce clutch size in an environment perceived as risky (Eggers et al., 2006).
Correspondence: M. Segoli, Department of Life Sciences, Ben Gurion University, Beer Sheva 84105, Israel.
e-mail: msegoli@bgu.ac.il
Consult the copyright statement on the inside front cover for non-commercial copying policies.
Evolutionary Ecology Research, 2010, 12: 259–267
© 2010 Michal Segoli
The trade-off between the number of offspring and their quality may be especially
pronounced in parasitoids, where the offspring develop on a limited amount of resources,
i.e. the body of the host (Godfray, 1994). Parasitoids show a very high variation in brood size,
both within and among species. In solitary parasitoids, only one individual emerges
from each host, while in gregarious parasitoids, all larvae within a host can complete
development and emerge (Mayhew and Glaizot, 2001). As expected, females of gregarious species
often adjust the number of eggs they lay to the quality of the host [e.g. host species (Godin and
Boivin, 2000), size (Reitz and Adler, 1995; Wang et al., 2008), developmental stage (Sato et al., 1986; Chong
and Oetting, 2006), and the risk of superparasitism (Pexton and Mayhew, 2005)], laying larger clutches in
higher quality hosts (reviewed by Godfray, 1994).
In some cases, however, female parasitoids may be limited in their ability to assess the
quality of the host. For example, in koinobiont parasitoids, where the host continues to
develop after parasitism, the amount of resources that will be available to the developing
offspring largely depends on the amount of food that will be consumed by the host after
parasitism (Harvey, 2005; Strand and Casas, 2008). In addition, offspring may have to compete for
resources with other larvae inside the host in the case of later superparasitism (for example,
parasitism by additional females). As a consequence, a female may face difficulties in
predicting the host’s final carrying capacity, and adjust her clutch size accordingly. One
possible adaptation for this limitation is to pass part of the control over brood size to the
offspring themselves (Craig et al., 1997).
An example for possible sharing of control over brood size may come from polyembryonic
parasitoid wasps, in which many genetically identical embryos develop from each egg.
In the process of polyembryonic development, a primary cell mass (morula) proliferates
to create a mass of many developing embryos (polymorula). Proliferation continues until
wasp embryos differentiate into active larvae at the final stages of host development. These
larvae consume the host tissues, pupate, and emerge as adult wasps (Grbic et al., 1998; Strand, 2003;
Segoli et al., 2009a). While the mother wasp may control the number of eggs to be laid, offspring
may have the potential to further adjust brood size by controlling the degree of proliferation
during embryonic stages. Low levels of proliferation, producing broods that are too
small, may be disadvantageous due to the inability of the developing larvae to consume all
of the host tissue and to emerge from the host. On the other hand, large brood sizes
may have a negative effect on individual body size and consequently on its fitness (Ode and
Strand, 1995). Thus, the adjustment of brood size to the host carrying capacity is very
important for the fitness of individuals in the brood. Since all wasps that develop from one
egg are genetically identical, rivalry between them is expected to be minimal [kin-selection
theory (Hamilton, 1963, 1964)]. High cooperation between offspring may enhance host utilization
and may result in a brood size that is optimal for both the mother and her offspring
(Godfray, 1994).
In this study, we tested the hypothesis that embryos adjust the level of clonal-proliferation
according to the body condition of the host, in the polyembryonic wasp, Copidosoma
koehleri Blanchard (Hymenoptera: Encyrtidea). We manipulated body condition by
starving hosts during the wasp proliferative phase. Host starvation was previously shown to
affect parasitoid survival, development, and body size (Beckage and Riddiford, 1983; Harvey et al., 1995).
In a study on the polyembryonic wasp C. floridanum, host starvation for 48 h substantially
decreased host mass and the number of wasps emerging from the host (Giron et al., 2004).
It is unclear, however, whether this decrease was due to increased embryonic mortality or
reduced proliferation. To address this, we dissected samples of hosts at fixed time intervals
Segoli et al.260
following starvation and counted the number of developing wasps inside the hosts. Similar
data were recorded for non-starved parasitized hosts that served as controls. We predicted
that if embryos adjust proliferation according to host condition, starvation would reduce
the number of embryos, larvae, and adults produced.
METHODS
Study organism
Copidosoma koehleri Blanchard is a polyembryonic parasitoid wasp that parasitizes the
potato tuber moth (Phthorimaea operculella Zeller, Gelechiidae, Lepidoptera), and is used
as a biological control agent of this pest (Horne, 1990; Kfir, 2003). The adult female lays her eggs
into the moth egg. Females usually lay one egg per oviposition event, but superparasitism
by the same female or by different females is common (Doutt, 1947; Keasar et al., 2006). The moth
larva hatches and develops, while the wasp egg divides clonally to produce many embryos.
Proliferation occurs mainly during the first and second larval instars of the host, and
normally ceases within 10 days of parasitism (when reared at 29⬚C), as the host enters
the third instar. Wasp embryos develop into larvae, which consume the entire host tissues
before pupation. Female clones produce more embryos than male clones (40–50 vs.
30–40 individuals, respectively). The wasp life cycle takes about a month and is highly
synchronized with that of the host (Segoli et al., 2009a). In several polyembryonic species, a
proportion of embryos develop into specialized soldier larvae that attack competitors inside
the host (Cruz, 1981, 1986; Giron et al., 2004). In C. koehleri, dissections of developing hosts indicate
that each female clone contains one female soldier. Male clones, on the other hand, do not
produce soldiers (Doutt, 1952; Keasar et al., 2006; Segoli et al., 2009a).
A laboratory stock of C. koehleri was used in the experiment. The stock originated from
field-collected individuals from South Africa (courtesy of Dr. R. Kfir, Plant Protection
Institute, Pretoria). Parasitoids were housed at 27⬚C, under natural daylight, and fed with
honey. A laboratory stock of potato tuber moth (PTM) was housed at 27⬚C, under natural
daylight, and fed with honey and water. The PTM eggs were collected daily and were used
within 24 h, since the age of the eggs is known to influence the parasitoids’ oviposition
decisions (Ode and Strand, 1995). Wasps were used within 3 days of emergence.
Starvation experiment
To avoid bias in the number of developing wasps due to the sex of the clone or the presence
of a soldier larva, we used virgin females that produce male clones only. To reduce genetic
variability among embryos within a brood, hosts were singly parasitized. We placed one
PTM egg at the centre of a Petri dish. We then introduced a female to the plate and directed
her towards the host. This was done by rotating the Petri dish while holding it vertically,
using the tendency of wasps to walk upwards on vertical surfaces. Females that touched
the host with their antennae normally started ovipositing. The female was removed
immediately after oviposition. We added a slice of potato to each Petri dish and incubated
it at 29⬚C.
Parasitized hosts were randomly assigned to two treatments: control and starvation.
Hosts of the starvation treatment were starved on the eighth day after parasitism, during
the proliferative phase of the parasitoid larvae (Segoli et al., 2009a). Each moth larva from this
Brood size in a polyembryonic parasitoid wasp 261
sample was removed from the potato on the eighth day and kept in a Petri dish with a wet
cotton ball. Approximately 24 h later, the moth larvae were returned to individual Petri
dishes and were provided with a slice of potato. A group of parasitized moth larvae that
were not starved served as a control.
Samples of hosts from each treatment were dissected at 2-day intervals following the
timing of starvation (days 10, 12, and 14 post-parasitism). At each dissection we recorded
host mass and counted the number of developing wasps inside the host. The remaining host
larvae were kept until wasp pupation and emergence. Hosts were checked daily and the
timing of wasp pupation, together with the mass of mummy at wasp pupation (including
all the wasps that pupated inside it), were recorded. Mummy mass at wasp pupation
may represent the carrying capacity of the host, since at this stage all of the resources
accumulated by the host during its growth are allocated to the wasp progeny. Following
emergence, we counted the number of wasps per brood, and measured the head width of
five wasps per host using the integrated Soft Imaging Software (SIS) image analysis package
(Soft Imaging Software, GmbH, Münster, Germany). The experimental design is shown
in Fig. 1.
Some of the hosts (N=36) that developed on potatoes were apparently non-parasitized
(no developing wasps were found inside the host at dissection, or the larva developed into a
moth). These hosts were removed from the data set. Thus, we were able to obtain data from
57 hosts of the control treatment (n=6 for day 10, n=14 for day 12, n=18 for day 14, and
n=19 that pupated), and 52 hosts of the starvation treatment (n=12 for day 10, n=11
for day 12, n=13 for day 14, and n=16 that pupated). In several cases, we failed to
obtain measures of variables such as host mass, wasp number or time to pupation; thus,
accordingly, samples were further reduced.
Statistical analyses
We used two-way analysis of variance (ANOVA) to test the effects of the starvation
treatment and the developmental stage on host mass and on the number of wasps per
host. We used one-way ANOVA to test the effect of the starvation treatment on the time
until pupation, and on the size of emerging wasps. We used linear regression to test the
relationships between number of wasps per host and host mass at different developmental
stages for control and starved hosts combined. Similarly, we used linear regression to test
the relationships between the number of emerging wasps and wasp size, for control and
starved hosts combined.
Fig. 1. Experimental design: the timing of host starvation and dissections. Starvation was conducted
over 24 h starting at day 8 after parasitism and a sample of host larvae from this treatment was
dissected on days 10, 12, and 14. A sample of control hosts was dissected at days 10, 12, and 14.
In addition, a sample from each treatment was kept until pupation and emergence.
Segoli et al.262
RESULTS
The effect of starvation on host mass
The mass of parasitized hosts was significantly affected both by starvation and by timing
after parasitism (including days 10, 12, 14, and upon pupation) (Treatment: F1,94 =11.4,
P=0.001; Day: F3,94 =40.1, P<0.001; Treatment ×Day: F3,94 =2.6, P=0.06; two-way
ANOVA) (Fig. 2). Mass of hosts increased throughout development and decreased again
for mummified hosts, probably due to the loss of water at this stage. The negative effect of
starvation on host mass was consistent through all developmental stages, but its magnitude
decreased towards the final stage.
The effect of starvation on the number of wasps
There was a trend for starved hosts to contain fewer wasps than control hosts. In addition,
the number of wasps was significantly affected by the day after parasitism (Treatment:
F1,92 =3.1, P=0.08; Day: F3,92 =10.2, P<0.001; Treatment ×Day: F3,92 =0.4, P=0.74;
two-way ANOVA) (Fig. 3). The day effect was probably due to the larger number of wasps
upon emergence than found at dissections.
The effect of starvation on the timing of pupation
Wasps developing in starved hosts pupated later than those developing in control hosts
(one-way ANOVA: F1,29 =4.8, P=0.04; 17.9 ±0.6 days for control hosts and 18.5 ±0.8 days
for starved hosts; mean ±..).
Fig. 2. Mass of control (triangles) and starved (squares) hosts (mean ±..). Starvation was
conducted over 24 h starting at day 8 after parasitism. Measurements were taken at 2-day intervals
following host starvation (days 10, 12, and 14) and upon wasp pupation.
Brood size in a polyembryonic parasitoid wasp 263
The effect of starvation on the size of emerging wasps
Starvation had no significant effect on the head width of emerging wasps (one-way
ANOVA: F1,29 =0.57, P=0.46; 459 ±26 µm for control hosts and 450 ±40 µm for starved
hosts; mean ±..).
The effect of host mass on the number of wasps
Pooling control and starved hosts, we found no significant relationship between host mass
and the number of developing wasps per host at any timing of dissection (linear regression,
Day 10: n=11, R2=0.06, P=0.33; Day 12: n=23, R2=0.05, P=0.96; Day 14: n=30,
R2=0.04, P=0.15). We found a marginally non-significant positive relationship between
mass of mummy and the number of emerging wasps (linear regression, number vs. mass:
n=31, R2=0.09, P=0.06). Furthermore, we found a significant negative relationship
between the number of emerging wasps and wasp head width (linear regression, n=31,
R2=0.42, P<0.001).
DISCUSSION
Polyembryonic development was suggested to represent a counter-adaptation for parents’
inability to predict the future carrying capacity of their offspring’s environment (Craig et al.,
1997). One prediction that emerges from this hypothesis is that the offspring are able to adjust
their numbers according to environmental cues they experience during development. In this
study, we tested whether offspring of the polyembryonic parasitoid wasp C. koehleri adjust
their numbers to the body condition of the host. The results did not strongly support
our predictions: although starvation had a significant effect on host mass throughout
development, it only had a minor effect on the number of wasps per host.
Fig. 3. Wasp brood size inside control (triangles) and starved (squares) hosts (mean ±..). Starvation
was conducted over 24 h starting at day 8 after parasitism. Measurements were taken by dissecting
hosts at 2-day intervals following host starvation (days 10, 12, and 14) and upon wasp emergence.
Segoli et al.264
Starved hosts tended to contain fewer wasps than control hosts, but this effect was not
significant and was only apparent at some of the developmental stages (e.g. days 10 and 14).
This may in part be explained by the relatively small sample size resulting in a low power of
the test (power =0.42 for the effect of treatment), but nevertheless suggests that the effect
of starvation on the number of wasps is less strong than its effect on host mass. In addition,
there was no significant relationship between host mass and the number of wasps per host
during development. This may suggest that embryos of C. koehleri cannot fully assess, or do
not strongly respond to, the host’s body condition.
Although there was no relationship between brood size and host mass during
development, we found a marginally non-significant positive relationship between the
final carrying capacity of the host (mummy mass) and the number of emerging wasps.
This positive relationship, although weak, may indicate that wasps affect the carrying
capacity of the host according to their numbers, rather than adjusting their numbers to the
host. Indeed, gregarious parasitoids are known to increase consumption by their hosts,
resulting in a larger mass for parasitized versus non-parasitized hosts (Slansky, 1986). There
are several examples for increased body mass by hosts parasitized by Copisodoma species
[e.g. C. floridanum (Strand, 1989); C. bakeri (Byers et al., 1993); C. koehleri (Segoli et al., 2009a)]. More-
over, in C. koehleri there is evidence that host mass increases according to the number
of developing wasps in their body, as hosts parasitized twice (containing two wasp clones)
are heavier than hosts parasitized once (Segoli et al., 2009b). This effect may reduce the adaptive
value of brood size adjustment at earlier stages.
The combined results suggest that hosts largely compensated for the loss of mass due to
starvation: at days 12 and 14 starved hosts weighed ∼40% less than control hosts compared
with only ∼15% less upon pupation. In accordance, starvation had no effect on the size
of the emerging wasps. Delayed pupation might have allowed starved hosts to compensate
for the loss of mass by increased consumption. It is possible that a stronger treatment
[such as longer starvation, as applied by Giron et al. (2004)] might have had a larger impact on
host carrying capacity than observed in our study. However, the proliferation phase of
C. koehleri occurs mostly during the host second instar (Segoli et al., 2009a). At this stage, host
larvae rarely survive starvation for more than 24 h (M. Segoli, personal observation). Thus, it
seems that longer starvation is not relevant at the proliferation phase of this wasp. Other
manipulations might elicit a stronger response through proliferation levels. For example, the
quality of the host diet, rather than starvation, could perhaps provide reliable information
on the future carrying capacity of the host (Ode, 2006). Finally, in species with larger broods, in
which the proliferation phase is longer [e.g. C. floridanum (Strand, 2003)], offspring may better
adjust their numbers to the conditions inside the host.
One puzzling result was that the number of wasps per host at emergence was larger than
their numbers at day 14. Such a result was unexpected and was not observed in a previous
study (Segoli et al., 2009a), although the trend was similar. There are two possible explanations
for this result: first, we might have overlooked some of the larvae during dissections, but this
is unlikely because at day 14 larvae are relatively large and conspicuous; second, smaller
broods were perhaps less probable to survive to emergence (Ode and Strand, 1995). Unfortunately,
we did not keep a record of hosts that died before the final stage, as it was often impossible to
find their remains in the potato to determine the stage at which they perished.
In summary, our results do not strongly support the hypothesis that offspring of the
polyembryonic wasp C. koehleri adjust their number according to the body condition of
their host. However, the results suggest that the applied starvation manipulation was not
Brood size in a polyembryonic parasitoid wasp 265
a strong indicator of the host carrying capacity. The observed trend for smaller broods
in starved hosts suggests that offspring have some ability to adjust their numbers to their
immediate environment. This ability should be further investigated using additional
manipulations of host quality and other polyembryonic species.
ACKNOWLEDGEMENTS
We thank Derek Roff, Michael Strand, David Giron, Ori Becher, Sara Baranes, Adi Sadeh, Daphna
Gottlieb, Snir Yehuda, Ittai Malca, Shalhevet Azriel, Na’ama Morag, and Moran Segoli for assistance
and discussions. This study was supported by the Israel Science Foundation (grant #184/06).
REFERENCES
Beckage, N.E. and Riddiford, L.M. 1983. Growth and development of the endoparasitic wasp
Apanteles congregatus: dependence on host nutritional-status and parasite load. Physiol.
Entomol., 8: 231–241.
Bergstrom, A., Janz, N. and Nylin, S. 2006. Putting more eggs in the best basket: clutch-size
regulation in the comma butterfly. Ecol. Entomol., 31: 255–260.
Byers, J.R., Yu, D.S. and Jones, J.W. 1993. Parasitism of the army cutworm, Euxoa auxiliaris (Grt)
(Lepidoptera, Noctuidae), by Copidosoma bakeri (Howard) (Hymenoptera, Encyrtidae) and
effect on crop damage. Can. Entomol., 125: 329–335.
Chong, J.H. and Oetting, R.D. 2006. Host stage selection of the mealybug parasitoid Anagyrus
sp. nov near sinope. Entomol. Exp. Appl., 121: 39–50.
Craig, S.F., Slobodkin, L.B., Wray, G.A. and Biermann, C.H. 1997. The ‘paradox’ of polyembryony:
a review of the cases and a hypothesis for its evolution. Evol. Ecol., 11: 127–143.
Cruz, Y.P. 1981. A sterile defender morph in a polyembryonic hymenopteran parasite. Nature, 294:
446–447.
Cruz, Y.P. 1986. Development of the polyembryonic parasite Copidosomopsis tanytmemus
(Hymenoptera: Encyrtidae). Ann. Entomol. Soc. Am., 79: 121–127.
Doutt, R.L. 1947. Polyembryony in Copidosoma koehleri Blanchard. Am. Nat., 81: 435–453.
Doutt, R.L. 1952. The teratoid larva of polyembryonic Encyrtidae (Hymenoptera). Can. Entomol.,
84: 247–250.
Eggers, S., Griesser, M., Nystrand, M. and Ekman, J. 2006. Predation risk induces changes in
nest-site selection and clutch size in the Siberian jay. Proc. R. Soc. Lond. B, 273: 701–706.
Giron, D., Dunn, D.W., Hardy, I.C.W. and Strand, M.R. 2004. Aggression by polyembryonic wasp
soldiers correlates with kinship but not resource competition. Nature, 430: 676–679.
Godfray, H.C.J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ: Princeton
University Press.
Godin, C. and Boivin, G. 2000. Effects of host age on parasitism and progeny allocation in
Trichogrammatidae. Entomol. Exp. Appl., 97: 149–160.
Grbic, M., Nagy, L.M. and Strand, M.R. 1998. Development of polyembryonic insects: a major
departure from typical insect embryogenesis. Dev. Genes Evol., 208: 69–81.
Hamilton, W.D. 1963. The evolution of altruistic behaviour. Am. Nat., 97: 354–356.
Hamilton, W.D. 1964. The genetical evolution of social behaviour. I & II. J. Theor. Biol., 7:
1–52.
Harvey, J.A. 2005. Factors affecting the evolution of development strategies in parasitoid wasps:
the importance of functional constraints and incorporating complexity. Entomol. Exp. Appl.,
117: 1–13.
Harvey, J.A., Harvey, I.F. and Thompson, D.J. 1995. The effect of host nutrition on growth and
development of the parasitoid wasp Venturia canescens. Entomol. Exp. Appl., 75: 213–220.
Segoli et al.266
Horne, P.A. 1990. The influence of introduced parasitoids on the potato moth, Phthorimaea
operculella (Lepidoptera: Gelechiidae) in Victoria, Australia. Bull. Entomol. Res., 80: 159–163.
Kagata, H. and Ohgushi, T. 2002. Clutch size adjustment of a leaf-mining moth (Lyonetiidae:
Lepidoptera) in response to resource availability. Ann. Entomol. Soc. Am., 95: 213–217.
Keasar, T., Segoli, M., Barak, R., Steinberg, S., Giron, D., Strand, M.R. et al. 2006. Costs and
consequences of superparasitism in the polyembryonic parasitoid Copidosoma koehleri
(Hymenoptera: Encyrtidae). Ecol. Entomol., 31: 277–283.
Kfir, R. 2003. Biological control of the potato tuber moth Phthorimaea operculella in Africa.
In Biological Control in IPM Systems in Africa (P. Neuenschwander, C. Borgemeister and
J. Langewald, eds.). Wallingford, UK: CABI.
Lack, D. 1947. The significance of clutch size. Ibis, 89: 309–352.
Mayhew, P.J. and Glaizot, O. 2001. Integrating theory of clutch size and body size evolution for
parasitoids. Oikos, 92: 372–376.
Nagano, M. and Suzuki, S. 2007. Effects of carcass size and male presence on clutch size in
Nicrophorus quadripunctatus (Coleoptera: Silphidae). Entomol. Sci., 10: 245–248.
Ode, P.J. 2006. Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy
interactions. Annu. Rev. Entomol., 51: 163–185.
Ode, P.J. and Strand, M.R. 1995. Progeny and sex allocation decisions of the polyembryonic wasp
Copidosoma floridanum. J. Anim. Ecol., 64: 213–224.
Pexton, J.J. and Mayhew, P.J. 2005. Clutch size adjustment, information use and the evolution of
gregarious development in parasitoid wasps. Behav. Ecol. Sociobiol., 58: 99–110.
Reitz, S.R. and Adler, P.H. 1995. Fecundity and oviposition of Eucelatoria bryani, a gregarious
parasitoid of Helicoverpa zea and Heliothis virescens. Entomol. Exp. Appl., 75: 175–181.
Sato, Y., Tagawa, J. and Hidaka, T. 1986. Effects of the gregarious parasitoids, Apanteles ruficrus and
Apanteles kariyai, on host growth and development. J. Insect Physiol., 32: 281–286.
Segoli, M., Bouskila, A., Harari, A.R. and Keasar, T. 2009a. Developmental patterns in the
polyembryonic parasitoid wasp Copidosoma koehleri. Arthropod Structure Dev., 38: 84–90.
Segoli, M., Harari, A.R., Bouskila, A. and Keasar, T. 2009b. Brood size in a polyembryonic
parasitoid wasp is affected by relatedness among competing larvae. Behav. Ecol., 20: 761–767.
Slansky, F. 1986. Nutritional ecology of endoparasitic insects and their hosts: an overview. J. Insect
Physiol., 32: 255–261.
Strand, M.R. 1989. Development of the polyembryonic parasitoid Copidosoma floridanum in
Trichoplusia ni. Entomol. Exp. Appl., 50: 37–46.
Strand, M.R. 2003. Polyembryony. In Encyclopedia of Insects (R. Carde and V. Resch, eds.),
pp. 928–932. London: Academic Press.
Strand, M.R. and Casas, J. 2008. Parasitoid and host nutritional physiology in behavioral ecology.
In Behavioral Ecology of Insect Parasitoids (E. Wajnberg, C. Berstein and J. van Alphen, eds.),
pp. 113–128. Oxford: Blackwell.
Wang, X.Y., Yang, Z.Q., Wu, H. and Gould, J.R. 2008. Effects of host size on the sex ratio, clutch
size, and size of adult Spathius agrili, an ectoparasitoid of emerald ash borer. Biol. Control, 44:
7–12.
Brood size in a polyembryonic parasitoid wasp 267
