(p.b.e.

) — BER — 88/3–4 — ISSUE — ( 850084 ) —MS 0622

Bulletin of Entomological Research (1998) 88, 299–304 299

The influence of host quality on

progeny and sex allocation in the pupal
ectoparasitoid, Muscidifurax raptorellus
(Hymenoptera: Pteromalidae)
J.A. Harvey* and G.J.Z. Gols
Department of Entomology, Wageningen Agricultural University,
PO Box 8031, 6700 EH Wageningen, The Netherlands

Abstract

Muscidifurax raptorellus Kogan & Legner is a gregarious pteromalid

ectoparasitoid that attacks pupae and pharate adults from several families of the
higher Diptera. Egg-to-adult development time, adult parasitoid size and emerging
offspring ( = secondary) sex ratio of M. raptorellus were compared with clutch size
in two hosts that differed greatly in mass, the small Musca domestica Linnaeus and
the larger Calliphora vomitoria Linnaeus. The mean number of emerging parasitoids
did not vary significantly with host species, although slightly higher clutch sizes
were recorded in C. vomitoria. Irrespective of offspring sex, parasitoids completed
development more rapidly in M. domestica than in C. vomitoria. In the small host,
the development time and adult size of M. raptorellus were negatively correlated
with clutch size. By contrast, female parasitoid size was unaffected by clutch size
in the larger host, C. vomitoria. In both hosts, female parasitoids were significantly
larger than male parasitoids. The secondary sex ratio (percentage males) of
emerging parasitoids was significantly lower in C. vomitoria, and varied with clutch
size in both hosts. In C. vomitoria, the greatest proportion of females emerged from
hosts with the highest clutch sizes, whereas in M. domestica hosts with the highest
clutch sizes produced the lowest proportion of female progeny. The results
described here show that the development of M. raptorellus is profoundly affected
by interspecific differences in host quality. Our results suggest that mating
structure and host quality have potentially different effects on sex ratio decisions
in M. raptorellus, and perhaps other gregarious parasitoids.

Introduction female parasitoids to manipulate the sex of the offspring at

Many empirical and theoretical studies using hy-
menopterous parasitoids have suggested that differences in
the sex ratio can have important fitness-related consequences
(reviewed by King, 1987; Hardy, 1992, 1994 and Godfray,
1994). Parasitoids are excellent organisms for sex ratio
studies, because their haplodiploid sex determination allows
*Address for correspondence: Department of Entomology,
University of Wisconsin-Madison, 739 Russell Laboratories, 1630
Linden Drive, Madison, Wisconsin 53706, USA.
Fax: 608 262 3222
E-mail: harvey@entomology.wisc.edu
oviposition. Unfertilized eggs develop into males and
fertilized eggs into females. Much attention has concentrated
on gregarious parasitoids (which habitually lay two or more
eggs per host) where the sex ratio is frequently female-biased
(Griffiths & Godfray, 1988; Hardy & Cook, 1995). Two major
interactive factors which influence the sex ratio of parasitoids
at oviposition are local mate competition and the influence
of host quality. In local mate competition, it is assumed that
the optimal mean progeny sex ratio depends on the number
of females (or foundresses) colonizing a patch, and
contributing their own progeny to the mating group
(Hamilton, 1967). When there are few foundresses, an
300 J.A. Harvey and G.J.Z. Gols
ovipositing female should only produce enough sons to
ensure that all of her daughters are inseminated. Thus, if a
single male can mate with all of his female siblings, the
predicted sex ratio (proportion of sons) should consist of one
male and the remainder female (Griffiths & Godfray, 1988).
The influence of host quality on parasitoid growth and
development has attracted considerable experimental atten-
tion in recent years (see reviews by Mackauer & Sequeira,
1993, Godfray, 1994, and Jervis & Copland, 1996). Host
quality is defined as the state or condition of the host that
influences the dynamic processes of parasitoid growth,
development and survival to adult. The quality of a host
depends on a number of physiological factors, including the
presence of toxins, competing parasitoids and disease
organisms, all of which may affect the nutritional status of
the host (Vinson & Iwantsch, 1980; Vinson, 1988). Optimality
models have frequently examined the influence of host
quality on sex allocation in parasitoids (Charnov, 1979, 1982).
They predict that, in situations where host quality
differentially influences the fitness of males and females, the
least adversely affected sex should be laid into poor quality
hosts, and the most adversely affected sex should be laid into
high quality hosts. It is generally agreed that fitness returns
in large females are greater than in correspondingly large
males (Godfray, 1994), because size is often positively
correlated with egg production and lifetime reproductive
success in female parasitoids (Jervis & Copland, 1996). Male
fitness may also be greater in large than in small individuals,
but there is a broad consensus that small size is less of a
disadvantage in males than in females.
Muscidifurax raptorellus Kogan & Legner (Hymenoptera:
Pteromalidae) is a gregarious parasitoid which develops
externally (but within the host’s puparium) on pupae and
pharate adults from several families of the higher Diptera,
including the Muscidae, Calliphoridae and Sarcophagidae.
The parasitoid injects venom into the host prior to
host-feeding or oviposition (Legner, 1987) which induces
developmental arrest that is sustained until host death
(Rivers & Denlinger, 1995). In a previous study, we examined
the relationship between secondary clutch size and the
development of M. raptorellus attacking standard-sized and
aged pupae of the housefly, Musca domestica Linnaeus
(Diptera: Muscidae) and found that parasitoid size decreased
with an increase in parasitoid load (Harvey et al., in press).
Here, we compare the development of M. raptorellus in
M. domestica and in a second, and much larger host, Calliphora
vomitoria Linnaeus (Diptera: Calliphoridae). This is the first
study ever to compare the development of M. raptorellus in
different sized host species. Our data show that qualitative
differences in host species affect parasitoid performance, and
that M. raptorellus responds to differences in host nutritional
conditions by controlling egg fertilization (i.e. sex ratio). We
reveal that, when laying clutches of five or more eggs per
host, the parasitoid lays a higher proportion of female eggs
in the larger host species (C. vomitoria) than in the smaller
host species (M. domestica), suggesting that sex ratio
decisions in M. raptorellus are strongly influenced by host
quality under conditions of local mate competition.
Materials and methods
Hosts and parasitoids used in experiments were
maintained at 25°C with a 12:12 h L : D photocycle. Adult M.
domestica were maintained in steel cages (40 × 23 × 25 cm) at
a density of approximately 100 flies per cage. They were fed
a 2:2:1 mixture of sugar, powdered milk and yeast. Water
was constantly supplied in a small Petri dish. Flies
oviposited into a mixture consisting of 3 g of powdered milk
and one litre of water absorbed into paper towel. Eggs were
removed daily from the cages, and larvae were reared in 1 kg
jars on the following diet:
(A) a mixture of 265 g yeast, 265 g powdered milk and
1400 ml water;
(B) 54 g agar and 1400 ml water, mixed and boiled.
(A) and (B) were mixed and left for approximately 30 min
before being poured into the jars. Eggs were added to the
food medium, which was then covered by a 10 cm layer of
fine sawdust. Pupae were isolated from the medium after
four to five days using sieves, and eclosing adult flies
transferred to other cages for culturing.
Calliphora vomitoria pupae used in experiments were
reared by a supplier in Drenthe, the Netherlands. Flies were
cultured by allowing the adult females to oviposit directly
onto decaying meat. Flies were sent to Wageningen as
pre-pupae; because we could only obtain small numbers of
hosts at a time from our supplier, the pre-pupae were stored
in a refrigerator (3°C) after pupation but before presentation
to parasitoids. This slows developmental changes that occur
within the puparium that may reduce the quality of these
hosts. Hosts stored for more than ten days under these
conditions were not used in our experiments.
Muscidifurax raptorellus were reared in small glass vials
(1 cm diameter) containing approximately 50 pupae of
M. domestica. Several male and female parasitoids were
placed in the vials with the host pupae, and sealed with a
plug of cotton wool; newly-emerged parasitoids were
transferred to separate vials containing fresh host pupae.
Experimental protocol
Host pupae were selected for experiments according to
age and size. We intentionally used standard-sized hosts
from each species for two reasons. First, this allows for a
direct comparison of interspecific host quality on parasitoid
development. Secondly, it is very difficult to determine
accurately the proportion of each host which is actually
accessible as food to the immature parasitoids, i.e. the
thickness of the cuticle varies between individual hosts, and
this is not consumed by the parasitoid larvae. All
M. domestica pupae were thus one to two days old and
between 5.8 and 6.2 mm long, measured on a calibrated
microscope at ×1.2. C. vomitoria pupae presented to
parasitoids were all between 8.5 and 9.5 mm long, measured
on a calibrated microscope at ×1.2. Muscidifurax raptorellus is
a synovigenic, host-feeding parasitoid and proteins from the
host’s haemolymph are a necessary pre-requisite for
prolonged egg maturation after eclosion (see Jervis & Kidd,
1986, for a review). Since the ovaries of newly-emerged
female parasitoids contain few fully-developed eggs (J.A.
Harvey, personal observations), we allowed female para-
sitoids to host-feed for three days and mature further eggs
prior to the commencement of the experiment. Groups of
newly-eclosed adult male and female M. raptorellus were
placed into plastic vials (3 cm diameter) containing several
M. domestica and C. vomitoria pupae for three days. Honey
was smeared on the inside of the vials.
 Host quality and sex ratio decisions in Muscidifurax raptorellus 301
Table 1. Secondary sex ratio (percentage female emergence) of parasitoids emerging from C. vomitoria being female,
Muscidifurax raptorellus from Calliphora vomitoria and Musca compared with 60% from M. domestica. A 2 × 2 × 3 contin-
domestica as a function of clutch size. gency table (G-test) was used to analyse offspring sex ratio
Clutch size Host species in M. raptorellus, with host species, parasitoid sex and clutch
size as factors. The overall test of independence was rejected
n C. vomitoria n M. domestica (G = 63.17, d.f. = 7, P < 0.01), showing that the offspring sex
1–2 31 52 43 54 ratio varied significantly with host species and clutch size.
3–4 93 80 68 75 Furthermore, there were significant interactions between
5+ 233 81 110 52 host species and offspring sex (G = 22.45, d.f. = 1, P < 0.01) and
Overall 357 76 221 60 clutch size and offspring sex (G = 14.64, d.f. = 1, P < 0.01). The
lowest percentage of female parasitoid emergence occurred
in M. domestica with five or more parasitoid larvae (52%);
Effect of host species and clutch size on the development time conversely, the opposite effect was observed in C. vomitoria,
and adult size of M. raptorellus where 81% of eclosing parasitoids were female.
The mean number of emerging parasitoids did not vary
After three days, the mated female parasitoids were significantly with host species (t = 1.74, d.f. = 126, P > 0.05),
placed individually in small plastic dishes (8 × 3 cm) although C. vomitoria contained slightly larger parasitoid
containing five to ten M. domestica or C. vomitoria pupae. clutches (4.4) than M. domestica (3.6). Figure 1 shows that
After 24 h exposure to parasitoids, host pupae were placed whereas M. raptorellus typically laid clutches of two to three
individually into plastic vials until parasitoid eclosion. Vials eggs in the smaller host species (M. domestica), in the larger
were checked several times daily (until 1700 h) for parasitoid host species (C. vomitoria) the parasitoid usually laid clutches
emergence; eclosing parasitoids were killed by freezing, of three to five eggs per host.
sexed, and oven dried for three days at 100°C before being
weighed individually on a Cahn 33 electronic microbalance
(accuracy 0.001 mg). At least 50 female parasitoids were used Effect of host species and clutch size on the egg-to-adult
over several weeks to obtain the complete data set.
development time of M. raptorellus
A three-way ANOVA was performed for parasitoid
development time with clutch size, offspring sex and host
Results
species as factors. Parasitoid development time varied
Sex-ratio and clutch size of M. raptorellus emerging from significantly with clutch size (F = 3.03, d.f. = 2, 300, P < 0.05),
host species (F = 234.04, d.f. = 1, 300, P < 0.0001) and offspring
C. vomitoria and M. domestica
sex (F = 60.61, d.f. = 1, 300, P < 0.0001; fig. 2a,b). Moreover,
Table 1 shows the proportion of emerging adult female there was a significant interactive effect between offspring
parasitoids (%) of M. raptorellus as a function of clutch sex and host species on the development time of
size. Percentage female eclosion was significantly higher M. raptorellus (F = 10.63, d.f. = 1, 300, P < 0.001) although other
in parasitoids emerging from C. vomitoria than from interactions were not significant (P > 0.05). Both adult male
M. domestica (x2 = 23.58, d.f. = 1, P < 0.01; table 1) with 76% of and female parasitoids reared from M. domestica emerged

Fig. 1. Percentage distribution of clutch sizes laid by Muscidifurax raptorellus in Musca domestica and Calliphora vomitoria pupae. Sample
sizes: M. domestica = 60; C. vomitoria = 81.
302 J.A. Harvey and G.J.Z. Gols
(a)
Fig. 2. Mean egg-to-adult development time, in days, of (a) male,
and (b) female Muscidifurax raptorellus emerging from Musca
domestica and Calliphora vomitoria containing different numbers
of parasitoids. Data from hosts containing five parasitoids or
more was pooled. Line bars represent standard error of the
mean. Sample sizes as indicated above each bar in the figure.
one to three days earlier than parasitoids reared from
C. vomitoria. Intraspecifically, male parasitoids completed
development more rapidly than female parasitoids
(fig. 2a,b). Furthermore, parasitoids developing in
M. domestica completed development faster as parasitoid
load increased, although this effect was less clear in
parasitoids reared from C. vomitoria (fig 2a,b).
Effect of host species and clutch size on adult parasitoid size
(dry mass) of M. raptorellus
A three-way ANOVA on emerging adult parasitoid size,
with clutch size, offspring sex and host species as factors
(a)
Fig. 3. Mean adult parasitoid size (dry mass in mg) of (a) male,
and (b) female Muscidifurax raptorellus emerging from Musca
domestica and Calliphora vomitoria containing different numbers
of parasitoids. Data from hosts containing five parasitoids or
more was pooled. Line bars represent standard error of the
mean. Sample sizes as indicated above each bar in the figure.
revealed that parasitoid size varied significantly with clutch
size (F = 14.30, d.f. = 2, 300, P < 0.0001) and offspring sex
(F = 84.93, d.f. = 1, 300, P < 0.0001) but not between the two
host species (F = 1.41, d.f. = 1, 300, P > 0.05; fig. 3a,b). A
significant interactive effect occurred between clutch size
and host species (F = 13.23, d.f. = 2, 300, P < 0.0001) and clutch
size and offspring sex (F = 9.62, d.f. = 2, 300, P < 0.0001) on the
adult size of M. raptorellus. The effect of clutch size on the
emerging adult size of M. raptorellus was more apparent in
M. domestica than C. vomitoria, with the smallest male and
 Host quality and sex ratio decisions in Muscidifurax raptorellus
female parasitoids emerging from hosts containing five
parasitoids or more (fig. 3a,b). However, irrespective of
offspring sex, parasitoids emerging from M. domestica
containing one to two parasitoid larvae were much larger
than parasitoids emerging from C. vomitoria containing the
same number of parasitoid larvae (fig. 3a,b).
Discussion
Interspecific differences in qualitative and quantitative
aspects of host physiology and nutrition clearly affected
the development of M. raptorellus. Parasitoids completed
development more rapidly in M. domestica than in
C. vomitoria (fig. 2) with males emerging earlier than females.
Furthermore, the largest parasitoids recorded in this study
eclosed from the smaller host species, M. domestica, with the
lightest parasitoid loads (fig. 3). However, whereas adult
parasitoid size decreased markedly with clutch size in
M. domestica, the size of parasitoids emerging from
C. vomitoria was fairly uniform, irrespective of clutch size per
host (fig. 3). Male parasitoids were also consistently smaller
than their female counterparts. Interspecific differences in
host quality suggest that parasitoid development is con-
strained by resource availability or by their inability to
acquire specific nutrients (Beckage & Riddiford, 1983;
Takagi, 1985). The reduced weight of parasitoids emerging
from M. domestica with heavy parasitoid loads was probably
attributable to a scramble-type competition for limited host
resources, where each parasitoid larva received less than
optimal quantities of food for their own development
(Waage & Ng, 1984; Taylor, 1988; Vet et al., 1994; Rivers &
Denlinger, 1995). By contrast, parasitoid size was less
affected by clutch size in C. vomitoria, presumably because
this host was considerably larger than M. domestica and
therefore resources did not become a limiting factor for
parasitoid development. Idiobiont parasitoids (which attack
non-growing or paralysed hosts, as opposed to koinobionts,
which attack growing, feeding hosts (Askew & Shaw, 1986))
lack the opportunity for increasing the food intake of the
host, and thus if the weight of the host is less than that
required by the parasitoids to achieve their optimal weight,
then the resulting parasitoids may suffer a reduction in body
weight, as was observed in parasitoids emerging from
M. domestica with heavy parasitoid loads.
Overall, significantly more male parasitoids emerged
from M. domestica than from C. vomitoria, and the secondary
sex-ratio of M. raptorellus was also strongly correlated with
parasitoid load in both hosts (table 1). The proportion of
emerging male and female offspring was similar in both
hosts containing up to four parasitoids, but in heavily
parasitized hosts significantly more female parasitoids
emerged from C. vomitoria than from M. domestica (table 1).
There are two possible reasons for the observed differences
in the secondary sex ratio of M. raptorellus: (i) the primary sex
ratio may be controlled by the ovipositing females (Charnov,
1979, 1982), or (ii) differential mortality between sons and
daughters may occur with concomitant variations in clutch
size, because one sex may exert a stronger competitive effect
on the other for host resources (therefore indicating that the
primary sex ratio is different from the secondary sex ratio;
Godfray, 1986; Ode & Strand, 1995). In many parasitoids, it
is not possible to assess the sex of eggs laid at oviposition.
However, differential mortality is unlikely since the sex ratio
varied differently with clutch size in both host species.
303
Therefore, it appeared that female parasitoids actively
controlled the brood sex ratios in both hosts.
Whereas across a range of clutch sizes the observed
secondary sex-ratio supports the predictions of local mate
competition models in C. vomitoria, in M. domestica they do
so only in hosts containing four or less parasitoids. In the
larger host, the proportion of emerging female parasitoids
increased significantly with a corresponding increase in
clutch size (table 1) whereas in M. domestica the proportion
of emerging female parasitoids increased intially with clutch
size, but then decreased sharply in the most heavily
parasitized hosts (table 1). The observed differences in the
sex ratio of M. raptorellus emerging from the two hosts
suggests that mating structure and host quality may have
profoundly opposite effects on sex ratio decisions in
gregarious parasitoids. Host quality, in terms of resources
per parasitoid larva, decreased with an increase in parasitoid
load in M. domestica, but not in C. vomitoria. Therefore, fitness
returns might have been reduced from the production of
single males and many daughters (under conditions of local
mate competition) in M. domestica with a high parasitoid
burden, because emerging female parasitoids would have
been very small, in comparison with larger females emerging
from hosts with lighter parasitoid loads. As male fitness is
less likely to be so adversely affected in small individuals
than female fitness (Godfray, 1994), the parasitoid mother
may assess host size and bias the sex ratio more towards
male offspring when laying larger clutches in M. domestica.
However, in C. vomitoria, resources were not limiting, hence
host quality was more-or-less uniform across a range of
clutch sizes. Consequently, the size of emerging females was
unaffected by variations in parasitoid load and the
conditions of fully local mating applied (Hardy, 1994).
Werren (1984) examined the influence of host quality under
fully local mating, and argued that the sex ratio is sensitive
to the proportion of low quality hosts among those
parasitized, and to the relative differences in fitness between
females developing in good and poor hosts.
In parasitoids, processes that influence growth, develop-
ment and ultimately fitness are usually dependent on the size
of the reproductive adult (Mackauer & Sequeira, 1993),
which suggests that body size is the main target of natural
selection. Several studies have reported that the body size of
adult females is closely related to their reproductive success
(reviewed by Godfray, 1994). Therefore, host quality is likely
to have a profound influence over the selection of hosts.
Assessment of the suitability of the puparium as an
oviposition site may be determined by the female parasitoid
only after ovipositor insertion into host tissues (Rivers &
Denlinger, 1995). An exception to this scenario may occur if
the parasitoid is able to measure the surface area and/or
volume of the puparium, as the egg parasitoid Trichogramma
minutum Riley (Hymenoptera: Trichogrammatidae) is
known to do (Schmidt & Smith, 1985). This enables the
parasitoid to assess the nutritional status of the host solely on
their physical parameters, and to manipulate clutch size and
sex ratio accordingly. However, it is probably unlikely that
a parasitoid can determine age-related variations in host
quality on the basis of surface measurements alone.
For idiobionts, the host represents a closed resource
environment, where host quality is largely a characteristic of
the host’s nutritional and developmental history and is
largely pre-determined at parasitism (Mackauer & Sequeira,
1993). Thus, for gregarious idiobiont species, parasitoid
304 J.A. Harvey and G.J.Z. Gols
fitness may be optimized on the basis of clutch size decisions
and control of sex ratio (Werren, 1984; Takagi, 1985; King,
1990). We have shown that M. raptorellus adaptively
manipulates the sex ratio of its progeny in response to
variations in clutch size in two hosts of different size. In hosts
with a low parasitoid burden, host quality did not vary
between the smaller host (M. domestica) or the larger host
(C. vomitoria). However, as parasitoid load increased,
competition for host resources became limiting in
M. domestica, but not in C. vomitoria, accounting for the
observed differences in offspring sex ratio. Further studies,
examining the reproductive strategy of M. raptorellus, may
determine how differences in host availability and type
influence parasitoid performance and lifetime reproductive
success.
Acknowledgements
We wish to thank Drs Mark Jervis and Louise Vet for
reviewing an early draft of the manuscript, Peter Mayhew
and Ian Hardy for discussion and Leo Koopman, Frans
van Aggelen, Andre Gidding and Hanneke van Heest
for technical support. The senior author wishes to
express his sincere thanks to the Royal Society (UK), for
their financial support through the European Exchange
Fellowship Programme.
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(Accepted 21 January 1998)
7 CAB INTERNATIONAL, 1998