Influence of host size on the clutch size and developmental success of the gregarious ectoparasitoid Eulophus pennicornis (Nees) (Hymenoptera: Braconidae) attacking larvae of the tomato moth Lacanobia oleracea (L.) (Lepidoptera: Noctuidae)
Central Science Laboratory, Sand Hutton, York, YO41 1LZ, UK
* Author for correspondence (e-mail: h.bell{at}csl.gov.uk)
Accepted 22 June 2005
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Summary |
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Key words: parasitoidhost interactions, oviposition behaviour, host selection, host regulation, Eulophus pennicornis, Lacanobia oleracea
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Introduction |
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Many factors can ultimately lead to the developmental success or failure of
a parasitoid's brood and affect the fitness of the ensuing progeny. For
example, overexploitation of a host through the oviposition of a large clutch
in or on a small host may lead to increased sibling competition and high
levels of mortality (Charnov and Skinner, 1983;
Vet et al., 1994;
Beckage and Gelman, 2001
).
Furthermore, large clutches for a given size of host reduce the unit of
resource available to each wasp larva, and can have a significant effect on
the ultimate fitness of those offspring that survive
(Vinson and Iwantsch, 1980a
;
Bezemer and Mills, 2003
). The
fitness of a parasitoid's progeny has frequently been linked to their size on
emergence as adults (Hardy et al.,
1992
; Visser,
1994
; Fidgen et al.,
2000
), and the ultimate fitness gain of a female parasitoid will
be determined by the numbers of a given clutch that ultimately survive and
their size (i.e. fitness) as adults
(Godfray, 1994
).
The factors that determine the clutch size that a female parasitoid will
oviposit in or on a host have been extensively researched. Such work has
demonstrated the importance of the ability of a female parasitoid to respond
to variations in host quality as a means of maximizing her lifetime fitness.
Several workers have demonstrated that the clutch sizes of gregarious
parasitoids are frequently correlated with the size of the host
(Takagi, 1986;
Hardy et al., 1992
; Zaviezo
and Mills, 2002) and that the survival of progeny may be either
density-dependent (Le Masurier,
1991
; Vet et al.,
1994
) or density independent
(Hardy et al., 1992
). Further
to this, within the range of host sizes that a parasitoid has the potential to
parasitize, the physiological status of the host may differ considerably and
thus may complicate the simplistic relationship between host size and clutch
size (Vinson, 1976
). As a
result, critical factors, such as the nutritional and endocrinological status
of the host, may come into play. This is an important consideration,
especially since many parasitoids actively manipulate the physiological status
of the host in order to facilitate the successful development of their progeny
(see reviews by Edwards et al.,
2001
; Beckage and Gelman,
2004
). Frequently, the success of such manipulation can be
affected by the host's physiological status at the time of parasitism and,
ultimately, the overall quality of the host can be seen to be a function of
several factors, and not necessarily just one of increasing host size
(Vinson and Iwantsch, 1980a
;
Rivers and Denlinger, 1995
;
Alleyne and Beckage, 1997
;
Husni and Honda, 2001
).
The gregarious koinobiont ectoparasitoid Eulophus pennicornis
(Nees) lays its eggs externally on the integument of late stadium larvae of
several species of noctuid hosts (Shaw,
1987). Studies into the basic biology of this parasitoid, when
parasitizing its usual laboratory host, the tomato moth Lacanobia
oleracea (L.), have largely used penultimate instar larvae (fifth larval
stadium), although final (sixth stadium) hosts were also reported to be
readily parasitized (Marris and Edwards,
1995
). No studies have elaborated on the ovipositional behaviour
of this wasp, however, or investigated how it adapts its egg clutches to the
size (and developmental stage) of the host. Despite the fact that this
parasitoid has been the subject of a number of biological studies (Bell et
al., 1999
,
2001
), no information is
available about the effect of parasitizing different larval stadia (i.e.
sizes) of L. oleracea on the reproductive success of the wasp, or on
how its ovipositional behaviour compares with the strategies of other
gregarious parasitoids.
For some ectoparasitoids, there is evidence that greater resource
availability (i.e. the size of the host) per egg increases the size, and
therefore the fitness, of the progeny that ensue
(Hardy et al., 1992;
Zaviezo and Mills, 2000
).
Therefore, attacking large hosts and provisioning the clutch with a greater
unit resource per egg could be considered adaptive if host quality was not
deleteriously affected by increased size. Recent work, investigating
koinobiont parasitoids, has made it apparent that host size at the time of
parasitism may have little bearing on the fitness functions of some species
(Harvey, 2000
;
Harvey et al., 2004
). However,
little information is available as to whether a similar situation occurs in
gregarious koinobiont ectoparasitoids. Furthermore, Harvey and Strand
(2002
) hypothesized that
progeny survival, not adult size, should be the primary selection target of a
parasitoid, with all other fitness traits rendered secondary to this tenet.
Here we report upon work designed to investigate the oviposition behaviour of
E. pennicornis, and test elements of this hypothesis by investigating
how host size and resource availability affects pre-adult survival and,
secondly, how progeny survival reflects host choice in this gregarious
ectoparasitoid species.
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Materials and methods |
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Effects of host size on clutch size
Newly ecdysed L5 and L6 larvae were taken from culture, placed individually
into ventilated 250 ml plastic pots (Cryovac Europe, Poole, UK) and provided
with a small cube of artificial diet. A single mated adult female E.
pennicornis (ca. 48 h old), which had had no previous exposure to hosts,
was introduced into each pot and a smear of 50% aqueous honey solution applied
to the lid to act as a food source. Each host was exposed to the wasp until
the latter had completed one oviposition. Any hosts that were not parasitized
after 4 days were discarded, as L. oleracea typically start to lose
mass and take on prepupal characteristics from the fourth day of the sixth
stadium onwards. Following oviposition, the parasitoid was removed and the
host weighed. The host was subsequently kept at 4°C for approximately 20
min to reduce activity, after which time it was anaesthetized with
CO2. Whilst immobile, the eggs present on each parasitized host
were counted under a binocular microscope. Each host was then returned to its
original pot and maintained until the parasitoid brood had completed
development, left the host and pupated. On pupation, all parasitoid pupae were
counted, the host cadaver removed to prevent contamination, and the wasp pupae
subsequently monitored for adult emergence. A total of 5060 parasitized
larvae of both the L5 and L6 stadia were monitored in this way.
|
Fixed host stadium experiments
To investigate how the availability of a restricted range of host sizes
affects the oviposition behaviour of E. pennicornis, the above
experiment was repeated using host cohorts comprising exclusively L4, L5 or L6
L. oleracea larvae. All methods were as above, except that as hosts
neared the end of the given stadium, and exhibited the signs of head capsule
slippage, they were removed and replaced with newly moulted insects of the
same stadium. Parameters measured were as described above.
|
Statistical analysis
Regression analysis of clutch size data was conducted using the
curve-fitting function of GraphPad Prism 4.01. All other statistical
procedures were carried out using StatsDirect 2.2.3. Differences between
parametric data sets were analysed by one-way analysis of variance (ANOVA) and
means separated by TukeyKramer HSD post-hoc tests. Prior to
ANOVA, all data was subjected to equality of variance tests and, where
variances differed significantly (P<0.05), data was
log-transformed. Comparisons between two data sets were conducted using
Student's unpaired t-tests and, in all cases, the accepted level of
significance was 5%.
|
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Results |
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Parasitized hosts were maintained until the parasitoid broods had pupated and adult wasps had subsequently emerged (Fig. 2A). Each parasitized larva was categorised as belonging to one of seven mass categories ranging from <0.1 g to >0.6 g. Increasing mass had a significant effect on both the numbers of eggs laid (F6,99=46.72, P<0.01) and the numbers of progeny that survived to adulthood (F6,99=7.69, P<0.01). The mean number of eggs oviposited increased with the size of the hosts such that caterpillars of 0.50.6 g received an average of 52.7±2.66 eggs as opposed to those of <0.1 g that received 11.7±1.27 eggs. As a result, hosts of >0.5 g received significantly larger clutches than larvae in all mass categories of <0.4 g (Tukey's HSD, P<0.01). However, the numbers of parasitoids that emerged as adults did not increase with the increasing size of the hosts above the 0.20.3 g category and, for the very highest mass category (>0.6 g), significantly fewer adults, at 8.1±4.28 per host, emerged than for hosts in categories of less than 0.3 g (Tukey's HSD, P<0.05). The marked decline in the proportion of wasps surviving in larger hosts (Fig. 2B) was a product of both increased larval mortality and an increased failure of adult parasitoids to emerge from the pupal stage. This was best illustrated by the largest hosts (>0.6 g) where, despite approximately 50% of the eggs ultimately developing to pupae, less than 16% of these gave rise to adults.
The unit mass of host per egg laid was seen to vary widely across the range of host sizes parasitized, from as little as 5 mg of host per egg to >20 mg per egg. Overall, with each successive increment in mass category, the average mass of host available to each egg increased. As such, for hosts of <0.1 g an average of 1 egg was laid for every 8 mg of host tissue whilst for hosts >0.6 g this value rose to almost 15 mg of host tissue per egg (results not shown). Regression analysis of the relationship between egg density and parasitoid survival showed that survival was independent of the unit mass of resource available per developing wasp (results not shown).
Brood sizes for parasitoids exposed to mixed and fixed stadium host populations
Host stadium had a significant effect on both the mean number of hosts
parasitized (F3,54=39.25, P<0.0001) and the
average number of eggs laid by each parasitoid
(F3,54=54.64, P<0.0001). When female E.
pennicornis were exposed to L4 hosts only, parasitism was negligible, and
only 2/14 parasitoids attacked any hosts
(Fig. 3A). The provision of L5
larvae increased the number of hosts parasitized such that, on average, 2.3
hosts were parasitized per wasp (N=14). Provision of mixed stadium
hosts, or L6 hosts only, resulted in averages of >7.0 hosts being
parasitized per wasp with no significant differences apparent (Tukey's HSD,
P>0.05) (N=15). The mean total numbers of eggs oviposited
followed the same trend as that of the number of hosts parasitized. Wasps
exposed to L4 hosts laid very few eggs, whilst those given L5 hosts oviposited
an average of 36.5±8.59 eggs each
(Fig. 3B). Parasitoids provided
with the mixed host populations, or with L6 larvae only, laid averages of
165.7±14.83 and 154.7±15.52 eggs, respectively. Exposure of
E. pennicornis females to a mixed population of L4L6 larvae
also provided a measure of the parasitoid's preference for attacking each of
the different stages of L. oleracea. Results reflected the rates of
parasitism recorded above, with the majority of attacks (>96%) occurring on
L6 hosts. All remaining attacks were against L5 larvae and no L4 larvae were
parasitized. The total number of hosts parasitized was significantly
correlated with the longevity of the female E. pennicornis when wasps
were exposed to either the mixed stage populations or L6 hosts only
(Fig. 3C,D). Similarly, the
number of eggs oviposited was also correlated with the longevity of the adult
wasp, although the relationship was non-linear due to a progressive reduction
in clutch sizes as the parasitoids aged (data not shown).
The relationship between clutch size and host size for parasitoids that were exposed to the mixed instar host population, or when restricted to L6 hosts only, is shown in Fig. 4. Exposure to the mixed population initially gave a significant non-linear asymptotic relationship of the type shown in Fig. 1, although non-linear regression explained only 43% of the variation. However, the relationship between host size and clutch size broke down over the reproductive lifetime of the parasitoid. The data were arbitrarily divided into the first three ovipositions for each wasp, and all subsequent egg laying events (Fig. 4A,B). In these experiments, it was apparent that, as the female parasitoids aged, their ability to adapt their clutch sizes to the size of the host declined. When the parasitoid was presented with a restricted host size range of L6 hosts only, no relationship was apparent at any time (Fig. 4C,D).
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When the mean clutch sizes were examined over time, a trend of average clutches in the region of 2535 eggs for the first two ovipositions was seen, followed by clutches of 2030 eggs for ovipositions 37 (Fig. 6A). This trend was more apparent in wasps exposed to the population of mixed stadium hosts than those provided with L6 hosts only, where clutch sizes were more variable and showed a general decline over time. When related to the mass of each host at oviposition, on average wasps provided with mixed host instars laid a single egg for approximately every 10 mg of host tissue (Fig. 6B). This trend held true for the first five ovipositions, after which time the ratios of host mass to clutch size increased. In the fixed stadium (L6 only) population, however, the trend broke down after the first two attacks, and the ratio of host mass to eggs laid increased to between 15 and 25 mg per egg laid from the third oviposition onwards. The individual clutch sizes over the entire reproductive lifetimes of the females are shown in Fig. 6C,D. For both the mixed stadium and the L6 only populations, the size of the clutches declined with time and became less variable. For mixed stadium hosts (Fig. 6C), clutch sizes ranged from 1161 eggs over the first 3 days, and 522 eggs for clutches laid from 10 days onwards. In the L6 hosts (Fig. 6D) a similar pattern was apparent with clutches of 1049 eggs oviposited during the first 3 days, whilst clutches laid from the tenth day onwards comprised 11 eggs or fewer.
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Discussion |
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The findings of the current study indicate that E. pennicornis similarly has the capacity to evaluate the size of a given host, and lay clutches of eggs that are in proportion to that host's size. This ability is not a learned response, and females with no previous oviposition experience show the same ability to adjust clutch size in response to host size as those that were allowed to parasitize hosts of mixed stadium populations over extended periods. However, the parasitoid's ability to match clutch size with host size was highly dependent on it being provided with host populations of a range of different sizes (i.e. different larval stadia) and, when given a restricted host range (i.e. L6 caterpillars only), no obvious trend for matching clutch size with host size was apparent.
The host encounter rate, and the variety (size and stadium) of hosts
available, can markedly affect the oviposition behaviour of a parasitoid
(Henry and Day, 2000;
Elzinga et al., 2005
). Here we
specifically examined the response of the parasitoid to populations of mixed
host stadia (with no host encounter constraints) compared to populations of
hosts comprising exclusively larvae of one of the three host stadia usually
attacked by this parasitoid. The availability of a range of hosts (of the
final three stadia) was seen to have a significant effect on the number of
hosts parasitized and the number of eggs oviposited over that seen in wasps
restricted to smaller (L4 and L5) hosts. Eulophus pennicornis is
synovigenic and can oviposit over 200 eggs during its reproductive life
(Bell et al., 2004
). When the
parasitoid was given a choice of host stadia, it almost always chose L6 L.
oleracea for parasitism. When presented with hosts of a single larval
stadium, only parasitoids provided with L6 hosts parasitized comparable
numbers of hosts, and laid similar numbers of eggs, to those exposed to the
mixed stadium populations. This would suggest that the wasp, in the absence of
larger hosts, does not compensate by parasitizing a greater number of smaller
insects. This suggests that the relatively long handling times involved in
parasitism, and the likelihood of hosts being naturally scarce, may impose
time constraints on the utilization of such hosts.
Despite the low rates of parasitism when the wasp was provided with L5
hosts only, the parasitoid frequently identified potential hosts at the end of
this stadium, as they neared ecdysis, and stayed with them in order to
oviposit immediately after the moult. This strategy effectively led to an
extended handling time (at least 24 h) for each of these hosts (which were, in
any case, removed prior to moulting to prevent any parasitism of L6 hosts).
This runs contrary to the suggestion that L5 larvae are avoided due to time
limitation constraints, and further highlights the fact that E.
pennicornis shows a preference for hosts that have just entered the sixth
larval stadium. Therefore, it would appear that the strategy of waiting for a
host to become acceptable is more profitable to the parasitoid than rejecting
it in order to search out a host that is immediately suitable for parasitism.
This strategy of identifying near acceptable hosts shortly prior to ecdysis
has similarly been observed in other Eulophid ectoparasitoids of lepidopteran
larvae (Shaw, 1981;
van Veen and van Wijk, 1987
).
The adjustments of clutch size relative to host size observed when E.
pennicornis was exposed to a range of sizes of host larvae (L4L6),
where identification of potential hosts just prior to the moult was allowed
for, and the absence of such relationships when hosts were restricted to a
single stadium, highlights the importance of this behaviour. Therefore, it
would appear that identifying hosts at a point prior to ecdysis is adaptive
and a major factor in the parasitoid adjusting clutch size to host size over
the duration of the parasitoid's life.
Female E. pennicornis emerge with approximately 6070
near-mature eggs within their ovaries. This initial egg load was probably
sufficient for the first two or three clutches. Subsequently, batches of eggs
were matured and each batch laid sequentially. Average clutch sizes for a
given oviposition event were mostly in the region of 2030 eggs per host
although, as the parasitoids aged, the clutch sizes became smaller. This could
indicate that the ability of the parasitoid to adjust clutch size in response
to host size may become limited by the supply of eggs in older individuals, as
is predicted by egg limitation models
(Godfray, 1994;
Rosenheim, 1999
). However,
whilst clutch size reduced with female age, the size range of hosts
parasitized remained largely unaltered. This was best illustrated by wasps
provided with mixed stadium hosts that, despite the declining size of their
clutches, continued primarily to choose L6 hosts of between 0.20.4 g
throughout their reproductive lifespans (over 70% of ovipositions fell within
this category). This may, therefore, suggest that choosing the correct
developmental stage of host is of greater importance to E.
pennicornis than accurately adjusting its clutch size to reflect the
absolute size of the host. The oviposition strategy of E. pennicornis
shares characteristics with several other gregarious ectoparasitoids
investigated (Uematsu, 1981
;
Henry ad Day, 2000
;
Zaviezo and Mills, 2000
) and
can be contrasted with work showing that some gregarious endoparasitoids
maximize reproductive fitness by producing relatively fixed clutch sizes
throughout their lives (Harvey,
2000
; Elzinga et al.,
2005
). However, despite the declining clutch sizes observed here,
in favourable host encounter conditions, the number of eggs laid per unit mass
of host remained, on average, remarkably constant until near the end of the
female's life. This would suggest that, although clutch sizes declined as the
females aged, E. pennicornis has evolved to accurately match clutch
size to the size of the host in order to minimize larval mortality through
scramble competition, which would potentially occur at high brood densities.
Examination of the relationship between egg density and parasitoid survival,
however, showed that wasp developmental success was independent from the
quantity of resource available to each developing parasitoid. This was largely
because the effect of host size on wasp survival far outweighed other
considerations and the true impact of egg density will probably be only
elucidated through the manipulation of clutch sizes upon fixed quality
hosts.
Many gregarious koinobiont parasitoids allow for significant growth of the
host following parasitism, and the number of progeny produced is frequently
correlated with the size that the parasitized host attains before parasitoid
egression (Beckage and Riddiford,
1983; Harvey,
2000
). For E. pennicornis, whilst clutch size was related
to the host mass at the time of oviposition, parasitized caterpillars were
seen to increase in size markedly following parasitism, although growth was
ultimately restricted in L5 larvae by the fact that they were unable to moult
following oviposition. Significant growth in both parasitized L5 and L6 hosts
was apparent, such that hosts increased in mass by as much as 60% before
feeding ceased, an aspect that may have been a factor in the degree of
variability observed between the host massclutch size relationships.
Moreover, this may lead to the possibility that clutch size was not only
determined by the size of the host at the time of parasitism, but by the
potential for growth subsequent to oviposition. This supposition could,
therefore, partially explain the fact that larger hosts (>0.5 g), which
have less potential for growth following parasitism, typically received fewer
eggs per unit mass than smaller hosts.
The fitness of parasitoid progeny (particularly female wasps) has been
equated with various measures of adult size, and such equations have generally
shown that fitness increases with the size of the wasps on reaching adulthood
(Waage and Ming, 1984;
Ueno, 1999
;
Fidgen et al., 2000
;
Rivero and West, 2002
). As a
result, the primary selection pressure driving the evolution of parasitoids is
often seen as one of maximizing the adult size of progeny, and oviposition
strategies have been presumed to maximize this trait
(Mackauer and Sequiera, 1993
;
Visser, 1994
). This assumption
frequently neglects pre-adult parasitoid mortality, however, and has recently
been challenged as oversimplistic. Harvey and Strand
(2002
) and Harvey et al.
(2004
) have emphasized that,
ultimately, the most important feature of parasitoid fitness is progeny
survival, and natural selection should drive wasps to accurately identify and
parasitized hosts that maximize pre-adult survival of their progeny. Here, we
observed a strategy in E. pennicornis that substantiates their
hypothesis, with host preference very closely reflecting progeny survival.
Host quality did not operate as a simple function of increasing host size
(i.e. the available resources), a principle similarly reported by Zaviezo and
Mills (2000
) when
investigating the oviposition behaviour of the Eulophid ectoparasitoid
Hyssopus pallidus (Askew). As a result, absolute fecundity in E.
pennicornis did not increase when hosts above a certain mass were
parasitized indeed the oviposition of large clutches onto hosts of
>0.6 g wasted a large proportion of the eggs laid due to high levels of
larval and pupal mortality. Therefore, whilst the available resource per egg
remained the same, or increased slightly, with successive increments in host
size, parasitoid survival decreased concomitantly and the parasitoid larvae
failed to benefit from the additional resource available to them. Whilst this
phenomenon could be equated with some inferred nutritional inferiority in
larger hosts, as Zaviezo and Mills
(2000
) have suggested, it is
equally plausible that the key element involved in this response to larger
hosts is the ability, or failure, of the parasitoid to physiologically
regulate the host following oviposition.
The ability of parasitoids to regulate their host's physiology is
frequently seen as critical to their reproductive success
(Vinson and Iwantsch, 1980b;
Beckage, 1985
;
Edwards et al., 2001
). In the
case of Eulophus pennicornis, manipulation of the host's physiology
is achieved through use of a non-paralysing venom that, most obviously,
prevents ecdysis in stung L5 larvae through modulation of ecdysteroid levels
(Weaver et al., 1997
;
Marris et al., 2001
).
Interestingly, in newly ecdysed L6 L. oleracea parasitized by E.
pennicornis, levels of juvenile hormone (JH) increase
100-fold
within 4 days of oviposition (J. Edwards, personal communication). This
suggests that the parasitoid manipulates the host's endocrinology to prevent
the physiological and behavioural changes associated with pupal commitment
that would normally occur if JH is absent during the early sixth stadium
(Nijhout, 1994
;
Edwards et al., 2001
). In the
current experiments, sixth instar larvae that were more than 2 or 3 days post
ecdysis at the time of parasitism were probably already committed to initiate
pre-pupation behaviour (burrowing, wandering, cessation of feeding), and these
changes may have been very important factors in reducing the survival of
parasitoids developing on these larger hosts. Alternatively, a number of
reports have indicated that ectoparasitoid venoms may play an important role
in the altering the nutritional composition of the host's haemolymph
(Coudron et al., 1998
;
Nakamatsu and Tanaka, 2004
).
It is possible that similar processes may occur in the hostparasitoid
under investigation here, and such nutritional manipulations could, again, be
highly dependent on the time of parasitism. If this is the case, the ability
of E. pennicornis to successfully regulate the host, and thus
generate a nutritionally and physiologically favourable environment for the
development of its progeny, may be the principle determinant of host choice
and developmental success. In this scenario, the major factor driving
selection in this parasitoid therefore becomes the ability to identify, and
successfully regulate the physiology of the host immediately after the final
larvallarval moult. Thus, in choosing hosts early in the sixth stadium,
E. pennicornis would appear to utilize the largest possible hosts
that allow for complete physiological regulation which, in turn, yield the
highest levels of developmental success in its progeny.
The fitness of E. pennicornis that developed from different sized hosts, or from differing clutch sizes, was not measured here. As a result, further measures of fitness gain when using different sized hosts, or laying eggs at different densities, remain to be determined. However, it was apparent that E. pennicornis preferentially attacked hosts at the start of the sixth stadium and typically laid clutches of 2030 eggs onto the integument of these hosts. Deviations from this strategy can be explained by the fact that at points during the wasp's lifespan the egg load will be considerably higher than 2030 eggs (typically when it first commences oviposition), when it may seek out larger hosts. Whilst a proportion of larger and smaller hosts were attacked, and clutch sizes increased or decreased accordingly, developmental success declined with any significant departure from the parasitism of early L6 hosts of around 0.20.4 g. The evidence presented here show that newly ecdysed L. oleracea larvae at the beginning of the sixth larval stadium represent the physiologically and nutritionally optimal stage for parasitism, and that E. pennicornis's reproductive fitness is maximized through the utilization of hosts that allow for the highest levels of parasitoid survival. Thus, in this case, bigger hosts are not necessarily better hosts, despite the fact that such hosts apparently represent a greater nutritional resource. In the case of E. pennicornis, we suggest that the major driver of selection has been for the identification and utilization of hosts that maximize progeny survival. Furthermore, we hypothesize that host choice is based on the requirement to identify the largest sized hosts that are amenable to the range of physiological and nutritional manipulations induced by the parasitoid and necessary for optimising the survival of parasitoid progeny. Thus, the ability to successfully regulate the host can be seen as the major factor governing host choice and oviposition behaviour in this parasitoid, a characteristic that may be commonplace in species where parasitoid-induced changes in host physiology are a prerequisite for progeny development.
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Acknowledgments |
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References |
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