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Oecologia (2007) 152:425–433
DOI 10.1007/s00442-007-0674-6

ECOPHYSIOLOGY

Manipulation of parasitoid size using the temperature-size rule:
Wtness consequences
H. Colinet · G. Boivin · Th. Hance

Received: 10 February 2006 / Accepted: 24 January 2007 / Published online: 8 March 2007
© Springer-Verlag 2007

Abstract The phenotypic eVects of rearing temperature
on several Wtness components of the koinobiont parasitoid,
Aphidius colemani, were examined. Temperatures experienced during development induced a plastic linear response
in the dry and fat masses of the immature stage and a nonlinear response in the growth rate as well as in the size of
adults. We investigated if the phenotypic morphometrical
plasticity exhibited by parasitoids reared at diVerent temperatures can induce variations in Wtness-related traits in
females. We did not Wnd any diVerence in immature (pupal)
mortality in accordance to rearing temperature. However,
when examining adult longevity, we found an inverse linear
relation with developmental temperature, conWrming the
usual rule that larger and fatter wasps live longer than
smaller ones. The pattern of female fecundity was non-linear; wasps that developed at high and low temperatures
were less productive. We suggest that when development is
short, the accumulated reserves are not adequate to support
both fecundity and survival. By manipulating adult size
through changes in the rearing temperature, we showed that
the usual shape of the size/Wtness function is not always linear as expected. Developmental temperature induced a

Communicated by Thomas HoVmeister.
H. Colinet (&) · Th. Hance
Unité d’Écologie et de Biogéographie,
Biodiversity Research Centre,
Université catholique de Louvain,
Croix du sud 4-5, 1348 Louvain-La-Neuve, Belgium
e-mail: colinet@ecol.ucl.ac.be
G. Boivin
Centre de Recherche et de Développement
en Horticulture, Agriculture et Agroalimentaire
Canada, 430 Boulevard Gouin,
Saint-Jean-sur-Richelieu, QC, Canada, J3B 3E6

plasticity in energy reserves which aVected the functional
constraints between survival and reproduction.
Keywords Aphidius colemani · Fat reserves · Fitness ·
Phenotypic plasticity · Size

Introduction
A knowledge of the relationship between body size and
Wtness is essential in many models of parasitoid evolutionary ecology (Rivero and West 2002), and this question has
received considerable attention (Leather 1988; Stearns
1992; Godfray 1994; Visser 1994; Jervis et al. 2003). In
insect parasitoids, body size and development time are key
components of life history strategies and Wtness (Sequeira
and Mackauer 1992). These two variables often compete,
resulting in a trade-oV where either large size is obtained at
the cost of a longer development time or the inverse. Adult
size has usually been considered to be a major trait on
which selection acts in parasitoids, as Wtness-related traits
such as fecundity and longevity generally increase with
increasing adult size (Cloutier et al. 1981; Visser 1994;
West et al. 1996; Ellers et al. 1998, 2001; Roitberg et al.
2001). However, development time can also be an important trait under conditions of high mortality risks (SG-HM
hypothesis; Benrey and Denno 1997; Williams 1999). The
relative importance of both traits depends on the feeding
ecology of the host (Harvey et al. 2000; Harvey and Strand
2002).
Body size is a trait that strongly covaries with the supply
of energy and materials for diVerent life-history processes
(West et al. 1999). The advantage of being large is thus
partly explained by the accumulation of fat reserves, which
are know to correlate positively with body size in parasitoids

123

426

(Ellers et al. 1998; Eijs and van Alphen 1999). In insects,
fat reserves play a crucial role in many metabolic processes,
as they are used for body maintenance, as an energy source
during Xight, or as an essential resource for oogenesis
(Ellers et al. 1998; Casas et al. 2005). As a result, lipid
availability is a key factor mediating the relationship
between size and Wtness (Rivero and West 2002).
Temperature plays an important role in the immature
development and subsequent adult size of ectotherms. Evolutionary biologists and ecologists use the term phenotypic
plasticity to describe the ability of a genotype to produce
distinct phenotypes – by altering its physiology, morphology, or development – in response to changes in its environment throughout its ontogeny (Sisodia and Singh 2002;
Pigliucci 2005). The developmental response to temperature is a form of phenotypic plasticity and one genotype
may thus express diVerent adult body sizes depending on
the temperature of the environment. The temperature-size
rule states that ectotherms grow larger at lower temperature, and this rule is supported by numerous studies
(reviewed by Atkinson 1994; Angilletta and Dunham
2003). As a generally accepted guideline, low temperature
results in a slower growth rate, longer development time
and larger adult size in insects (Sibly and Atkinson 1994).
In a comprehensive survey of the literature, Atkinson
(1994) demonstrated that the developmental eVect of temperature on adult size has been found in over 80% of experimental studies. Many hypotheses have been proposed to
explain the temperature-size rule, but no general mechanism has yet been established (Angilletta et al. 2004) since
there are exceptions to the usual pattern (e.g. Lamb and
Gerber 1985; Atkinson 1994; Birkemoe and Leinaas 2000;
Strohm 2000).
In the majority of ectotherm species, morphometrical
quantitative traits exhibit a large amount of phenotypic
plasticity as a consequence of developmental temperature.
Consequently, the experimental manipulation of the phenotype could be an interesting approach to assessing the shape
of the size/Wtness function. Along this same line, Li and
Mills (2004) analysed the relationship between host size
and quality by manipulating the host rearing temperature.
In koinobiont parasitoids, the host and the parasitoid larvae coexist and closely interact until the end of the parasitoid development, and temperature thus aVects the length of
time the parasitoid and the host are physiologically integrated. At high temperatures, the short immature development increases adult parasitoid opportunities for resource
access (food, hosts, mating), reduces the generation time
(Pandey and Singh 1999) and also reduces “the window of
vulnerability” to mortality factors such as hyperparasitism
or predation (SG–HM hypothesis; Benrey and Denno
1997). On the other hand, at high temperatures, the reduction in phenotypic body size may translate into reduced

123

Oecologia (2007) 152:425–433

energy reserves that may not be adequate to support both
high fecundity and longevity in the adults. Moreover, high
temperature can have both direct and indirect eVects on survivorship of the juveniles (Angilletta et al. 2004). In fact,
the high growth rate associated with high temperature is
assumed to carry a mortality cost (Sibly and Atkinson
1994; Nylin and Gotthard 1998).
Under low temperature conditions, slow growth may
translate into an increase in enemy-inXicted mortality risk
(SG-HM hypothesis; Benrey and Denno 1997) and may
also be costly in terms of lost opportunity. On the other
hand, there may be compensating advantages if the resulting potential increase in body size translates into increased
Wtness-related traits (Atkinson and Sibly 1997). Delayed
maturation may result in a higher fecundity as the latter
increases with body size (Stearns 1992). Larger individuals
may also survive better when there is no food, if body size
is correlated with energy reserves (Ohgushi 1996). Indeed,
it has been shown that parasitoid longevity is closely linked
to the amount of energy reserves (Ellers et al. 1998; Colinet
et al. 2006).
The Wtness costs of host-induced size variations has been
studied extensively in parasitoids (see Harvey et al. 2004;
Colinet et al. 2005); however, apart from studies on the
adaptative signiWcance of size variations, the Wtness consequences of temperature-induced size variations have
received little attention. The main purpose of this study was
to test if the expected size phenotypic plasticity exhibited
by parasitoids reared at diVerent temperatures can produce
variations in Wtness-related traits between insects of a given
genotype. We used Aphidius colemani Viereck (Hymenoptera: Aphidiidae), a small parasitic wasp attacking the aphid
Myzus persicae Sulzer (Homoptera: Aphididae). A. colemani is oligophagous on Aphididae (Starý 1975). By
manipulating the temperature under which A. colemani
developed, we Wrst veriWed if the parasitic wasp follows the
temperature-size rule; we then tested if the usual relationship between parasitoid size and Wtness-related traits is conserved when the size variation is due to the rearing
temperature.

Material and methods
Insects rearing
Laboratory cultures of the green peach aphid Myzus persicae were established from individuals collected in 2000 at
Louvain-la-Neuve, Belgium (50.3°N latitude). Aphids were
reared in 0.3-m3 cages on oilseed rape (Brassica napus L.,
var. Mesural) under laboratory conditions of 18°C, §60%
RH and a long-day photoregime [16/8 h (light/dark)]. Aphidius colemani was obtained from Biobest Co. (Edinburgh,

Oecologia (2007) 152:425–433

UK) and was reared in the laboratory on M. persicae under
the same rearing conditions.
Thermal treatments
Parasitoid Wtness can be aVected by host age-related quality
(Kouame and Mackauer 1991; Colinet et al. 2005) and by
qualitative diVerences among the host plant (reviewed by
Harvey 2005; Ode 2006). Therefore, to standardize host
quality and focus only on the temperature eVect, aphids
used as hosts in the experiments were all from synchronized cohorts and reared on an artiWcial diet following the
method described by Cambier et al. (2001).
The parasitoid females used in the experiments were less
than 48 h old and naive; in order to ensure they were mated,
each female was left for 24 h at 18°C with two males and
fed with water + honey (50:50). To avoid potential maternal eVects (Jann and Ward 1999; Blanckenhorn 2000),
females were all primarily reared for several generations at
the same temperature (18°C). One parasitoid female was
released for 3 h in a plastic petri dish (diameter: 4.5 cm)
containing 50 three-day-old aphids at 18°C. After parasitization, the female was removed, and the 50 aphids were
immediately transferred and assigned to one of the four
thermal treatments – 12, 15, 18 and 25°C – until parasitoid
emergence. There were ten replicates for each rearing temperature. The parasitized aphids were maintained on the
artiWcial diet to continue their development until mummiWcation.
Dry mass, fat mass, growth rate and size
The mummiWcation time was recorded and related to the
formation of the mummy. For each thermal treatment, 30
one-day-old mummies were subjected to individual mass
measurements (Mettler-electrobalance Me22; sensitivity: 1
g). The mummies were dried at 60°C for 3 days in an air
oven and then weighed to measure dry mass. The lean dry
mass was measured after an extraction in chloroform:methanol (2:1) (Terblanche et al. 2004; Colinet et al. 2006).
Each mummy was left for 2 weeks in an Eppendorf tube
containing 1 ml of the extracting solution, with agitation
daily. The mummies were then placed for 12 h in an air
oven at 60°C to eliminate the residues of the extracting
solution and the lean dry mass was measured. The fat mass,
corresponding to the diVerence between dry mass and lean
dry mass, and the fat content, corresponding to fat mass
divided by lean dry mass, were calculated. The growth rate
was calculated as a ratio between body size and development time (Jann and Ward 1999) [growth rate = ln
(dry mass/mummiWcation time)].
The length of the hind tibia, a standard estimation of size
in parasitoids (Godfray 1994), was measured on 30 adult

427

females for each thermal treatment. Digital pictures were
taken with a camera (Nikon 4500) mounted on a stereomicroscope. The pictures were analysed using Scion IMAGE
BETA ver. 4.02 software (Scion Corp., Frederick, Md.).
Fitness-related traits
For each replicate, the emergence rate was used to estimate immature (pupal) mortality. A parasitoid was considered as surviving when complete emergence from the
mummy occurred. To test the possible variation in longevity due to rearing temperature, ten newly emerged
females were maintained at 18°C with water only, and
survival was checked twice a day until the last parasitoid
died.
In A. colemani, 90% of the total fecundity occurs during the Wrst three oviposition days (Hofsvang and Hagvar
1975; Van Steenis 1993), and these 3 days contribute the
most to the rate of population increase (Sequeira and
Mackauer 1994). Therefore, for each thermal treatment,
the fecundity of ten newly emerged females was measured
during the Wrst three oviposition days, at the same experimental temperature (18°C). Each day, 130 § 10 threeday-old M. persicae larvae were oVered to a mated female
(maximum time: 24 h) in a plastic petri dish (diameter:
4.5 cm). Once removed from contact with the parasitoid
female, the aphids were maintained on the artiWcial diet
for 6 days at 18°C before being dissected under a stereomicroscope to detect the presence of a parasitoid larva.
For each female tested, the cumulated fecundity was
calculated by adding up the number of parasitized hosts
during the 3 days.
Statistical analysis
Least-squares linear models (Proc Reg; SAS Institute,
Cary, N.C.) were used to model the relationships
between variables and temperature. However, as morphometrical, developmental and Wtness-related traits
may vary non-linearly with temperature (Blanckenhorn
1997; Karan et al. 1998; Ris et al. 2004), quadratic functions
were also applied to model the relationships. F-tests
were used to compare the two models as an indication of
whether a non-linear function added a more accurate Wt
to the data (F-test on the quadratic term; Colinet et al.
2005).
Normality was veriWed using the Shapiro-Wilk statistic
( = 0.05). For mass parameters, size and fecundity no
transformation was required. Arcsin square root transformation was used to normalize the distribution of emergence
rate. For longevity, data were transformed using the BoxCox procedure [ = 2.58, T(y) = y ¡ 1/ ] (Box and Cox
1964). Untransformed data are presented in the Wgures.

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428

Oecologia (2007) 152:425–433

Results
Mass and size at diVerent rearing temperatures
The mummies emerging at the lower temperature condition
were heavier and fatter than those ones emerging at the
higher temperature condition. As predicted, dry mass (Fig. 1)
and fat mass (Fig. 2) were plastic in response to rearing temperature. Linear decreases with an increase in rearing temperature were observed for dry mass (n = 120, r2 = 0.461,
F = 99.25, P < 0.001) and fat mass (n = 120, r2 = 0.5,
F = 116.15, P < 0.001). The fat content (Fig. 3) also followed the same pattern (n = 120, r2 = 0.19, F = 27.71,
P < 0.001). For these three variables, the addition of a quadratic term to the linear model did not increase the adjustment to the data (dry mass: F = 0.58, P = 0.44; fat mass:
F = 3.45, P = 0.06; fat content: F = 3.26, P = 0.07). The fat
content was positively correlated to the dry mass (n = 120,
r2 = 0.17, F = 23.96, P < 0.001; Fig. 4), indicating that larger
mummies contained a higher proportion of fat. The eVect of
rearing temperature on the adult wasp size was also conWrmed. The adult size of the females (Fig. 5) decreased nonlinearly with increasing temperatures (n = 102, r2 = 0.41,
F = 43.43, P < 0.001), and a best Wt was obtained using a
curvilinear function (F = 12.29, P = 0.0006).

Fig. 2 Change in mummy fat mass in relation to the parasitoid rearing
temperature. The straight line is the least-squares linear regression
modelling the reduction in fat mass with increases in rearing temperature. Each square represents an individual value; n = 30 for each rearing temperature. See top of the Wgure for regression equation

Larval development and Wtness-related traits
The rearing temperature aVected larval development by
decreasing the time to mummiWcation (20 § 1.28,

Fig. 3 Change in mummy fat content, expressed as the ratio between
fat mass (FM) and lean dry mass (LDM), in relation to the parasitoid
rearing temperature. The straight line is the least-squares linear regression modelling the reduction in fat content with increasing rearing temperature. Each square represents an individual value; n = 30 for each
rearing temperature. See top of the Wgure for regression equation

Fig. 1 Change in mummy dry mass in relation to the parasitoid rearing temperature. The straight line is the least-squares linear regression
modelling the reduction in dry mass with increases in rearing temperature. Each square represents an individual value; n = 30 for each rearing temperature. See top of the Wgure for regression equation

123

15 § 0.87, 10.1 § 0.77, 7.3 § 0.79 days at 12, 15, 18,
25°C, respectively) and by increasing non-linearly the
growth rate (n = 120, r2 = 0.83, F = 281.86, P < 0.001;
Fig. 6). For growth rate, the best Wt was obtained with a
quadratic model (F = 51.39, P < 0.001).
For pre-adult mortality, no clear pattern appeared as
emergence values at all temperatures were above 90%
(90.1 § 7.69, 90.5 § 8.84, 96.3 § 4.33, 93.2 § 6.35 at 12,

Oecologia (2007) 152:425–433

Fig. 4 Relationship between mummy dry mass and fat content. The
latter is expressed as the ratio between fat mass (FM) and lean dry mass
(LDM). The straight line is the least-squares linear regression modelling the positive relationship between dry mass and fat content. Each
square represents an individual value; n = 30 for each rearing temperature. See top of the Wgure for regression equation. Two curves surrounding the best-Wt line deWne the 95% mean prediction interval

Fig. 5 InXuence of parasitoid rearing temperature on female adult
size, expressed as tibia length. The line represents the curvilinear function which best Wts the data. Each square represents an individual value; n = 30 for each rearing temperature. See top of the Wgure for
regression equation

15, 18, 25°C, respectively). The emergence rate was not
dependent on the temperature during juvenile development
for both models (linear: F = 1.27, P = 0.26; quadratic:
F = 1.69, P = 0.20).
The longevity of the females (Fig. 7) decreased linearly
with increasing temperatures (n = 40, r2 = 0.32, F = 18.25,
P < 0.001). The addition of a quadratic term did not
improve the adjustment to the data (F = 1.68, P = 0.20).

429

Fig. 6 Change in growth rate, expressed as ln (dry mass/mummiWcation time), in relation to parasitoid rearing temperature. The line represents the curvilinear function which best Wts the data. Each square
represents an individual value; n = 30 for each rearing temperature.
See top of the Wgure for regression equation

Fig. 7 Change in female adult longevity in the presence of water only
in relation to parasitoid rearing temperature. The straight line is the
least-squares linear regression showing a reduction in adult longevity
with increasing rearing temperature. Each square represents an individual value; n = 10 for each rearing temperature. See top of the Wgure
for regression equation

The rearing temperature also aVected female fecundity
(Fig. 8). A marginally signiWcant linear decrease was
observed with increasing rearing temperature (n = 40,
r2 = 0.11, F = 4.56, P = 0.04), suggesting that wasps reared
at lower temperature had a higher cumulate fecundity than
wasps reared at the higher temperature. However, a curvilinear function gave a better Wt to the data (F = 11.06,
P = 0.002), indicating a lower fecundity potential for

123

430

Fig. 8 InXuence of parasitoid rearing temperature on cumulated
fecundity during the Wrst 3 days of adult life. The line represents the
curvilinear function which best Wts the data. Females developing from
rearing at 12 and 25°C had a lower fecundity potential. Each square
represents an individual value; n = 10 for each rearing temperature.
See top of the Wgure for regression equation

females reared at the two extremes, 12 and 25°C (quadratic
model: n = 40, r2 = 0.32, F = 8.43, P = 0.001).

Discussion
In insects, size at emergence is a key life history variable
that is tightly linked with Wtness. In parasitoids, several
indicators of Wtness, such as longevity and fecundity, have
been shown to be positively correlated with size (Cloutier
et al. 1981; Visser 1994; West et al. 1996; Ellers et al.
1998, 2001). In this work, we focused on gaining an understanding of whether the usual relationship between parasitoid size and Wtness is conserved when plasticity in size is
due to the rearing temperature.
The eVect of rearing temperature on growth rate, development time and body size appears to be characteristic of
ectotherms. A. colemani follows the typical pattern where
development time and body size are negatively correlated
with temperature during development. The temperaturesize rule (Atkinson 1994) holds not only for adult size but
also for immature size, as we found variations in the dry
mass of mummies, indicating that phenotypic plasticity
occurred before metamorphosis. Temperatures experienced
during development induced a plastic linear response in the
dry mass of the immature stage, whereas the response was
non-linear in the size of the adults. The overall plasticity of
morphometrical traits can sometimes exhibit diVerent
responses to temperature, depending on the trait analysed.
In Drosophila melanogaster, the phenotypic response to
temperature is higher for weight traits than for length ones
(Karan et al. 1998).

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Oecologia (2007) 152:425–433

The inverse relationship between rearing temperature
and insect size has been thoroughly documented in the Diptera, mostly in Drosophila (e.g. Powell 1974; Cavicchi
et al. 1989; David et al. 1994; Partridge et al. 1994; Nunney
and Cheung 1997; Bochdanovits and de Jong 2003). A few
studies have analysed the eVects of developmental temperature on the size of parasitic wasps under laboratory conditions (Nealis et al. 1984; Elliott et al. 1995; Bazzocchi
2003; Ichiki et al. 2003; Ris 2003), and these have obtained
results similar to those reported here. A seasonal variation
of parasitoid body size has also been found in the Weld,
probably due to a temperature eVect (Ellers et al. 2001;
Sequeira and Mackauer 1993).
As expected (Huey and Kingsolver 1989; Blanckenhorn
1997), the plasticity in growth rate showed a quadratic
response as a function of temperature, which may be interpreted as a physiological response rather than an adaptative
one. Accelerated growth rates in A. colemani, as inXuenced
under high ambient temperatures, are assumed to carry signiWcant costs in terms of adult parasitoid Wtness (Sibly and
Atkinson 1994; Nylin and Gotthard 1998), such as a correspondingly higher rate of pre-adult mortality. In this study,
no clear pattern appeared as the pre-adult mortality (i.e.
emergence rate) was not dependent on the temperature
experienced during juvenile development. Other researchers have reported similar results in a favourable temperature range (i.e. without extreme conditions) (Deng and Tsai
1998; Röhne 2002; De Vis et al. 2002; Ichiki et al. 2003).
When the development time was reduced, the accumulated reserves available for adult functions were also
reduced. Indeed, not only adult size and mummy dry mass
decreased with rearing temperature but also the total
amount of fat reserves (i.e. fat mass) and the relative proportion of fat reserves (i.e. fat content). Fat reserves are
known to be positively correlated with size (dry mass)
(Ellers et al. 1998; Strohm 2000; Rivero and West 2002),
and lipids are the most eYcient energy source used in
insects (Van Handel 1993; Rivero and Casas 1999). In parasitoids, fat reserves decrease linearly during life, and parasitic wasps, especially non-host feeding parasitoids, seem
to be unable to synthesize lipids de novo (Ellers et al. 1998;
Olson et al. 2000; Rivero and West 2002; Giron and Casas
2003). The consequence of this lack of lipogenesis makes
the fat reserve a non-replaceable resource that is potentially
a limiting factor, particularly for small parasitoids (Rivero
and West 2002). Thus, when the immature parasitoid stops
feeding on its host tissues, the accumulated reserves are
allocated to somatic and reproduction functions, presumably in a manner that maximizes Wtness (Sequeira and
Mackauer 1994). We have shown that the longevity of
adults correlated negatively with temperature conditions.
Starved small wasps that were reared at the higher temperature survived for a shorter period of time than starved larger

Oecologia (2007) 152:425–433

and fatter wasps reared at the lower temperature. The longevity of parasitoids kept without food has been directly
linked to the amount of fat reserve (Ellers et al. 1998;
Rivero and West 2002). In this study, we show that the
rearing temperature induced a plasticity in size and in fat
reserves that probably acts as a main factor mediating the
life span of the parasitic wasps.
A delayed maturation should indirectly provide a beneWt
of greater fecundity because fecundity increases with body
size (Stearns 1992). In A. colemani, the pattern of female
fecundity in relation to the temperature-induced size variation did not follow the usual relationship between body size
and fecundity. Indeed, the best Wt was obtained with a curvilinear function, suggesting that the largest and the smallest females, which emerged from rearing at 12 and 25°C,
respectively, had a lower fecundity potential. Our results
support those already observed in Drosophila (Nunney and
Cheung 1997; Sisodia and Singh 2002), where phenotypic
plasticity breaks the usual positive correlation between
body size and fecundity. Similarly, Ris et al. (2004)
observed that the parasitoid Leptopilina heterotoma reared
at diVerent temperatures had a fecundity (expressed as egg
load) that varied as a curvilinear function of the temperature, with an optimum at intermediate temperatures. The
size variation for L. heterotoma followed the same pattern
as that in A. colemani (Ris 2003).
Several studies have emphasized that there is a trade-oV
between reproduction and survival in parasitoids (Ellers
and van Alphen 1997; Ellers et al. 2000; Jervis et al. 2003),
and fat reserve has been shown to play a central role in the
physiology of resource allocation for this trade-oV (Ellers
and van Alphen 1997). Lipids are known to be directly
involved in egg production (Nijhout 1994; Ellers and van
Alphen 1997; Zhao and Zera 2002) and may thus be
directly linked to fecundity. For the females raised at temperatures ranging between 12 and 18°C, it seems that fat
reserves, which can be used for both survival and egg production, are suYciently high to be plastic in their allocation, leading to a trade-oV. Indeed, in this temperature
range, the highest fecundity corresponds to the lowest longevity, and vice-versa. On the other hand, when development is reduced, which occurs at the highest rearing
temperature (25°C), the females have a much reduced
amount and proportion of fat reserves, which gives them a
smaller range within which the allocation between reproduction and survival can be shifted. As suggested by Rivero
and West (2002), the parasitoids seem to suVer disproportionately from being small because they have to rely more
heavily on carbohydrates, which provide signiWcantly
fewer calories than fat (Nijhout 1994), for survival and
reproduction. Thus, it seems that when development is
short, the accumulated reserves of the females are not adequate to support both fecundity and survival. According to

431

the growth rate function, the maximum growth rate occurs
at 24.5°C. At 25°C, individuals may have grown faster by
allocating a greater proportion of the available energy to
growth, but this increase may occur at the expense of other
functions, such as maintenance and reproduction.
Apart from the evident eVect of temperature on the
phenotypic plasticity in size and fat reserves and their
consequences on Wtness-related traits, temperature also
aVects the period of time during which the parasitoid
coexists with the host. Rapid development may be advantageous in terms of mortality risks, as the temporal exposure of the host to natural enemies would be decreased
(SG-HM hypothesis; Benrey and Denno 1997). This study
clearly stresses the necessity of incorporating the diversity of trade-oVs existing between diVerent life history
traits in the prediction of the multiple host-parasitoidenvironment interactions.
By manipulating body size using the temperature-size
rule, we have experimentally tested and validated the ideas
proposed by Rivero and West (2002). This study underlines
the importance of temperature on developmental reaction
norms and, in particular, on energy reserves which are
known to shape the functional constraints between survival
and reproduction. It would be interesting to determine if the
Wtness costs in the response associated with changes in parasitoid size under diVerent temperature regimes are equivalent to those related to diVerences in host size but reared at
the same temperature. Our observations suggest that the
usual linear relationship between Wtness-related traits and
size is not always conserved when the size variation is due
to the developmental temperature. A knowledge of the relationship between body size and Wtness is essential in many
models of parasitoid evolutionary ecology but also from an
applied perspective: in inundative biological control programs, parasitoids are mass-reared, and diVerent rearing
techniques could result in diVerent wasp size distributions
before release.
Acknowledgements We sincerely thank J. Ellers, D. Giron and N.
Ris for very constructive comments on the manuscript. We are also
grateful to P. Baret and C. Salin for useful helps. This study was supported by “Ministère de la Région wallonne – DGTRE Division de la
Recherche et de la Coopération scientiWque.” FIRST EUROPE Objectif 3. This paper is BRC109 of the Biodiversity Research Centre. The
experiments comply with the current laws of the country in which they
were performed.

References
Angilletta MJ, Dunham AE (2003) The temperature-size rule in ectotherms: simple evolutionary explanations may not be general. Am
Nat 162:332–342
Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate,
and body size in ectotherms: Wtting pieces of a life-history puzzle.
Integr Comp Biol 44:498–509

123

432
Atkinson D (1994) Temperature and organism size – a biological law
for ectotherms? Adv Ecol Res 25:1–58
Atkinson D, Sibly RM (1997) Why are organisms usually bigger in
colder environments? Making sense of a life history puzzle. Tree
12:235–239
Bazzocchi GG, Lanzoni A, Burgio G, Fiacconi MR (2003) EVects of
temperature and host on the pre-imaginal development of the parasitoid Diglyphus isaea (Hymenoptera: Eulophidae). Biol Control
26:74–82
Benrey B, Denno RF (1997) The slow growth–high mortality hypothesis: a test using the cabbage butterXy. Ecology 78:987–999
Birkemoe T, Leinaas HP (2000) EVects of temperature on the development of an arctic Collembola (Hypogastrura tullbergi). Funct
Ecol 14:693–700
Blanckenhorn WU (1997) EVects of temperature on growth, development and diapause in the yellow dung Xy – against all the rules?
Oecologia 111:318–324
Blanckenhorn WU (2000) Temperature eVects on egg size and their Wtness consequences in the yellow dung Xy Scathophaga stercoraria. Evol Ecol 14:627–643
Bochdanovits Z, de Jong G (2003) Temperature dependent larval resource allocation shaping adult body size in Drosophila melanogaster. J Evol Biol 16:1159–1167
Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc
26:211–252
Cambier V, Hance Th De HoVmann E (2001) EVects of 1,4-benzoxazin-3-one derivatives from maize on survival and fecundity of
Metopolophium dirhodum (Walker) on artiWcial diet. J Chem
Ecol 27:359–370
Casas J, Pincebourde S, Mandon N, Vannier F, Poujol R, Giron D
(2005) Lifetime nutrient dynamics reveal simultaneous capital
and income breeding in a parasitoid. Ecology 86:545–554
Cavicchi S, Guerra D, Natali V, Pezzoli C, Giorgi G (1989) Temperature-related divergence in experimental populations of Drosophila melanogaster. II. Correlations between Wtness and body
dimensions. J Evol Biol 2:235–251
Cloutier C, McNeil JN, Regnière J (1981) Fecundity, longevity and sex
ratio of Aphidius nigripes (Hymenoptera: Aphidiidae) parasiting
diVerent stages of its host, Macrosiphum euphorbiae (Homoptera:
Aphididae). Can Entomol 113:193–198
Colinet H, Salin C, Boivin G, Hance Th (2005) Host age and Wtnessrelated traits in a koinobiont aphid parasitoid. Ecol Entomol
30:473–479
Colinet H, Hance T, Vernon P (2006) Water relations, fat reserves, survival and longevity of a cold-exposed parasitic wasp Aphidius colemani (Hymenoptera: Aphidiidae). Environ Entomol 35:228–236
David JR, Moreteau B, Gautier JP, Pétavy G, Stockel A, Imasheva AG
(1994) Reaction norms of size characters in relation to growth
temperature in Drosophila melanogaster: an isofemale lines analysis. Genet Sel Evol 26:229–251
De Vis RMJ, Fuentes LE, van Lenteren JC (2002) Life history of Amitus fuscipennis (Hym., Platygastridae) as parasitoid of the greenhouse whiteXy Trialeurodes vaporariorum (Hom., Aleyrodidae)
on tomato as function of temperature. J Appl Entomol 126:24–33
Deng YX, Tsai JH (1998) Development of Lysiphlebia japonica
(Hymenoptera: Aphidiidae), a parasitoid of Toxoptera citricida
(Homoptera: Aphididae) at Wve temperatures. Fla Entomol
81:415–423
Eijs IEM, van Alphen JJM (1999) Life history correlations: why are
hymenopteran parasitoids an exception? Ecol Lett 2:27–35
Ellers J, van Alphen JJM (1997) Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction. J Evol Biol 10:771–785
Ellers J, van Alphen JJM, Sevenster JG (1998) A Weld study of size–
Wtness relationships in the parasitoid Asobara tabida. J Anim Ecol
67:318–324

123

Oecologia (2007) 152:425–433
Ellers J, Driessen G, Sevenster JG (2000) The shape of the trade-oV
function between reproduction and survival in the parasitoid Asobara tabida. Neth J Zool 50:29–36
Ellers J, Bax M, van Alphen JJM (2001) Seasonal changes in female
size and its relation to reproduction in the parasitoid Asobara tabida. Oikos 92:309–314
Elliott NC, Burd JD, Kindler SD, Lee JH (1995) Temperature eVects
on development of three cereal aphid parasitoids (Hymenoptera:
Aphididae). Great Lakes Entomol 28:199–204
Giron D, Casas J (2003) Lipogenesis in an adult parasitic wasp. J Insect
Physiol 49:141–147
Godfray HCJ (1994) Parasitoids, behavioral and evolutionary ecology.
Princeton University Press, Princeton
Harvey JA (2005) Factors aVecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints
and incorporating complexity. Entomol Exp Appl 117:1–13
Harvey JA, Strand MR (2002) The developmental strategies of endoparasitoid wasps vary with host feeding ecology. Ecology
83:2439–2451
Harvey JA, Kadash K, Strand MR (2000) DiVerences in larval feeding
behavior correlate with altered development strategies in two parasitic wasps: implications for the size-Wtness hypothesis. Oikos
88:621–629
Harvey JA, Bezemer TM, Elzinga JA, Strand MR (2004) Development
of the solitary endoparasitoid Microplitis demolitor: host quality
does not increase with host age and size. Ecol Entomol 29:35–43
Hofsvang T, Hagvar EB (1975) Duration of development and longevity in Aphidius ervi and Aphidius platensis (Hymenoptera: Aphidiidae), two parasites of Myzus persicae (Homoptera: Aphididae).
Entomophaga 20:11–22
Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity in
ectotherms. Trends Ecol Evol 4:131–135
Ichiki R, Takasu K, Shima H (2003) EVects of temperature on immature development of the parasitic Xy Bessa parallela (Meigen)
(Diptera: Tachinidae). Appl Entomol Zool 38:435–439
Jann P, Ward PI (1999) Maternal eVects and their consequences for
oVspring Wtness in the Yellow Dung Fly. Funct Ecol 23:51–58
Jervis MA, Ferns PN, Heimpel GE (2003) Body size and the timing of
egg production in parasitoid wasps: a comparative analysis. Funct
Ecol 17:375–383
Karan D, Morin JP, Moreteau B, David JR (1998) Body size and developmental temperature in Drosophila melanogaster: analysis of
body weight reaction norm. J Therm Biol 23:301–309
Kouame KL, Mackauer M (1991) InXuence of aphid size, age and
behaviour on host choice by the parasitoid wasp Ephedrus californicus – a test of host-size models. Oecologia 88:197–203
Lamb RJ, Gerber GH (1985) EVects of temperature on the development, growth, and survival of larvae and pupae of a north-temperate chrysomelid beetle. Oecologia 67:8–18
Leather SR (1988) Size, reproductive potential and fecundity in insects: things aren’t as simple as they seem. Oikos 51:386–389
Li B, Mills N (2004) The inXuence of temperature on size as an indicator of host quality for the development of a solitary koinobiont
parasitoid. Entomol Exp Appl 110:249–256
Nealis VG, Jones RE, Wellington WG (1984) Temperature and development in host–parasite relationships. Oecologia 61:224–229
Nijhout HF (1994) Insect hormones. Princeton University Press,
Princeton
Nunney L, Cheung W (1997) The eVect of temperature on body size
and fecundity in female Drosophila melangonaster – evidence for
adaptive plasticity. Evolution 51:1529–1535
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev
Entomol 43:63–83
Ode PJ (2006) Plant chemistry and natural enemy Wtness: eVects on
herbivore and natural enemy Wtness. Annu Rev Entomol 51:163–
185

Oecologia (2007) 152:425–433
Ohgushi T (1996) Consequences of adult size for survival and reproductive performance in a herbivorous ladybird beetle. Ecol Entomol 21:47–55
Olson DM, Fadamiro H, Lundgren JOG, Heimpel GE (2000) EVects of
sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiol Entomol 25:17–26
Pandey S, Singh R (1999) Host size induced variation in sex ratio of an
aphid parasitoid Lysiphlebia mirizai. Entomol Exp Appl 90:61–
67
Partridge L, Barrie B, Fowler K, French V (1994) Thermal evolution
of pre-adult life history traits in Drosophila melanogaster. J Evol
Biol 7:645–663
Pigliucci M (2005) Evolution of phenotypic plasticity: where are we
going now? Tree 20:481–486
Powell JR (1974) Temperature related divergence in Drosophila body
size. J Hered 65:257–258
Ris N (2003) Hétérogénéité spatiale, plasticité phénotypique et tradeoV environnementaux: Rôle de l’espèce hôte et de la température
dans la diVérenciation génétique des populations du parasitoïde
Leptopilina heterotoma (Hymenoptera). PhD thesis, Université
Claude Bernard, Lyon
Ris N, Allemand R, Fouillet P, Fleury F (2004) The joint eVect of temperature and host species induce complex genotype-by-environment interactions in the larval parasitoid of Drosophila,
Leptopilina heterotoma (Hymenoptera: Figitidae). Oikos
106:451–456
Rivero A, Casas J (1999) Incorporating physiology into parasitoid
behavioral ecology: the allocation of nutritional resources. Res
Popul Ecol 41:39–45
Rivero A, West SA (2002) The physiological costs of being small in a
parasitic wasp. Evol Ecol Res 4:407–420
Röhne O (2002) EVect of temperature and host stage on preference of
Aphelinus varipes Förster (Hym., Aphelinidae) parasiting the cotton aphid, Aphis gossypii Glover (Hom., Aphididae). J Appl Entomol 126:572–576
Roitberg BD, Boivin G, Vet LEM (2001) Fitness, parasitoids, and biological control: an opinion. Can Entomol 133:429–438
Sequeira R, Mackauer M (1992) Quantitative genetics of body size and
development time in the parasitoid wasp Aphidius ervi (Hymenoptera, Aphidiidae). Can J Zool 70:1102–1108
Sequeira R, Mackauer M (1993) Seasonal variation in body size and
oVspring sex ratio in Weld populations of the parasitoid wasp,
Aphidius ervi (Hymenoptera: Aphidiidae). Oikos 68:340–346

433
Sequeira R, Mackauer M (1994) Variation in selected life-history
parameters of the parasitoid wasp, Aphidius ervi: inXuence of host
developmental stage. Entomol Exp Appl 71:15–22
Sibly RM, Atkinson D (1994) How rearing temperature aVects optimal
adult size in ectotherms. Funct Ecol 8:486–493
Sisodia S, Singh BN (2002) EVect of temperature on longevity and
productivity in Drosophila ananassae: evidence for adaptive
plasticity and trade-oV between longevity and productivity. Genetica 114:95–102
Starý P (1975) Aphidius colemani Viereck: its taxonomy, distribution
and host range (Hymenopetra: Aphidiidae). Acta Entomol Bohemoslov 72:156–173
Stearns SC (1992) The evolution of life histories. Oxford University
Press, Oxford
Strohm E (2000) Factors aVecting body size and fat content in a digger
wasp. Oecologia 123:184–191
Terblanche JS, Klok CJ, Chown SL (2004) Metabolic rate variation in
Glossina pallidipes (Diptera: Glossinidae): gender, ageing and
repeatability. J Insect Physiol 50:419–428
Van Handel E (1993) Fuel metabolism of the mosquito (Culex quinquefasciatus) embryo. J Insect Physiol 39:831–833
Van Steenis MJ (1993) Intrinsic rate of increase of Aphidius colemani
Vier. (Hym., Braconidae) a parasitoid of Aphis gossypii Glov.
(Hom., Aphididae) at diVerent temperatures. J Appl Entomol
116:192–198
Visser ME (1994) The importance of being large: the relationship
between size and Wtness in females of the parasitoid Aphaereta
minuta (Hymenoptera: Braconidae). J Anim Ecol 63:963–978
West SA, Flanagan KE, Godfray HCJ (1996) The relationship between
parasitoid size and Wtness in the Weld: a study of Achrysocharoides zwoelferi (Hymenoptera, Eulophidae). J Anim Ecol 65:631–
639
West GB, Brown JH, Enquist BJ (1999) The fourth dimension of life:
fractal geometry and allometric scaling of organisms. Science
284:167–169
Williams I (1999) Slow-growth, high mortality a general hypothesis,
or is it? Ecol Entomol 24:490–495
Zhao Z, Zera AJ (2002) DiVerential lipid biosynthesis underlies a
tradeoV between reproduction and Xight capability in a wingpolymorphic cricket. Proc Natl Acad Sci USA 99:16829–16834

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