Journal of Thermal Biology 37 (2012) 159–163
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Journal of Thermal Biology
journal homepage: www.elsevier.com/locate/jtherbio
Thermal dependence of reproductive allocation in a tropical lizard
Zuzana Starostová a,n, Michael J. Angilletta Jr.b, Lukáš Kubička a, Lukáš Kratochvı́l a
a
b
Department of Zoology and Department of Ecology, Faculty of Science, Charles University in Prague, Viničná 7, Praha 2, 12844, Czech Republic
School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA
a r t i c l e i n f o
abstract
Available online 30 December 2011
In ectotherms, environmental temperature is the most prominent abiotic factor that modulates lifehistory traits. We explored the influence of environmental temperature on reproduction in the
Madagascar ground gecko (Paroedura picta) by measuring reproductive traits of females at constant
temperatures (24, 27, 30 1C). Females of this species lay clutches of one or two eggs within short
intervals. For each female, we measured egg mass for the first five clutches. For one clutch, we also
measured the energetic content of eggs via bomb calorimetry. Temperature positively influenced the
rate of egg production, but females at 30 1C laid smaller eggs than did females at either 24 or 27 1C. Dry
mass of eggs scaled allometrically with wet mass, but this relationship was similar among thermal
treatments. Females at all temperatures produced eggs with similar energy densities. Females at 24 1C
allocated less energy per time unit (E 8 mW) to reproduction than did females from higher
temperatures (E 12 mW). However, females at either 24 or 27 1C allocated significantly more energy
per egg than did females at 30 1C. Our results demonstrate that a complex thermal sensitivity of
reproductive rate can emerge from distinct thermal sensitivities of egg size, egg composition and clutch
frequency.
& 2012 Elsevier Ltd. All rights reserved.
Keywords:
Egg composition
Life history
Maternal investment
Phenotypic plasticity
Reproduction
Thermal effect
1. Introduction
Life histories differ greatly among animals, partly because of
variation in environmental conditions. Temperature is one of the
most important environmental factors that influence life-history
traits, including reproductive allocation (reviewed by Angilletta,
2009). Reproductive strategies have many components, some of
which may depend on temperature and others which may not (e.g.,
see Angilletta et al., 2006). Thus, thermal effects on reproduction
involve multiple parameters, such as the size and composition of
eggs as well as the rate of egg production. Understanding how these
parameters combine to determine the thermal plasticity of reproduction could alter our view of organismal energetics. For instance,
the Metabolic Theory of Ecology (Brown et al., 2004) predicts that
rates of biomass production, including reproduction, scale proportionally to the metabolic rate of an organism (see Hayward and
Gillooly, 2011). If so, the energy allocated to reproduction should
increase with temperature according to the Boltzman–Arrhenius
function (Gillooly et al., 2001). Deviations from this expectation
could reflect evolutionary adaptation of the life history (Clarke,
2006; Gillooly et al., 2006).
n
Corresponding author. Tel.: þ420 221951838; fax: þ420 221951841.
E-mail addresses: [email protected] (Z. Starostová),
[email protected] (M.J. Angilletta Jr.), [email protected] (L. Kubička),
[email protected] (L. Kratochvı́l).
0306-4565/$ - see front matter & 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jtherbio.2011.12.009
Much debate over adaptive vs. non-adaptive variation in
reproduction has focused on patterns of egg size. Although one
could naively assume that a single optimal egg size exists in any
environment, egg size depends greatly on micro-environmental
factors such as temperature (e.g. Fischer et al., 2003; Angilletta
et al., 2004). In general, ectothermic animals produce smaller eggs
at higher temperatures. Although an explanation for this observation is still a subject of debate (e.g. Perrin, 1988; Blanckenhorn,
2000; Oufiero et al., 2007), a potential explanation involves
morphological constraints imposed by body size. In many species
of ectotherms, individuals that develop at higher temperatures
reproduce at smaller sizes (e.g. Atkinson, 1994). Small females,
with correspondingly small body cavities or pelvic openings,
cannot lay large eggs (Congdon and Gibbons, 1987; Sinervo and
Licht, 1991). Therefore, females that develop at a low temperature
would be able to produce larger eggs than would females that
develop at a high temperature. This non-adaptive explanation
predicts that one would observe the same relationship between
maternal size and egg size in all thermal environments (Oufiero
et al., 2007). Smaller eggs at higher temperatures can also reflect an
adaptive strategy of energy allocation, because warm environments facilitate juvenile growth and thus permit mothers to
increase their fecundity by producing small eggs (e.g. Perrin,
1988). This adaptive explanation makes no prediction about the
scaling of egg size with maternal size in different thermal environments (Oufiero et al., 2007).
160
Z. Starostová et al. / Journal of Thermal Biology 37 (2012) 159–163
Reproductive output depends not only on the size of eggs but
also on the number of eggs and the frequency of clutches . Given
the tradeoff between the size and number of eggs, females at lower
temperatures produce fewer, large eggs in each clutch (Atkinson
et al., 2001; Fischer et al., 2003; Geister et al., 2008; but see
Blanckenhorn, 2000). Reproductive output at low temperature
might also suffer because clutches cannot be produced as rapidly
as they can at high temperature. Estimating the thermal plasticity
of reproductive frequency requires considerable time, especially for
long-lived seasonal breeders. Consequently, we know much less
about the thermal plasticity of reproductive frequency than we do
about the thermal plasticity of egg size and clutch size.
The energy density of eggs can also represent an adaptive
component of reproduction (see Geister et al., 2009). If a small
female cannot lay large eggs, she might compensate by producing
eggs with a greater concentration of lipids, which would enhance
the energy content of each egg. Such effects would cause an
allometric relationship between the size and energy content of
eggs (Oufiero et al., 2007; Geister et al., 2008). Therefore, the
thermal dependence of this relationship should be considered
when describing reproductive plasticity.
We studied the thermal plasticity of reproductive traits in the
Madagascar ground gecko (Paroedura picta (Peters, 1854)). Among
reptiles, this species grows quickly, maturing at the age of about
4 months. Females usually lay two hard-shelled eggs per clutch in
extremely short intervals (7–10 days) and breed throughout the
year when resources permit (Kubička and Kratochvı́l, 2009). The
invariant clutch size of this species, typical for all geckos (e.g.
Kratochvı́l and Kubička, 2007), eliminates a tradeoff between egg
size and egg number in a given clutch. Yet, due to the high
frequency of reproduction, females make many sequential decisions about using energy to reproduce. By measuring the number,
size and composition of eggs produced at different temperatures,
we hoped to uncover the mechanisms by which temperature
determines reproductive output.
2. Material and methods
2.1. Studied organism and thermal experiment
This study was part of an experiment focusing on thermal
plasticity of life-history traits in P. picta. The experimental design
was described in detail by Starostová et al. (2010). Briefly, we
collected 160 eggs from 20 adult females that had been maintained
under common conditions. On the day of laying, eggs were
distributed based on a predefined balanced design among three
thermal treatments: 24, 27 and 30 1C (70.3 1C). These treatments
were based on temperatures of the natural environment, which
range from 28 to 35 1C during the day and from 20 to 25 1C during
the night (Schönecker, 2008) and also according to our previous
experience with incubating eggs of P. picta (see also Blumberg
et al., 2002). For all three treatments, the light cycle was 12L:12D.
After hatching, lizards were housed individually in opaque plastic
cages containing a shelter and a water dish on a substrate of sand;
these cages were kept in the same climatic chambers that maintained the thermal treatments. Water supplemented with calcium
was provided ad libitum. Twice per month, water was enriched
with vitamins E, A and D3 (Combinal E and Combinal AþD3; IVAX
Pharmaceuticals, Opava, Czech Republic). Twice per week, lizards
were fed with live crickets (Gryllus assimilis) dusted with vitamins
and minerals (Roboran H, Univit, Czech Republic). An over-abundance of crickets was provided at each feeding. Geckos were
weighed four times a week and snout-to-vent length (SVL) was
measured every 3 weeks.
When a female reached a mass of 6 g, an unrelated male from
the same thermal treatment was assigned as her mate. Females
were allowed to mate every 14 days until the first oviposition and
every month thereafter. Females began laying eggs soon after the
first mating. We measured the mass of eggs in the first five
clutches of each female (23, 19 and 18 females at 24, 27, and
30 1C, respectively). Females were weighted and measured soon
after oviposition. Eggs from the fifth intact double-egg clutch of
each female were frozen at 80 1C for subsequent measurements
of water content and energy density. Eggs from other clutches
were weighed and incubated.
2.2. Analysis of egg composition
Frozen eggs taken for energy density estimation were lyophilized
for 24 h and then re-weighed to the nearest 0.001 g. Eggs were then
homogenized with mortar and pestle. Samples of the homogenate
were compressed into pellets, ranging in mass from 0.062 to 0.174 g.
Pellets were combusted using a semimicro calorimeter (Model 1425,
Parr Instruments Company, Moline, IL, USA) to determine caloric
density. The calorimeter was calibrated twice daily using benzoic acid
as a standard. The energy content of each egg was calculated as the
product of energy density and dry mass.
We estimated the rate at which each female allocated energy
to reproduction (further referred to as reproductive rate) based on
the energy contained in her clutch and the mean interval between
her clutches. For this calculation, we assumed that females always
laid two eggs, although females occasionally laid a single egg.
Recently, Kubička and Kratochvı́l (2009) reported that P. picta
produces a clutch of one egg in about 10% of clutches. In our
study, single-egg clutches accounted for less than 6% of the 261
clutches. Moreover, the frequency of single-egg clutches varied
strongly among females: 9 of 15 single-egg clutches were produced by females at 30 1C, and seven of them were produced by
one female. Single-egg clutches seem to result from reproductive
failure of one ovary rather than adjustments of reproductive effort
(for discussion see Kubička and Kratochvı́l, 2009; Kubička et al., in
press). Nevertheless, even females that produced single-egg
clutches occasionally produced a double-egg clutch, and thus
could have reached the reproductive rate estimated under our
assumptions.
2.3. Statistical analyses
We analyzed the effects of maternal size (SVL), clutch number
(1–5), and temperature (24, 27, and 30 1C) on the wet mass of eggs.
Maternal identity was included as a random factor. Following Zuur
et al. (2009), we started out by fitting a linear mixed model with all
possible main effects and interactions using the ‘‘nlme’’ library
(Pinheiro et al., 2011) of the R statistical package (version 2.13.1; R
Development Core Team, 2011). We then progressively simplified
the model by dropping the highest-order terms. The best model
was selected using the Akaike information criterion (AIC; Burnham
and Anderson, 2002).
Clutch frequency was analyzed using the mean interval
between several subsequent clutches. For other reproductive traits,
we avoided pseudo-replication by analyzing data from a single
clutch per female and by analyzing the mean value for each female.
These statistical analyses were performed in Statistica 10.0
(StatSoft Inc., 2011).
3. Results
We measured the masses of 535 eggs produced by 60 females
in their first five clutches. The best model included maternal size,
Z. Starostová et al. / Journal of Thermal Biology 37 (2012) 159–163
Fig. 1. At all three temperatures, egg size increased among consecutive clutches.
The thermal effect on egg size was more pronounced for later clutches. Means
were adjusted for maternal body size. Error bars denote 95% confidence intervals.
Table 1
Parameters of the general linear mixed model of the effects of environmental
temperature, clutch number, and maternal size (SVL) on egg mass. The effect of
maternal identity was modeled as a random effect in the intercept (SD ¼0.0589).
Parameter
Value
SE
df
P
Intercept
Maternal SVL
Temperature 27 1C
Temperature 30 1C
Clutch 2
Clutch 3
Clutch 4
Clutch 5
Temp. 27 1C: Clutch
Temp. 30 1C: Clutch
Temp. 27 1C: Clutch
Temp. 30 1C: Clutch
Temp. 27 1C: Clutch
Temp. 30 1C: Clutch
Temp. 27 1C: Clutch
Temp. 30 1C: Clutch
0.3409
0.0072
0.0563
0.0811
0.0413
0.0342
0.0780
0.0788
0.0316
0.0115
0.0663
0.0198
0.0560
0.0318
0.0431
0.0134
0.1070
0.0016
0.0228
0.0234
0.0130
0.0140
0.0150
0.0166
0.0183
0.0190
0.0180
0.0188
0.0180
0.0191
0.0180
0.0188
462
462
57
57
462
462
462
462
462
462
462
462
462
462
462
462
0.0015
o0.0001
0.0165
0.0010
0.0016
0.0155
o0.0001
o0.0001
0.0850
0.5454
0.0003
0.2943
0.0020
0.0975
0.0169
0.4765
2
2
3
3
4
4
5
5
included maternal SVL as a covariate in analyses of egg mass,
energy content, and reproductive rate. Maternal SVL significantly
affected all of these reproductive traits. Eggs of females at 30 1C
were significantly smaller than those of females at 24 or 27 1C,
both in absolute terms (ANOVA: F2, 57 ¼ 3.29, P¼0.045) and
relative to maternal size (ANCOVA: F2, 56 ¼6.24, P¼0.004). Mean
water content of eggs was 71.7% (range ¼66.4–74.2%). Mean dry
egg mass increased nearly linearly with mean wet egg mass (dry
egg mass¼0.0406þ0.2392 wet egg mass). The non-zero intercept of this relationship (0.0470.02 g [SE]) suggests that larger
eggs contained proportionally more water. ANCOVA indicated
that scaling of dry egg mass with wet egg mass was not
significantly affected by temperature (F2, 56 ¼1.77, P¼0.18).
Females at all temperatures produced eggs with similar energy
densities 4662.8726.6 cal g 1 of dry mass (ANOVA: F2, 57 ¼0.71,
P¼0.50). Temperature affected the mean energy content of eggs
both in absolute terms (ANOVA: F2, 57 ¼7.07, P¼0.002) and
relative to maternal size (ANCOVA: F2, 56 ¼11.01, Po0.001).
Fisher’s post-hoc test revealed that females at 30 1C produced
eggs containing significantly less energy than did females at the
other temperatures. Table 2 contains descriptive statistics for
maternal size and reproductive traits.
The mean interval between clutches was estimated for 57 females
based on 204 intervals; three females were excluded from the
analysis because of low egg production. We recorded laying dates
for a minimum of three, a maximum of eight, and a mode of four
consecutive clutches per female (for details see Kubička et al., in
press). Temperature positively influenced the frequency of reproduction (ANOVA: F¼129.28, Po0.0001). Fisher’s post-hoc test revealed
that females at 30 1C produced clutches more frequently than did
females at 27 1C, which produced clutches much more frequently
than did females at 24 1C (Fig. 2). The mean interval between clutches
was unrelated to maternal size (ANCOVA: F2, 53 ¼0.01, P¼0.91).
17
Mean interclutch interval (days)
temperature, clutch number, and the interaction between clutch
number and temperature. Larger females tended to lay larger eggs.
Females tended to make larger eggs in later clutches, but the
magnitude of this clutch effect varied among thermal treatments
(see Fig. 1 and Table 1). Overall, females at the highest temperature
laid the smallest eggs (Fig. 1).
Masses and SVLs of females at the time when eggs were
collected for analysis of water and energy contents were similar
among thermal treatments (ANOVA: SVL: F2, 57 ¼2.01, P ¼0.14;
body mass: F2, 57 ¼0.07, P ¼0.93; N ¼60 females; Table 2). Still, we
161
16
15
14
13
12
11
10
9
8
24
27
Temperature (°C)
30
Fig. 2. The interval between clutches decreases with increasing environmental
temperature. Error bars denote 95% confidence intervals.
Table 2
Mean values of maternal body size and egg characteristics, with standard errors in parentheses. Egg characteristics at each environmental temperature were computed
from the average of two eggs for each female (N¼ 23, 19 and 18 females for 24, 27 and 30 1C, respectively).
Female body mass (g)
Female SVL (mm)
Egg wet mass (g)
Egg dry mass (g)
Egg energy density (cal g 1 of dry mass)
Egg energy content (cal)
24 1C
27 1C
11.75 (7 0.598)
74.26 (7 0.856)
0.94 (7 0.023)
0.266 ( 70.007)
4661.738 ( 753.392)
1237.544 ( 728.310)
11.99
76.14
0.96
0.28
4702.88
1291.15
30 1C
(70.342)
(70.922)
(70.013)
(70.004)
(749.054)
(721.929)
11.96 (7 0.484)
76.67 (7 0.978)
0.89 (7 0.022)
0.248 (7 0.005)
4621.852 (7 24.566)
1148.361 (7 25.790)
162
Z. Starostová et al. / Journal of Thermal Biology 37 (2012) 159–163
0.014
Reproductive rate (W)
0.013
0.012
0.011
0.010
0.009
0.008
0.007
24
27
Temperature (°C)
30
Fig. 3. The rate at which females allocate energy to reproduction was greater at 27
or 30 1C than it was at 24 1C. Means were adjusted for maternal body size. Error
bars denote 95% confidence intervals.
Temperature significantly impacted the rate at which females
used energy to reproduce (ANOVA: F ¼57.72, Po0.00001, N ¼57).
Reproductive rate did not differ between females at 27 and
females at 30 1C, while females at 24 1C allocated much smaller
amounts of energy to reproduction per unit of time. Larger
mothers had higher reproductive rates, but this relationship was
similar at all temperatures (ANCOVA–temperature: F ¼49.24,
Po0.00001; maternal size: F¼6.50, P ¼0.01; temperature–
maternal size interaction n.s. and dropped from the model based
on AIC; Fig. 3).
4. Discussion
The reproductive rate of P. picta increased with environmental
temperature, however the thermal effect did not accord with
predictions based on reaction kinetics as described by the Metabolic
Theory of Ecology (Gillooly et al., 2001; Hayward and Gillooly,
2011). Females at 27 1C and 30 1C had comparable rates of reproduction, because females at 27 1C produced clutches less frequently
but their eggs were larger. Thus, our results demonstrate that both
energy content of eggs and rates of oviposition are needed to
compare the thermal dependence of reproductive rate. In other
words, a complex thermal sensitivity of reproductive rate emerged
from distinct thermal sensitivities of egg size and composition and
clutch frequency.
Although egg size generally depended on environmental
temperature, the thermal effect on egg size was more pronounced
in later clutches (Fig. 1). The fact that the smallest eggs were laid
at the highest temperature accords with the general pattern
among ectotherms (Atkinson et al., 2001). Among lizards, a
similar pattern was reported in comparative studies of the genus
Sceloporus (Angilletta et al., 2006). By contrast, grass lizards
(Takydromus septentrionalis) produced the largest eggs at an
intermediate temperature (Luo et al., 2010). This result might
reflect differences between the life-histories of the grass lizard
and the Madagascar ground gecko. Unlike the gecko, which
produces frequent clutches of a fixed size, the grass lizard
produces clutches of different sizes on a seasonal basis; clutches
get smaller as the reproductive season progresses (Luo et al.,
2010). Females of P. picta at the higher temperatures laid smaller
eggs, relative to their body size, which does not support the view
that pelvic or other morphological constraints caused the thermal
dependence of egg size. The morphological constraint hypothesis
is not supported by experimental manipulations of the thermal
environments of insects, in which egg size depended on the
thermal regime of the mother at the time of vitellogenesis rather
than her thermal regime during the juvenile period (Blanckenhorn,
2000; Fischer et al., 2003). The thermal dependence of egg size in
ectotherms could reflect adaptive variation in energy allocation
among thermal environments (e.g. Perrin, 1988; Oufiero et al.,
2007). Nevertheless, adaptive explanations are not the only alternatives to the morphological constraint hypothesis. Support for an
adaptive explanation would be stronger if one knew the fitness
consequences of thermal variation in egg size. Such knowledge
would come from studies of the size-dependence of egg mortality
at various temperatures, as well as studies of thermal effects on
hatchling phenotypes (size, growth, locomotory performance or
behavior, e.g., Burger, 1989; Van Damme et al., 1992; Elphic and
Shine, 1998; Trnı́k et al., 2011, but see also Warner et al., 2012).
Moreover, manipulating the nutrition of P. picta revealed that egg
size depends on energy supply (Kubička and Kratochvı́l, 2009);
thus, temperature is not the only factor that affects reproductive
allocation. Interactions between temperature and other factors
should be considered when developing hypotheses about the
adaptive significance of thermal plasticity.
The scaling of water content with egg mass was not isometric,
because larger eggs contained proportionally greater amounts of
water. Thus, females at the highest temperature, which produced
small eggs, partially compensated for the negative size effect by
changes in egg composition. Nevertheless, the scaling of dry egg mass
with wet egg mass did not differ among temperatures, which
suggests that compensation is not directly connected to thermal
effects but is a general response associated with variation in egg size.
Eggs of geckos with hard, highly calcareous eggshells are unable to
absorb water from their environment (reviewed in Thompson and
Speake, 2004). In fact, all water necessary for successful embryonic
development must be provided by the mother before oviposition. The
scaling of water content with egg size could serve to manage water
balance during longer developmental times at lower temperatures.
Dry matter of eggs produced at different temperatures had similar
energy densities, which suggests similar proportions of proteins and
lipids, the major components of lizard eggs (reviewed in Thompson
and Speake, 2004).
Reproduction greatly increases the energy requirements of
P. picta. Non-reproducing females of this species have a standard
metabolic rate of approximately 8 mW at 25 1C based on their
resting oxygen consumption and a conversion factor of 20 J ml 1
of O2 (Starostová et al., unpublished data). This rate compares
favorably to the rate at which a reproductive female at 24 1C
expended energy on her eggs (Fig. 3). Hence, females that become
reproductive could increase their energy requirements by 100%
just to cover the energy invested in offspring. At the same time,
reproduction can impose indirect costs stemming from the metabolic demands of pregnancy. Angilletta and Sears (2000) estimated
that metabolic rates were more than doubled in post-vitellogenic,
gravid lizards (Sceloporus undulatus), relative to non-gravid lizards.
Such indirect costs would add to the direct costs estimated in this
study. Females of P. picta, which are continuous breeders, must
sustain elevated levels of energy expenditure for long periods.
Moreover, their metabolic rates during activity must be even
higher. It would be interesting to explore whether these lizards
meet the high energetic demands of reproduction through behavioral shifts in activity (Cooper et al., 1990; Vézina et al., 2006) or
through changes in feeding behavior and assimilation efficiency
(Angilletta, 2001). The latter possibility seems more probable for P.
picta, which fuels reproductive expenditure primarily from incoming energy and stores fat only after meeting reproductive costs
(Kubička and Kratochvı́l, 2009).
A nonincreasing relationship between temperature and reproductive rate (Fig. 3) emerged from distinct thermal sensitivities of
Z. Starostová et al. / Journal of Thermal Biology 37 (2012) 159–163
egg size, egg composition, and clutch frequency. The mean size of
eggs was considerably smaller at the highest temperature, while
the mean energy density remained relatively constant among
thermal treatments. The frequency of clutches increased nonlinearly with increasing temperature. By integrating these thermal
sensitivities, we determined a relationship between temperature
and reproductive rate that could not have been predicted from the
thermal sensitivity of any single component of reproduction. This
finding suggests that previous studies, which estimate reproductive rates without quantifying all components of reproduction (e.g.
Boback and Guyer, 2008; Sibly and Brown, 2007; Hayward and
Gillooly, 2011) may be biased. To identify general patterns of
reproductive plasticity, biologists will need to directly measure
the size and composition of eggs and the size and frequency of
clutches.
Acknowledgments
The authors thank Libor Mikeš and Dagmar Kozáková for help
with lyophilization, Jason Borchert and Jan Červenka for help and
stimulating discussions, and two anonymous reviewers for comments
that improved our article. The research was supported by the Czech
Science Foundation, project No. P505/10/P174 and the ThermAdapt
research network program of the European Science Foundation,
Exchange Grant no. 3022 (http://www.esf.org/thermadapt). The
experiment was performed with approval from the Ethical Committee of the Faculty of Science, Charles University in Prague.
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