Oikos 000: 001–007, 2011
doi: 10.1111/j.1600-0706.2010.18809.x
© 2011 The Authors. Oikos © 2011 Nordic Society Oikos
Subject Editor: Tom J. Webb. Accepted 4 October 2010
Capital energy drives production of multiple clutches whereas
income energy fuels growth in female collared lizards
Crotaphytus collaris
Rory S. Telemeco and Troy A. Baird
R. S. Telemeco ([email protected]) and T. A. Baird, Dept of Biology, Univ. of Central Oklahoma, 100 N. University Drive, Edmond, OK
73034, USA. Present address for RST: Dept of Ecology, Evolution and Organismal Biology, Iowa State Univ., Ames, IA 50011, USA.
Animals invest energy in reproduction that is obtained at two distinct times relative to the reproductive cycle. Energy
obtained during egg production is referred to as income energy whereas stored energy acquired prior to reproduction is
capital energy. Similar to most ectotherms, squamate reptiles are generally hypothesized to be capital breeders. Nearly all
squamates in which income/capital energy investment has been examined thus far produce only one clutch per reproductive season. Although it is likely that squamates producing multiple seasonal clutches fuel first clutches with capital energy,
either capital or income energy may be used to produce later clutches. We first monitored female eastern collared lizards
over 14 reproductive seasons to confirm that the number of clutches females produce seasonally is a plastic response to variable environmental parameters, and to examine the effects of female body condition at the beginning of the reproductive
season on clutch production. Clutch production varied annually and both the size and number of clutches were positively
correlated with body condition. We then tested the competing predictions of the income and capital hypotheses experimentally by supplementing the diets of female collared lizards in situ for one season. Diet-supplementation had no effect
on the number of clutches produced but increased growth rates of gravid females. We further tested the competing predictions of these two hypotheses by examining variation in maternal energy investment per clutch using preserved specimens
collected near our primary field site. Clutch size was highly correlated with female body size. Together, our results suggest
that variation in reproductive output by female collared lizards is linked to stored capital energy rather than income energy,
similar to most ectotherms.
Life-history theory predicts that iteroparous organisms will
partition energy among growth, reproduction and storage
(Fisher 1930, Adolph and Porter 1993, Shine 2005). Patterns of energy partitioning have received much theoretical and experimental attention (Williams 1966, Reznick et
al. 2000, Therrien et al. 2008). However, the relationship
between the timing of energy acquisition and expenditure
on reproduction is less well studied (Olsson and Shine 1997,
Roff et al. 2006). Energy expended on reproduction may
either be acquired during a reproductive bout (hereafter
income energy) or be derived from energy reserves acquired
prior to reproduction (hereafter capital energy; Stearns 1992,
Jönsson 1997). Organisms that primarily fuel reproduction
with income energy are called income breeders (Drent and
Daan 1980, Jönsson 1997, Houston et al. 2006) whereas
capital breeders primarily fuel reproduction using capital
energy (Doughty and Shine 1997, Bonnet et al. 2002, Bowen
et al. 2006). Whether income or capital energy is used to fuel
reproduction may depend upon the temporal and spatial
correspondence between food availability and other parameters necessary for reproduction (Bonnet 1998, Shine 2005).
Capital breeding may be advantageous because it allows
temporal disassociation of energy aquisition and reproductive
expenditure (Doughty and Shine 1997, Bonnet et al. 2002,
Bowen et al. 2006). By contrast, the ability to use income
energy to increase reproductive output may be advantageous
when food is abundant.
Income and capital breeding strategies are best viewed
as ends of a continuum with most animals investing some
stored and recently acquired energy in reproduction (Bonnet
1998, Doughty and Shine 1998). Even so, the vast majority of endothermic vertebrates examined to date primarily fuel reproduction using income energy (Bonnet 1998,
Houston et al. 2006), whereas ectothermic vertebrates are
thought to primarily fuel reproduction using capital energy
(Bonnet 1998, Du et al. 2005, Shine 2005). Many studies of reproductive energetics have used squamate reptiles
(snakes and lizards) that are limited to production of a single
annual clutch as experimental models (Bonnet 1998, Shine
2005). Of these, most must meet a threshold level of stored
energy before egg production is possible (Stearns 1992,
Madsen and Shine 1999), which in some species requires years
to attain (Shine and Madsen 1997, Bonnet et al. 2002,
Lourdais et al. 2003). Much less is known about the
1
relationship between energy acquisition and egg production in squamates that produce multiple clutches per season
(we are aware of only five studies; Hahn and Tinkle 1965,
Derickson 1976, Shanbhag and Prasad 1992, Brown and
Shine 2002, Warner et al. 2007). Given the prevalence of
capital breeding in species that produce one clutch annually, it is possible that multiple-clutching species also use this
tactic (Shine 2005). However, the observation that at least
four squamates use income energy to produce second and
third clutches (Hahn and Tinkle 1965, Shanbhag and Prasad
1992, Brown and Shine 2002, Warner et al. 2007) indicates
that studies of the energetics of egg production in additional
species that produce multiple seasonal clutches are merited.
Eastern collared lizards Crotaphytus collaris are a good system for examining the relative roles of income and capital
energy in the production of multiple seasonal clutches which
are common. The short time (∼ 2 weeks) available for foraging between emergence from hibernacula and detectable follicle development (Baird et al. 2001, Baird and Sloan 2003)
suggests that capital stores fuel the first clutch of the season.
However, the second and third clutches (Baird et al. 2001,
Baird and Sloan 2003) may be fuelled by either income or
capital energy. The income hypothesis predicts that current
food intake will influence the number of clutches that lizards produce in a given season and/or the amount of energy
invested per clutch. Alternatively, the capital hypothesis predicts that lizards will allocate income energy toward growth
and/or storage, and will use capital energy acquired during
previous seasons to fuel reproduction. Furthermore, maternal investment per clutch should not vary in response to food
availability under the capital hypothesis, because females
should delay reproduction until they have stored enough
energy to produce optimally sized clutches. Maternal investment per clutch may vary, however, in response to changes
in factors that affect optimal clutch size such as body volume
(Tinkle et al. 1993, Bizerra et al. 2005).
We used a multifaceted approach to test predictions of
the income and capital hypotheses in female collared lizards. First, we monitored females during 14 seasons to test
whether or not the number of clutches produced is a plastic
response to variable environmental parameters (likely food
availability and/or opportunities to forage) rather than a
genetically canalized phenotype. We then used these longterm data to examine the effects of body condition upon
spring emergence (proxy for capital reserves) on reproductive
output. Next, we experimentally supplemented the diets of
reproductively active females in situ to examine the effects of
increased income energy on seasonal clutch production and
growth rates. Finally, we examined the dry mass of clutches
collected from preserved specimens to determine whether
variation in maternal investment per clutch better supports
the predictions of the income (highly variable investment) or
capital (little variation in investment) hypotheses.
Material and methods
Study site, species and general methods
This study was conducted at Arcadia Lake Dam (hereafter
AL) located on State Highway 66, approximately 9.6 km
2
east of Edmond, Oklahoma (Baird et al. 2003). At AL, collared lizards occur on three, topographically homogeneous
patches (1505–19 850 m2) of granite boulders imported
to construct flood-control spillways. These boulder patches
are separated by at least 50 m of open prairie grass that is
rarely traversed by lizards. This site is optimal for field study
because human access is restricted, lizards are undisturbed
and readily observed, and the age of all individuals is known
from mark–recapture studies conducted since 1990 (Baird
et al. 2003). Beginning when they were hatchlings, lizards
were noosed, the terminal phalanges of three digits were
uniquely clipped for permanent identification, and unique
combinations of non-toxic acrylic paint spots were applied
to the dorsum for identification from a distance. Sex of
hatchling C. collaris is readily determined by the presence
(males) or absence (females) of enlarged post-anal scales, and
later by development of dimorphic coloration (McCoy et al.
1997, Baird et al. 2003).
The reproductive season of collared lizards at AL is midApril through early-July. Males that are two years of age and
older defend territories that overlap the home-ranges of 3–10
females (Baird et al. 1996). Females are not territorial and,
because males compete for access to mates, female reproductive success is not limited by access to males (Baird and Sloan
2003). Importantly, follicle recruitment occurs prior to each
individual clutch rather than simultaneously at the beginning of the reproductive season (Baird unpubl.). Females
that are two years of age or older (hereafter 2y-females)
begin producing their first clutches in mid-April and usually oviposit during the second week of May, at which time
their second clutches begin to ripen. Females that hatched
the previous season and are 75 mm snout–vent length
(SVL) upon emergence from hibernacula (hereafter first-year
females) also produce eggs. Clutch production by first-year
females begins in early to mid-May, approximately the same
time that 2y-females begin production of their second
clutches (Baird et al. 2001, Baird and Sloan 2003). Females
that are  75 mm SVL upon emergence from hibernacula
do not reproduce (Baird unpubl.).
Unless stated otherwise, we used the software program
Statview 5 (SAS Inst.) for all analyses and an alpha level of
0.05. To ensure that we met the assumptions of parametric
statistics, we tested for normality using Shapiro-Wilk analyses with the software program Statistix 7 (Analytical Software, Tallahassee, FL) and for homogeneity of variance using
F-tests.
Annual variation in clutch production
We monitored clutch production by 534 reproductively
mature C. collaris from 1993–2006 (x– females per year 
1.0 SE: first-year  21.5  3.4; 2y  17.9  2.3). We
captured females multiple times throughout each reproductive season by noosing (x– number of captures 1.0 SE 
6.6  0.3). Because these captures were spread throughout
May and June, and because we made a special effort to capture
females that were known to be carrying shelling eggs and
then appeared emaciated and/or covered with dried mud
(indicators of oviposition; Sloan and Baird 1999, Baird et al.
2001), we were able to monitor the ripening and oviposition
of all clutches. At each capture, we measured SVL and mass,
and palped the abdomen to characterize the development of
follicles/eggs following criteria used previously for C. collaris
in central Oklahoma (Sloan and Baird 1999, Baird 2004).
We grouped females into one of six follicle/egg development
categories: 1) prior to development of enlarging follicles, 2)
2–8 mm rounded follicles in the ovary, 3) larger (9–12 mm),
round follicles either in the ovary or recently ovulated, 4)
oval, oviductal follicles prior to shelling, 5) shelled, oval,
oviductal eggs having a well defined outline, and 6) postoviposition indicated by females being gravid at the previous capture followed by absence of eggs at the subsequent
capture. Although this method allowed us to monitor the
presence/absence and progress of developing follicles, it did
not allow us to accurately determine the number of follicles developing in a given clutch. Furthermore, we were
unable to locate and count eggs after oviposition because at
AL females excavate nests underneath boulders that are too
large to move. We therefore used the difference in female
body mass measured before and after oviposition as a proxy
estimate of clutch mass. We returned all individuals to their
precise capture locations within 20 minutes of noosing.
Because females at AL produced either one, two, or three
clutches per season, the number of clutches females produce
per season is a discrete variable. We therefore used c2-analyses
to examine variation in the number of clutches produced
by first-year and 2y-females, and annual variation in the
number of clutches produced per season by females of both
age classes (together and separately). To compare the relationships between annual variation and the number of clutches
produced in first-year and 2y-females we regressed the
mean number of clutches produced by each age class each
year. As an estimate of capital energy reserves at the beginning of the reproductive season, we calculated body condition (mass/SVL) upon spring emergence from hibernacula
for each female using measurements taken at each female’s
first seasonal capture. We used logistic regression to examine
the effects of initial female body condition on the number of
clutches that females produced per season using the software
program JMP 8 (SAS Inst.). We then used linear-regression
analyses to examine the effects of initial body condition
on the masses of first and second clutches (n  177 and
n  64, respectively). Only clutch masses calculated using
pre-oviposition and post-oviposition body-masses collected
10 d apart were included in these analyses because a visual
examination of the data revealed this to be the point above
which some females gained weight between the two measurements. Because production of third clutches is relatively rare
and unpredictable, our sample (n  17) was not sufficient to
examine the effects of body-condition on third clutches.
Diet-supplementation experiment
To experimentally test the influence of income energy on
clutch production, we manipulated the food intake of 31
reproductively active female C. collaris in the field. From
8 May–30 June 2006, females were noosed every 1–4
d (x– number of captures  1.0 SE first-year: 12.2  2.7,
n  13; 2y:12.1  2.4, n  18). At each capture, one
author (RST) measured and recorded the reproductive condition of females as described above and made three measurements of SVL to ensure repeatability. We characterized
female body size using SVL rather than body mass because
the later was likely confounded by variation in gut weight
resulting from diet-supplementation. Individual growth
rates were determined by dividing the difference between
initial and final SVL by the number of days between the two
measurements.
The diets of 15 of these females (first-year n  6,
2y n  9) were supplemented by feeding crickets (approx.
20 mm) at each capture (x– number of crickets/capture 
1.0 SE  4.7  0.32), whereas the 16 control females (firstyear n  7, 2y n  9) that lived on the same rock patches
ate only their natural diet. We chose crickets for dietsupplementation because orthopterans are the major prey of
C. collaris at AL (Best and Pfaffenberger 1987, Baird and
Sloan 2003). Crickets were maintained on Fluker’s brand
‘gut loading’ cricket food thereby removing the need to
dust them with vitamins. Diet-supplementation involved
holding lizards by the pectoral girdle and presenting them
with a cricket held in forceps. Lizards were allowed to
take crickets voluntarily and were not force-fed. Once lizards had taken five crickets or refused to take more, they
were placed in a 9.5-l bucket with lid for 5–7 min and
allowed to swallow completely. In a pilot study, we found
that if lizards regurgitated, they did so within this period
(Telemeco unpubl.). However, no lizards regurgitated
during the present study. After each capture, we returned
lizards to where they were first sighted prior to noosing.
There was no difference in the number of times that females
in the two diet-supplementation treatments were captured
(x– number of captures  1.0 SE  diet-supplemented:
12.9  2.8, non-diet-supplemented: 13.6  2.5; ANOVA:
F1,26  0.04, p  0.84).
Females resumed normal behavior (e.g. basking, social
interaction, scanning for prey) within 5 min of release at the
point of capture (see similarly; Baird 2008, 2009). Moreover,
all subjects increased in SVL over the course of this study,
and 68% of subjects survived at least until the end of the
reproductive season. This rate of survival to the end of the
reproductive season is well within the normal range observed
during several seasons of studies (1992–2010) of this same
population (Baird unpubl.). Together these observations
strongly suggest that our manipulations did not adversely
affect the condition of female subjects. We attempted to
measure growth rates and the number of clutches produced
for our experimental and control females during the 2007
season. However, we were unable to do so because only 19%
of them survived to 2007. Because our female subjects were
in good condition at the end of the experiment in June, and
there are many possible sources of mortality (predation,
freezing, starvation, old age) that could have killed lizards
over the 10 months between the end of the experiment and
emergence in 2007, we think that it is unlikely that our
manipulation was responsible for the high rate of mortality.
To examine the effects of diet supplementation on the
number of clutches produced by females of each age-class,
we used separate c2-analyses. We then used two-factor
analysis of covariance (ANCOVA) to examine the effects
of diet-supplementation and age-class on growth rate
with initial SVL as the covariate. Because growth rate data
were not normal despite conventional transformation,
they were rank-transformed to meet the requirements of
3
parametric ANCOVA (Conover and Iman 1981, 1982,
Kepner and Wackerly 1996). ANCOVA revealed that initial
SVL had a much stronger effect on growth rate than ageclass. We therefore used linear regression analyses to examine
how much variation in growth rate was explained by SVL
within the two diet-supplementation treatments.
Maternal energy investment per clutch
Because we were unable to collect eggs from nests, we
further examined variation in the amount of energy that
females invest per clutch using specimens collected near
AL from 1992–1994. These lizards were located by periodically driving the rural roads within an 8 km radius of
AL during the AL reproductive season and visually scanning
adjacent rocks. These lizards were noosed and transported
to the laboratory at the Univ. of Central Oklahoma where
they were measured (SVL and body mass), euthanized by
freezing at –20°C, and dissected. These lizards did not differ
in size from those used in the diet-supplementation experiment described above (SVL: t48  –0.832, p  0.41, mass:
U20,19  184, p  0.87). After dissection, the reproductive
tracts of each female were removed and preserved individually
in 10% formalin. We only used specimens having undamaged clutches of fully developed, shelled eggs (n  14 of the
51 female specimens collected). In May 2009, the eggs
(n  100) were separated from any remaining oviductal tissues and water rinsed to remove the formalin. To determine
dry egg mass as an estimate for maternal energy investment
per egg, eggs (intact with shell) were placed individually in
glass petri dishes of known mass, weighed, dried to constant
mass at 40°C (Parker and Andrews 2006), and re-weighed
on the same electronic balance. For each clutch, individual
dry egg masses were summed to calculate total dry clutch
mass (estimate for maternal energy investment per clutch).
We used a multiple linear regression to examine the effects of
female SVL and body mass on dry clutch mass. Because these
individuals were not monitored from hatching like those at
AL, we were unable to assign them to age-classes for analyses.
Figure 1. Annual variation in the number of clutches (x–  1.0 SE)
produced by first-year and 2y-female eastern collared lizards at
Arcadia Lake from 1993–2006.
with the number of clutches that females produced per
season (c22  79.06, r2  0.12, p  0.0001) and the mass
of those clutches (clutch 1: F1,165  129.47, r2  0.44,
p  0.0001, clutch 2: F1,62  8.03, r2  0.12, p  0.0062,
Fig. 2).
Diet-supplementation experiment
Diet-supplementation did not influence the number of
clutches produced by females of either age-class (firstyear: c22  2.20, p  0.33; 2y: c22  0.93, p  0.63;
Fig. 3A), or all females pooled (all females: c23  1.93,
p  0.59). However, similar to results from the 14-y dataset (Fig. 1), age class did affect the number of clutches that
females produced with 2y-females producing 1.3 more
clutches (c23  9.85, p  0.02) on average than first-year
Results
Annual variation in clutch production
On average, females produced 1.5 clutches per season
(SE  0.03, range  1–3). Clutch production by 2yfemales (x–  1.0 SE  1.8  0.05) exceeded (c22  60.5,
p  0.0001) that of first-year females (x–  1.0 SE  1.4 
0.03). The number of clutches produced per season showed
significant annual variation in both age classes (Fig. 1,
first-year: c226  61.1, p  0.0001, 2y: c224  98.7,
p  0.0001, all females: c226  143.8, p  0.0001).
When all years were included in regression analysis,
annual variation in the number of clutches produced by
first-year and 2y-females were not significantly correlated
(F1,11  2.15, p  0.17, r2  0.16), although there was
a positive trend. However, when we removed one outlying
year (1994, Fig. 1) from the analysis, this positive trend
became statistically significant (F1,10  9.43, p  0.012,
r2  0.49). Initial body condition was positively correlated
4
Figure 2. Effects of body condition (mass/snout-vent length) of
female eastern collared lizards at Arcadia Lake upon spring emergence from hibernacula on total clutch mass for (A) the first clutch
of the season (p  0.05) and (B) the second clutch of the season
(p  0.05). Clutch mass was estimated by subtracting female body
mass after oviposition from female body mass before oviposition.
Figure 4. Effects of snout– vent length upon spring emergence from
hibernacula on the growth rates of diet-supplemented (p  0.05)
and non-diet-supplemented (p  0.05) female eastern collared
lizards at AL.
Discussion
Figure 3. Effects of supplementing the diets of first-year and
2y-female eastern collared lizards at Arcadia Lake on (A) number
of clutches produced (x–  1.0 SE), and (B) growth-rates (x– 1.0
SE). Different letters above adjacent bars indicate statistically
significant (p  0.05) differences.
females (Fig. 3A). Furthermore, diet-supplementation had a
positive effect on growth rate (F1,24  29.94, p  0.0001),
with diet-supplemented females growing an average of
0.31 mm d-1 more than those females that were not dietsupplemented (Fig. 3B). Even though age class appeared to
have a differential effect on growth rate with first-year females
growing more when diet-supplemented than 2y-females
(Fig. 3B), ANCOVA revealed that the effect of age class on
growth rate was not significant (F1,24  1.59, p  0.22)
when initial SVL (F1,24  8.52, p  0.008) was accounted
for. Furthermore, ANCOVA revealed no significant interactions (p  0.2 for all). Linear regression analyses revealed a
significant negative effect of initial SVL on the growth rates
of diet supplemented females (F1,12  16.31, r2  0.58,
p  0.002, slope  –0.023, Fig. 4), but only a negative
trend in non-diet-supplemented females (F1,12  3.39,
r2  0.22, p  0.09, slope  –0.005, Fig. 4).
Two important and related components of an organism’s lifehistory are how they partition available energy (Reznick et al.
2000, Therrien et al. 2008) and how they make reproductive
decisions (i.e. when to reproduce, how much energy to allocate to a reproductive event, etc., Emlen and Wrege 1994,
Shine 2005, Hesse et al. 2008). Especially for iteroparous species, the relative contributions of capital and income energy
investments toward reproduction may strongly impact these
important life-history traits (Bonnet 1998, Shine 2005). We
describe how energy from income and capital sources is differentially utilized by female eastern collared lizards during
the production of multiple seasonal clutches and some of the
impacts of this allocation pattern on the life-history of these
organisms.
Marked variation in clutch production during 14 seasons and a positive correlation between this variation and
initial female body condition suggest that the number of
clutches produced by female collared lizards each season is
a plastic response to environmental variation prior to the
onset of reproduction. Moreover, diet supplementation during follicular development did not increase the number of
clutches produced by either first-year or 2yr-females even
Maternal energy investment per clutch
Collared lizards produced 4–11 eggs per clutch (x–  1.0
SE  6.9  0.46). The mean (1.0 SE) dry mass of these
eggs was 0.51  0.005 g and the mean (1.0 SE) dry mass
for entire clutches (maternal investment per clutch) was
3.6  0.3 g. Multiple linear regression revealed that maternal body size (mass and SVL) explained nearly all variation
in dry clutch mass (F2,11  36.23, p  0.0001, r2  0.868)
with only maternal body mass explaining a significant
portion of this variation (body-mass: p  0.0031, SVL:
p  0.58, Fig. 5).
Figure 5. Effect of female body mass on maternal energy investment per clutch (measured as dry clutch mass) in eastern collared
lizards from central Oklahoma.
5
though the large differences that we observed in the growth
rates of diet-supplemented and non-diet-supplemented
individuals suggest that we successfully increased the income
energetic budgets of these lizards. These results suggest that
the number of clutches that female collared lizards produce
each season is pre-determined by the capital energy reserves
that they have upon emergence from hibernacula in the
spring, rather than income energy acquired during the reproductive season.
If surplus income energy does not affect the number of
clutches that female collared lizards produce per season,
how is this energy allocated? Our result that diet-supplemented
females grew faster than non-diet-supplemented females
suggests that income energy is allocated toward somatic
growth. It is unlikely that income energy is allocated toward
the production of larger clutches because nearly all (87%) of
the variation that we documented in dried clutch mass was
explained by variation in female body size. Further supporting this conclusion, initial body condition over our 14 year
data set had a positive effect on the mass of both first and second clutches. Because clutch size increases with body size in
female collared lizards (Fig. 5), and larger individuals should
be able to carry larger energy stores (Madsen and Shine
1999, 2002, Roff et al. 2006), allocation of income energy
to growth can be interpreted as a form of capital investment
in this species. Therefore, our data suggest that female C. collaris allocate income energy toward capital investments such
as somatic growth rather than toward immediate reproduction, either through increased clutch size or number.
Our diet-supplementation experiment also revealed that
small females grew faster than large females, independent of
age. The fact that this correlation is strongest in diet-supplemented
females suggests that experimental feeding swamped natural
variation in income energy thereby unmasking the effects
of body size on growth rate. These data suggest that female
body size differences influence their energy-allocation priorities with investment in growth being more adaptive for small
females. Fast growth may increase fitness of females in this
species in a variety of ways. For instance, larger females produce more eggs and may be less susceptible to predators and
winter kill (Baird et al. 2001, Baird and Sloan 2003, Husak
et al. 2006). Our results suggest that as females increase in size,
the advantages of further growth decrease and an increasing
proportion of income energy is shifted toward other things,
presumably the production of long-term energy stores. This
energy investment pattern suggests a tradeoff between the
costs and benefits of allocating energy toward growth, and is
consistent with what life-history theory predicts for iteroparous organisms with indeterminate growth (Stearns 1992,
Bowden et al. 2004, Shine 2005).
Although our data suggest that reproductive allocation in
female collared lizards (e.g. number of clutches and maternal investment per clutch) is determined by capital energy
availability, we cannot rule out the possibility that both capital and income resources are mobilized for egg production
(Casas et al. 2005, Santos et al. 2007, Warner et al. 2008).
In those squamates where the metabolic mobilization of
reproductive resources has been tracked (we know of two),
lipids are derived from capital stores whereas proteins are
derived from both capital and income resources (Santos
and Llorente 2004, Santos et al. 2007, Warner et al. 2008).
6
Because yolk lipids are the primary source of energy for
embryonic development in oviparous amniotes (i.e. birds;
Speake et al. 1998, and squamates; Thompson et al. 2001),
capital resources provide the majority of energy for offspring
development in these species. Therefore, assuming that
metabolic mobilization of reproductive resources in female
collared lizards follows the same pattern, our results suggest
that capital resources provide the energy (i.e. fuel) for egg
production in female collared lizards.
In conclusion, we find that the seasonal reproductive output of female collared lizards is primarily determined by how
large females are and the number of clutches that they produce. Furthermore, our data suggest that variation in these
factors is driven by capital energy stores developed prior to
reproduction. To our knowledge, this is the first time that
a multi-clutching squamate species has been shown to fuel
production of all clutches primarily using capital energy.
Given the prevalence of capital breeding in squamates that
produce a single clutch annually (Bonnet 1998, Shine 2005),
the occurrence of the same pattern in our multi-clutching
lizard species reinforces the generalization that ectotherms
are primarily capital breeders.
Acknowledgements – We thank W. Parkerson of the United States
Army Corps of Engineers for access to the Arcadia Lake Study
Site, C. Brawn, M. Telemeco, J. Curtis, B. Martin and S. LaFave
for their assistance in the field and laboratory. We further thank
F. Janzen, D. Warner, C. Chandler, G. Cordero, T. Mitchell,
A. Sethuraman, J. Refsnider, X. Bonnet and L. Luiselli for constructive comments. Funding was provided by the Joe C. Jackson
College of Graduate Studies and Research at the Univ. of Central
Oklahoma. This research complies with United States law and was
conducted with the approval of the Oklahoma Dept of Wildlife
Conservation (permit no. 4227 to TAB) and the Institutional
Animal Care and Use Committee at the Univ. of Central
Oklahoma.
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