Division of Comparative Physiology and Biochemistry, Society For Integrative and Comparative Biology, The University of Chicago Press Physiological Zoology

Division of Comparative Physiology and Biochemistry, Society for Integrative and
Comparative Biology
Proximate and Evolutionary Constraints on Energy Relations of Reptiles
Author(s): Justin D. Congdon
Source: Physiological Zoology, Vol. 62, No. 2 (Mar. - Apr., 1989), pp. 356-373
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356
Proximate and Evolutionary Constraints on Energy
Relations of Reptiles
Justin D. Congdon
Savannah River Ecology Laboratory, Drawer E, Aiken, South Carolina 29802
Accepted 7/15/88
Abstract
Proximate constraints on the energetics of desert lizards and turtlesfall into four
major categories: (1) absolute resource availability; (2) harvest rate limitations;
(3)process rate limitations; and (4) limitation on harvest orprocessing resources

imposed by risk ofpredation. Patterns ofbasking behavior and allocation of resources to reproduction and growth ofturtles at high latitudes suggest that ambient
air and marsh temperatures combine to regulate the timing and rates of energy
processing and allocation. Because reptile eggs contain all of the chemical energy
available to developing embryos, interactions between the level ofparental investment in each offspring and egg size must, by definition, occur. Thatportion of the
egg material that is invested in the egg butfunctions asparental care of the hatchling after it leaves the eggfunctionsprimarily to affect hatchling quality rather than
hatchling size. Therefore, with regard to many reptiles, optimal egg-size models
would be more aptly considered to be optimal offspring-quality models.
Introduction
A number of evolutionary theories are based on assumed interactions among
resource availability, behavior, morphology, and age-specific demographics. These interactions presumably determine the association of an organism's life-history traits and energy budgets. However, the argument that sim-
ilar life-history phenotypes can result from very different selective forces
(Wilbur, Tinkle, and Collins 1974) seems well founded and can certainly
be extended to energy-allocation phenotypes as well. Interactions among
trophic level, morphology, demographic environment, and phylogeny of an
organism combine to make the mere presentation of total energy budgets,

in the absence of an ecological and evolutionary context, of limited value.
At present, total energy budgets of reptiles represent first-order approxima-
tions of average energy allocations for all individuals or for individuals of

each sex within a population (Avery 1975; Turner, Medica, and Kowalewsky
Physiological Zoology 62(2):356-373. 1989. @ 1989 by The University of Chicago.

All rights reserved. 0031-935X/89/6202-8831$02.00
Constraints on Energetics of Reptiles 357
1976; Congdon, Dunham, and Tinkle 1982; Nagy 1982). As such, the resolution needed to distinguish among various sequential decision-making processes that lead to energy budget phenotypes is, at best, only partially attained.
The purpose of this article is to review some concepts related to construction and interpretation of ecological energy budgets that attempt to measure
an individual's allocation of net assimilated energy to the competing com-
partments of maintenance, growth, reproduction, and storage (Wiegert

1968; Congdon et al. 1982; Nagy 1982; Anderson and Karasov 1988). To ac-
complish this goal, I shall (1) discuss some broad categories of resource
constraint on energy acquisition and allocation of desert lizards and temper-
ate-zone turtles; (2) examine some data on ecological and life-history factors that constrain energy allocations of desert lizards in general and turtles
on the University of Michigan's E. S. George Reserve (ESGR) in Livingston

County, Michigan; and (3) review life-history theories concerning predictions about energy-allocation decisions of reptiles.
I. Major Categories of Constraints on Resource Availability

Interpretations of ecological energy budgets and most, if not all, life-history
theories are based on the assumption that the energy available to an individ-
ual is finite. The maximum resources that can be harvested by individuals

may be set by absolute quantity of resources available or by constraints imposed during foraging, handling, or processing of resources. Temporal constraints may take the form of biophysical limitations on energy acquisition
and allocation that may be imposed daily or seasonally or by competing

demands for time spent in social activities. Levels of resource acquisition
for a given level of resources and associated biophysical and time constraints
might then be further limited by risks associated with resource acquisition.
Resource Availability
A comparison of the types of energy constraints that may exist among reptiles indicates that correct identification of the type and cause of the limita-
tion is important (table 1). The response of the animal to different types
of energy-acquisition constraints may be the same in different habitats or
different in similar habitats.
Low primary productivity of desert habitats is primarily caused by low wa-
ter availability (Noy-Meir 1973, 1974; Webb et al. 1978; Cunningham et al.
1979; Hadley and Szarek 1981) that indirectly limits secondary production
(Dunham 1981). Of secondary influence are the timing, frequency, and inThis content downloaded from 177.230.235.179 on Sat, 09 Apr 2016 04:08:26 UTC
358 Justin D. Congdon
TABLE 1
Possible causes of limitation on energy acquisition and

processing of reptiles
Limitations
Location
Absolute resource availability Deserts

Harvest rate Deserts, high latitude, or altitude
Biophysical
Risk of harvest activities
Social activities
Process rate High latitude or altitude

Food type
Biophysical
Water availability
Risk of thermoregulating
tensity of rainfall, soil type, and nitrogen availability (Lightfoot and Whitford
1987) and their relative effects on annual and perennial plants (Evanari et
al. 1976; Cunningham et al. 1979; Szarek 1979; Hadley and Szarek 1981).
For example, in the Mojave Desert, which averages approximately 1,200 m
elevation, precipitation seldom exceeds 12.5 cm per year and occurs primarily during the relatively cold winter (Shreve 1925). Annual net primary pro-
duction averages 14-43 g dry mass/m2. In contrast, most of the Sonoran

Desert is below 600 m elevation, and rainfall there averages under 12 cm
and occurs almost equally during winter and summer (Shreve 1942). Annual
net primary production averages 92-129 g dry mass/m2. Precipitation has
been shown to be tightly linked to resource availability in desert habitats
(Turner 1973, 1974; Dunham 1981).

Desert reptiles, whether herbivorous, insectivorous, or carnivorous, certainly face resource limitation that fluctuates seasonally and sporadically.
The intensity and frequency of these fluctuations can be expected to have
major effects on the timing of energy storage and allocation. Sparse rainfall
limits the amount of plant production and also may result in much of the
available plant material's being too dry for herbivores to eat. For example,
the chuckwalla (Sauromalus obesus; Nagy and Shoemaker 1975) and the
desert tortoise (Scaptochelys agassizii; Nagy and Medica 1986), both herbivorous reptiles, may have energy available in the form of dried plant material,
but this cannot be processed while there are no alternative sources of water.
A similar condition has also been shown in jackrabbits in the Mojave Desert
(Nagy, Shoemaker, and Costa 1976). Unlike herbivores, both insectivorous

and carnivorous reptiles obtain preformed water in food, so reduced rainfall
acts primarily to reduce prey abundance rather than quality. Two studies
have documented reduced growth rates in insectivorous lizards that were
associated with low food resources (Dunham 1978; Ballinger and Congdon 1980).
Limitations on Harvest Rate
Linked to absolute resource limitation in the desert are a set of constraints
on the rate of harvesting resources (table 1). These constraints can be as

obvious as the restrictions placed on activity over a relatively long period by
seasonally high or low temperatures. In some habitats and situations, similar
constraints can also occur on a daily basis (Karasov and Anderson 1984;
Grant and Dunham 1987; Anderson and Karasov 1988). Perhaps the best
study of this type of daily constraint has been made on an insectivorous liz-
ard (Sceloporus merriami) in the Big Bend National Monument in west

Texas (Grant and Dunham 1987). During summer, the thermal environment
restricted daily activity to approximately a 2-h period in the morning and a
brief period in late afternoon. Despite the apparent severity of time constraints on activity, the lizard has an average preferred body temperature
lower than that of any other North American iguanid lizard studied (Grant
and Dunham 1987). The restricted daily activity period, coupled with the
low productivity of desert habitat, would seem to place the lizard in a very
poor environment for food acquisition. However, it would be interesting

to know whether the same thermal constraints that affect lizard behavior
concentrate the activity of many insect prey items into the same microhabitat
and window of time.
Competing demands on restricted activity times can also have a dramatic

effect on the short-term energy balance of animals. For example, some male
lizards spend much of their time defending boundaries of territories, displaying from prominent sites (Ruby 1981; Ruby and Dunham 1984), or actively searching for females (Anderson 1986; Anderson and Karasov 1988).
During the breeding season, male Sceloporusjarrovi are active most of the
day every day, lose body mass rapidly, and are in a negative energy balance.
In contrast, gravid females are active only for short periods about every third
day and yet are able to maintain a constant body mass and energy balance
(Congdon 1977). Large males of the wide-foraging lizard Cnemidophorus

tigris spend much time patrolling their home ranges during the reproduc-
tive season and maintain a constant energy balance, whereas females have a
positive energy balance during vitellogenesis (Anderson and Karasov 1988).
Process Rate Limitation
An organism's total energy intake may be limited not only by its ability to
harvest food but also by its ability to process food already harvested. In contrast to desert lizards that are probably not under severe process constraints,
aquatic turtles occupy relatively productive habitats, with primary productiv-
ity averaging 2,500 g/m 2/yr (as cited in Ricklefs 1979); however, low water
temperatures may constrain the ability of temperate-zone turtles to harvest

and process food. Evidence for this type of constraint was found in a compar-
ison of growth and body size from two populations of slider turtles (Trachemys scripta) occupying a thermally enhanced and a natural habitat in
South Carolina (Gibbons 1970). Turtles from the warmer habitats had
higher growth rates and attained larger body sizes than did those from the
natural environment. Because of the positive relationship between tempera-
ture and rate of digestion and gut clearance (Avery 1987), it may be predicted that, among turtle populations, the severity of constraint will increase
with the amount of plant material in the diet and with either latitude or
altitude. The potential effect of harvest and processing constraints on the
population dynamics of turtles may have been overlooked. Harvesting and
processing constraints may be the major factors that determine (1) the reli-
ance on stored lipids for reproduction (Congdon and Tinkle 1982) and (2)
the timing of energy allocation to, and transfers among, energy budget com-
partments of many turtles. In addition, these dual constraints may also limit
the total amount of resources consumed by turtles each year. A suggestion

that processing constraints may be influential can be seen in the following
comparison of turtle populations from South Carolina and Michigan. Annual
biomass production of the entire six species constituting a turtle community
in South Carolina averaged 9.7 kg/ha (3.9 X 10-2% of average primary productivity), and a community consisting of three turtle species in Michigan
averaged 7.3 kg/ha (2.9 X 10-2% of average primary productivity; Congdon
and Gibbons 1989).
II. Factors Influencing Energy Availability and Allocation

Basking Behavior and Thermal Constraints on Processing Rates
A number of studies have attempted to determine the functional significance
of basking by turtles (table 2; and see review by Moll and Legler [1971]).
Basking out of the water or in mats of vegetation is the primary way that most
aquatic turtles elevate their body temperature above that of the surrounding
water (Boyer 1965; Auth 1975; Standora 1982; Crawford, Spotila, and Standora 1983).
TABLE 2
Suggestedfunctions for basking behavior in turtles other than
raising body temperature

Function
Reference
Control of external environment:
Elimination of ectoparasites Cagle 1950

Eliminate epizoic algae from
carapace Neill and Allen 1954

Drying of integument to reduce
bacterial and fungal
infections Boyer 1965

Metabolic processes:
Synthesis of vitamin D
associated with calcium
metabolism Pritchard and Greenhood 1968
Enhanced digestive efficiency .. Kenyon 1925

Enhanced digestive rates Gatten 1974; Hammond,
Spotila, and Standora 1988;
Kepenis and McManus 1974;

Parmenter 1981
Reproduction:
Increased fat mobilization Whittow and Balazs 1982
Increased rate of follicle
development Congdon and Tinkle 1982;

Whittow and Balazs 1982
It has been stated that the time spent in thermoregulation (1) cannot be
used as efficiently for other behaviors such as foraging for food, (2) may
expose the animal to predators, and (3) would increase metabolic demands
(Huey and Slatkin 1976). The time spent in aerial basking certainly restricts
a turtle's ability to engage in other activities; however, basking in a vegeta-
tion mat may also provide opportunities to feed. Two studies have used the
concept of operative environmental temperatures (Te) to study basking behavior of turtles (Crawford et al. 1983; Schwarzkopf and Brooks 1985). A
general definition of Te is "the temperature of an inanimate object of zero
heat capacity with the same size, shape and radiative properties of the animal
exposed to the same microclimate" (Bakken and Gates 1975). A prediction
from cost-benefit analysis of basking behavior is that turtles will bask when
T,'s are highest so that basking time can be minimized (Crawford et al.
1983). This prediction makes the implicit assumption that time free from
basking is the factor being optimized or maximized. However, if turtles are
primarily process limited (table 1), then time spent at temperatures that
promote rather than optimize enhanced digestive efficiencies and rapid gut
clearance should be optimized (table 2). Thus, heating rapidly and returning to the water would only be the expected behavior of turtles with little
or no food in their guts (i.e., no resources need processing, so the turtle may
be expected to bask only long enough to raise its body temperature high
enough to permit efficient foraging). When water temperatures are below
that for efficient absorption of food material and rapid gut clearance, turtles
with full guts will attempt to maintain their body temperature above that
of the surrounding water regardless of whether they can reach preferred
temperatures. Thus, turtles with full guts will not wait for optimum basking
conditions but will take advantage of any opportunity to maintain body tem-
perature as close to the preferred range as possible.
The selected temperature of slider turtles (Trachemys scripta) varies

from approximately 240 C for individuals with empty guts to 29 *C when their
guts contain food (Gatten 1974). A similar temperature range was attained
by basking painted turtles in Pennsylvania (22.5*-29.0 *C; Ernst 1972) and
in Minnesota (26.3O-30.20C; Brattstrom 1965). After spring emergence,

painted turtles become active at about 8"C but do not begin feeding until
water temperatures reach approximately 150 C (Cagle 1950; Sexton 1959;

Ernst 1972). In some years, monthly means of maximum water temperatures
at approximately 1 m depth in East Marsh (ESGR) do not exceed 150 C until
May. Mean minimum temperatures in some parts of East Marsh do not exceed 15 "C during the summer (fig. 1). Mean daily water temperatures at the
bottom of East Marsh in 1987 increased from 170C in mid-May to 20'C at

the end of June. The minimum and maximum water temperatures at approx-
imately 0.5 m, recorded at Crane Pond (ESGR) between June 1 and August
31, were 130C and 29"C in 1954 and 18'C and 31 0C in 1957 (Sexton 1959).
These temperatures indicate that turtles can harvest food only during the
months of May through September. And, during the summer months at high
latitudes, they are restricted to the warmer portions of the aquatic habitat in
order to maintain their body temperatures at levels higher than the minimum necessary to harvest and process food.
Dietary Constraints on Growth

Comparing the rate of allocation of energy to growth by juvenile turtles of all
three species on the ESGR can indicate how each species views its resource
environment. The three species attain maximum adult body sizes of 0.6 kg
EAST MARSH (MI)

MEAN WATER TEMPERATURE
MAX
MIN
30
Cn 201
10
MONTHS (1981-1982)
Fig. 1. Average minimum and maximum temperatures approximately 1 m

deep in East Marsh taken every third day over 2 yr.
(Chrysemyspicta), 1.7 kg (Emydoidea blandingi), and 13 kg (Chelydra serpentina). Juveniles of all three species occupy aquatic habitats on the ESGR;
however, each species may occupy different microhabitats. Two of the spe-
cies, C. picta and E. blandingi, are omnivores; C. serpentina is primarily a

carnivore. The increase in body mass of juveniles of the omnivorous species
followed similar trajectories (50 g yr-1), whereas C. serpentina increased in

body mass approximately three times as rapidly (145 g yr-'; fig. 2). Growth
rates of these juveniles suggest either that C. serpentina harvests more food
or that the animal matter in its diet is of higher quality. The proportion of
protein in the diet of T scripta dramatically influences growth rates of juve-
niles. When fed food with 10% protein, they did not gain in body mass, and
their plastrons curled. Juveniles fed a diet with either 25% or 40% protein
grew at rates similar to those in the field (Avery 1987). Dietary protein content is probably a major factor in diet selection and dietary shift from omni-
vory toward herbivory that is associated with size or age of some emydid
turtles (Clark and Gibbons 1969; Moll and Legler 1971; Parmenter 1981;
Hart 1983).
Allocation of Energy to Reproduction in Turtles
In order to understand reproduction in turtles, it is necessary to know the
total amount of energy allocated to each clutch of eggs, the amount allocated
EMYDOIDEA CHRYSEMYS CHELYDRA

1800
1600
1400'
1200
< 1000
800
600,
400
/*
200
1 2 3 4 5 6 7 8 9 10 11 12 13 14
AGE
Fig. 2. Growth of three species of turtles on the E. S. George Reserve. Data
are from hatching to sexual maturity.
to each egg, the time over which the energy was harvested and allocated,
and the relative contributions of stored versus directly harvested energy to
each clutch.
Follicle sizes of C. picta are smallest just after the nesting season, with
substantial follicle enlargement taking place from late August through Octo-
ber (Ernst 1971a, 1971 b; Congdon and Tinkle 1982). On average, the set of
largest follicles found in females in October represented 50% of the energy
of a complete clutch of eggs that would be laid during May and June of the
following year. Energy allocated to follicle enlargement during summer and
early fall was presumably obtained directly from harvested resources, because stored lipids in females also increased during this period. The addi-
tional 50% of the energy to complete follicle enlargement to ovulatory

size was allocated between spring emergence in late March and mid-May
when nesting began (Tinkle, Congdon, and Rosen 1981; Congdon and
Tinkle 1982).
The energy allocated to follicles during spring presumably came entirely
from stored body lipids, because the decrease in lipid levels of females dur-
ing the period was almost equivalent to the increase in lipids in follicles
(Congdon and Tinkle 1982). In addition, examination of growth in C. picta
from Michigan and Pennsylvania indicated that very little or no growth, and
presumably little or no feeding activity, was taking place before June (Sex-
ton 1959; Ernst 1971c). At high latitudes, the temporal patterns of energy
acquisition and allocation to growth and reproduction, coupled with the

need to lay eggs early enough to allow adequate time for embryonic development, may be more limiting in some years than is absolute availability of
energy. A similar pattern of follicle development during late summer has

been observed in Sternotherus odoratus in Alabama, where follicles were
fully developed (ovulatory size) between August and December, and ovulation of the first clutch occurred during late April of the following year (Mc-
Pherson and Marion 1982).

The minimum interval between the first and second clutches of C. picta
in Michigan and T. scripta in South Carolina is approximately 12 d (J. W.
Gibbons, unpublished data). This short interval indicates that (1) ovulation
of a subsequent clutch of eggs can occur shortly after a clutch has been
placed in a nest; (2) the follicles for the second clutch develop at the same
time as those for the first clutch and, if necessary, complete vitellogenesis
during the time the eggs for the first clutch are in the oviducts; and (3) the
time between depositions of subsequent clutches is too short to allow a

major portion of the energy for the second clutch to come from resources
harvested during the interval.
III. Energy Allocation and Life-History Theories

In preparation for reproduction, a female must make three major "determinations": (1) the total amount of energy available for present reproduction,
(2) the quantity of energy to be allocated to each offspring, and (3) the
number of individuals that can be produced by the present level of investment in each offspring. The three determinations fall roughly into the con-
ceptual categories of reproductive effort, parental investment, and optimal

egg size.
Reproductive Allocation: Theories and Morphological Constraint

Some life-history theories deal with how an organism should apportion its
finite resources among the competing compartments of maintenance,

growth, storage, and reproduction. Central to these theories is the concept
of reproductive effort, that portion of an animal's resource budget that is
allocated to reproduction (Fisher 1930; Hirshfield and Tinkle 1975). However, a number of proximate constraints may affect both the total amount of
energy allocated to reproduction and the amount allocated to each individual offspring of turtles.
All of the energy allocated to each individual turtle hatchling is contained
within the egg. However, it has been argued that the eggs of turtles and
other reptiles should be viewed as two distinct components in which energy
is allocated by the female for (1) embryogenesis and (2) extended parental
care in the form of yolk reserves that remain in the hatchling after it leaves
the egg (Kraemer and Bennett 1981; Congdon and Tinkle 1982; Congdon,
Tinkle, and Rosen 1983a; Congdon, Gibbons, and Greene 1983b; Troyer
1983; Wilhoft 1986; Congdon and Gibbons 1987). Considering turtle eggs
as a two-component system points out how the concepts of parental invest-
ment and optimal egg size are tightly coupled in reptiles when compared
to mammals or birds that provide extended parental care such as guarding
and feeding of young.
Trivers (1972) defined parental investment as "any investment by the parent in an individual offspring that increases the offspring's chance of surviv-
ing (and hence reproductive success) at the cost of the parent's ability to
invest in other offspring." Under Trivers's definition, both categories of in-
vestment, that used for embryogenesis and that used for fueling the developed hatchling, fall under the overall category of PI. This definition is ade-
quate only where it is assumed that all of the PI is used to make a larger
offspring (salamanders [Nussbaum 1987]; insects [Parker and Begon 1986])
rather than to provide it with posthatching reserves. By lumping together
both categories of investment in an egg, Trivers's definition obscures impor-
tant ecological and evolutionary questions about distinct processes that pro-
ceed in different ways and at different times toward the common goal of
making a successful offspring.
Parental investment in reptiles should be separated into energy invested

in making a complete embryo (PIE), and energy invested by the female for
parental care (PIC)-that is, energy in excess of that needed to produce a

complete hatchling. This excess may be in the form of a yolk sac or of hatchling fat bodies that are both used by the hatchling after it leaves the egg. The
separation of energy allocated to each egg is based on the assumption that

some of the energy allocated to an egg by the female is done expressly to
fuel the hatchling. Since data on turtles and other reptiles indicate that the
lipids or energy left in the hatchling yolk sac when it leaves the egg or is
born usually exceeds 50% of the original lipids in the egg, this investment
is far from trivial (Kraemer and Bennett 1981; Congdon and Tinkle 1982;
Congdon et al. 1983a, 1983b; Troyer 1983; Stewart and Castillo 1984; Wil-
hoft 1986; Congdon and Gibbons 1987). This assumption could be shown
to be incorrect by demonstrating that hatchlings incubated under optimal
conditions hatch with no residual yolk sac or formed fat bodies. In this case
all of the material in the egg would be in the form of hatchling tissues or
waste products. Since all of the PIC must be added to the contents of the
egg, it must, by definition, increase the size of the egg, but it appears to
influence hatchling quality in ways not directly related to hatchling size.
Interactions between determinants of size or quality of offspring and off-
spring numbers have been considered for some time (Darwin 1859). More
recent considerations have centered on the idea that organisms should invest in offspring at the level that maximizes the fitness of the parents (Lack
1948, 1954, 1968; Svardson 1949; Williams 1966; Nussbaum 1985, 1987).
There are currently two major categories of evolutionary theories (i.e., opti-
mality or canalization theories and developmental plasticity theories) that

attempt to explain the range of variation in egg size either within or among
females. Morphological constraint on egg size has also been offered to ex-
plain some of the variation in egg size of turtles (Congdon and Gibbons 1987).
Optimal egg-size (OES) models (Williams 1966; Smith and Fretwell 1974;
Brockelman 1975; Parker and Begon 1986) attempt to model the relationships and interactions between egg size and number. The models make the
following assumptions: (1) parents have a limited amount of resources or
energy available for a given reproductive bout; (2) a minimum amount of
energy is required to produce a viable offspring; and (3) the fitness of offspring is not linearly related to the amount of parental investment, that is,
there is a level at which a given investment in offspring results in large gains
followed by a level of investment where minimal or no increase in the fitness
of offspring occurs (also see Pianka 1974; Schaffer and Gadgil 1975). If assumption (1) is true, it follows that, as the amount of energy invested in
individual offspring goes up, the number of individuals produced must be
reduced. However, if some factor other than absolute energy availability lim-
its allocation to reproduction (e.g., time constraints or morphological constraints such as volume of a turtle's body cavity, size of the pelvic opening,
or parental investment that does not primarily influence the size of the
hatchling), then results inconsistent with predictions from OES models can
be obtained.
A major prediction from OES theory is that, within a population, the

amount of variation in reproductive output among females should result pri-
marily from variation in the number of offspring produced and secondarily

from variation in egg size. One problem is that the actual level of variation
in reproductive output owing to variation in egg size that is acceptable under
OES models has not been defined in either relative or absolute terms. A
second problem is that the relationships among egg size, hatchling size,
and hatchling quality have not been established. The above discussion of
parental investment in egg material points out that egg size may be related
to hatchling quality through care rather than exclusively in hatchling size.

Therefore, OES models might be better termed optimal offspring-quality

models.
In contrast to OES theorists, other investigators have proposed that natural
selection should favor developmental plasticity that results in a range of

reproductive characteristics under conditions in which environmental vari-
ability is unpredictable (Robertson 1971; Capinera 1979; Kaplan 1980; Cooper and Kaplan 1982; Caswell 1983; Kaplan and Cooper 1984). Within these
models, variation in egg size should occur within a single reproductive bout
or among reproductive bouts within a single year (Kaplan and Cooper

1984). It might be expected that there are life-history traits and environmen-
tal conditions that could result in either strategy, and the existence supporting data for one theory should not be considered as refuting the other.
A study of three species of emydid turtles (Chrysemyspicta, Deirochelys

reticularia, and Trachemys scripta) found that pelvic constraint on egg size
among the species appeared to be related to body size (Congdon and Gib-
bons 1987). In two smaller-bodied species (C. picta and D. reticularia),

egg size increased from the smallest to the largest gravid females, and the
slopes of the lines relating egg size and pelvic opening width to body size
were essentially equal. In contrast, eggs of female T scripta only slightly
increased with body size compared to the other two species, and the slope
of the line relating pelvic width to body size was five times steeper than was
the line for egg width. The constraint on egg size due to pelvic opening size
in C. picta and D. reticularia apparently resulted in a situation that is not in
accord with that predicted by OES; i.e., substantially more of the variation
in reproductive output was due to variation in egg size than was found in T
scripta, where pelvic constraint did not exist. Thus, the additional factor of
morphological constraint apparently limits the way reproductive investments can be partitioned in some turtles, and the degree of limitation is
greater in smaller-bodied species.
The preceding discussions have attempted to identify some obvious, and
some less than obvious, ways that energy acquisition, processing, and allocation by reptiles can be influenced by extrinsic and intrinsic factors. Identification of the way these factors limit the total resources available to or-
ganisms and determine the timing of energy allocation is necessary for

interpreting energy budgets and exploring the ways that energetics interacts
with life-history and population processes.
Acknowledgments
This paper is dedicated to Richard M. Wiltse, foreman of the University of
Michigan's E. S. George Reserve maintenance crew, who died in May 1988.

He was a friend and an enthusiastic supporter of the long-term turtle research program on the George Reserve. Earlier drafts of this manuscript
were improved by comments from Roger Anderson, William Cooper, Gary
Hepp, Gary Meffe, J. Whitfield Gibbons, David Scott, and Laurie J. Vitt. Fund-
ing for this study was provided by NSF grants DEB-79-06301 and BSR-8400861 and contract DE-AC09-76SR00-819 between the University of Georgia
and the United States Department of Energy.
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Division of Comparative Physiology and Biochemistry, Society for Integrative and

Division of Comparative Physiology and Biochemistry, Society for Integrative and

Proximate and Evolutionary Constraints on Energy

Savannah River Ecology Laboratory, Drawer E, Aiken, South Carolina 29802

(3)process rate limitations; and (4) limitation on harvest orprocessing resources

organism combine to make the mere presentation of total energy budgets,

tions of average energy allocations for all individuals or for individuals of

Physiological Zoology 62(2):356-373. 1989. @ 1989 by The University of Chicago.

Constraints on Energetics of Reptiles 357

an individual's allocation of net assimilated energy to the competing com-

partments of maintenance, growth, reproduction, and storage (Wiegert

on the University of Michigan's E. S. George Reserve (ESGR) in Livingston

I. Major Categories of Constraints on Resource Availability

ual is finite. The maximum resources that can be harvested by individuals

and allocation that may be imposed daily or seasonally or by competing

358 Justin D. Congdon

Possible causes of limitation on energy acquisition and

Absolute resource availability Deserts

Process rate High latitude or altitude

duction averages 14-43 g dry mass/m2. In contrast, most of the Sonoran

(Turner 1973, 1974; Dunham 1981).

Constraints on Energetics of Reptiles 359

(Nagy, Shoemaker, and Costa 1976). Unlike herbivores, both insectivorous

Limitations on Harvest Rate

Linked to absolute resource limitation in the desert are a set of constraints

on the rate of harvesting resources (table 1). These constraints can be as

ard (Sceloporus merriami) in the Big Bend National Monument in west

poor environment for food acquisition. However, it would be interesting

Competing demands on restricted activity times can also have a dramatic

(Congdon 1977). Large males of the wide-foraging lizard Cnemidophorus

360 Justin D. Congdon

Process Rate Limitation

temperatures may constrain the ability of temperate-zone turtles to harvest

the total amount of resources consumed by turtles each year. A suggestion

II. Factors Influencing Energy Availability and Allocation

Constraints on Energetics of Reptiles 361

Suggestedfunctions for basking behavior in turtles other than

raising body temperature

Control of external environment:

Elimination of ectoparasites Cagle 1950

carapace Neill and Allen 1954

bacterial and fungal

infections Boyer 1965

metabolism Pritchard and Greenhood 1968

Enhanced digestive efficiency .. Kenyon 1925

Kepenis and McManus 1974;

development Congdon and Tinkle 1982;

362 Justin D. Congdon

perature as close to the preferred range as possible.

The selected temperature of slider turtles (Trachemys scripta) varies

in Minnesota (26.3O-30.20C; Brattstrom 1965). After spring emergence,

water temperatures reach approximately 150 C (Cagle 1950; Sexton 1959;

at approximately 1 m depth in East Marsh (ESGR) do not exceed 150 C until

bottom of East Marsh in 1987 increased from 170C in mid-May to 20'C at

Dietary Constraints on Growth

Constraints on Energetics of Reptiles 363

EAST MARSH (MI)

Fig. 1. Average minimum and maximum temperatures approximately 1 m

cies, C. picta and E. blandingi, are omnivores; C. serpentina is primarily a

followed similar trajectories (50 g yr-1), whereas C. serpentina increased in

364 Justin D. Congdon

EMYDOIDEA CHRYSEMYS CHELYDRA