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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. 356-373Published by: The University of Chicago Press. Sponsored by the Division of Comparative

Physiology and Biochemistry, Society for Integrative and Comparative Biology

Stable URL: http://www.jstor.org/stable/30156175

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3 5 6

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 re-

sources 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 invest-

ment 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 hatch-

ling 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 demograph-

ics. These interactions presumably determine the association of an organ-

ism'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


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Constraints on Energetics of Reptiles 357

1976; Congdon, Dunham, and Tinkle 1982; Nagy 1982). As such, the resolu-

tion needed to distinguish among various sequential decision-making pro-

cesses that lead to energy budget phenotypes is, at best, only partially at-

tained.

The purpose of this article is to review some concepts related to construc-

tion 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 fac-

tors 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 predic-

tions 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 im-

posed during foraging, handling, or processing of resources. Temporal con-

straints 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 rep-

tiles 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 in-


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358 Justin D. Congdon

TABLE 1

Possible causes of limitation on energy acquisition and

processing of reptiles

Lmtations 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 primar-

ily 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, cer-

tainly 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 herbiv-

orous 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


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(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 Cong-

don 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 con-

straints 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, dis-

playing from prominent sites (Ruby 1981; Ruby and Dunham 1984), or ac-

tively 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).


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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 con-

trast 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 (Tra-

chemys 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 pre-

dicted 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 pro-

ductivity), 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 Stan-

dora 1983).


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TABLE 2

Suggestedfunctions for basking behavior in turtles other than

raising body temperature

unctonRference

Control of external environment:

Elimination of ectoparasites Cagle 1950

Eliminate epizoic algae from

carapace Neill and Alen 954

Drying of integument to reduce

bacterial and fungal

infections Boyer 965

Metabolic processes:

Synthesis of vitamin D

associated with calcium

metabolismPritchard and Greenhood 968

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 be-

havior 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


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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 return-

ing 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 ex-

ceed 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 mini-

mum 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


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EAST MARSH (MI)

MEAN WATER TEMPERATURE

M XMN

30

Cn 201

w

67891

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 ser-

pentina). 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 con-

tent 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


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EMYDOIDEA CHRYSEMYS CHELYDRA

1800

1600

1400

1200

< 1000

800

6 0 0

400 /

200

1 2 3 4 5 6 7 8 9 10 11 12 13 14

A GE

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, be-

cause 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


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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 devel-

opment, 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 ovula-

tion 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 determi-

nations : (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 invest-

ment 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). How-

ever, a number of proximate constraints may affect both the total amount of

energy allocated to reproduction and the amount allocated to each individ-

ual offspring of turtles.


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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 par-

ent 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 devel-

oped 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 hatch-

ling 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


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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 in-

vest 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 Gib-

bons 1987).

Optimal egg-size (OES) models (Williams 1966; Smith and Fretwell 1974;

Brockelman 1975; Parker and Begon 1986) attempt to model the relation-

ships 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 off-

spring 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 as-

sumption (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 con-

straints 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.


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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; Coo-

per 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 support-

ing 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 invest-

ments 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 allo-

cation by reptiles can be influenced by extrinsic and intrinsic factors. Iden-

tification 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.


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He was a friend and an enthusiastic supporter of the long-term turtle re-

search 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-84-

00861 and contract DE-AC09-76SR00-819 between the University of Georgia

and the United States Department of Energy.

Literature Cited

ANDERSON, R. A. 1986. Foraging behavior, energetics of reproduction and sexual se-

lection in a widely foraging lizard, Cnemidophorus tigris. Ph.D. diss. University of

California, Los Angeles.

ANDERSON, R. A., and W. H. KARASOV. 1988. Energetics of the lizard Cnemidophorus

tigris and life history consequences of food-acquisition mode. Ecol. Monogr. 58:

79-110.

AUTH, D. L. 1975. Behavioral ecology of basking in the yellow-bellied turtle, Chry-

semys scripta scripta (Schoepff). Bull. Florida State Mus. Biol. Sci. 20:1-45.

AVERY, H. W. 1987. Roles of diet protein and temperature in the nutritional energetics

of juvenile slider turtles, Trachemys scripta. M.S. thesis. State University College

at Buffalo, Buffalo, N.Y.

AVERY, R. A. 1975. Clutch size and reproductive effort in the lizard Lacerta vivipara

Jacquin. Oecologia (Berl.) 19:165-170.

BAKKEN, G. S., and D. M. GATES. 1975. Heat transfer analysis of animals: some implica-

tions for field ecology, physiology, and evolution. Pages 255-290 in D. M. GATES

and R. B. SCHMERL, eds. Perspectives of biophysical ecology. Springer-Verlag, New

York.

BALLINGER, R. E., and J. D. CONGDON. 1980. Food resource limitation of body growth

rates in Sceloporus scalaris (Sauria, Iguanidae). Copeia 1980:921-923.

BOYER, D. R. 1965. Ecology of the basking habit of turtles. Ecology 46:99-118.

BRATTSTROM, B. H. 1965. Body temperatures of reptiles. Am. Midl. Nat. 73:376-422.

BROCKELMAN, W. Y. 1975. Competition, the fitness of offspring, and optimal clutch

size. Am. Nat. 109:677-699.

CAGLE, F. R. 1950. The life history of the slider turtle, Pseudemys scripta troostii

(Holbrook). Ecol. Monogr. 20:31-54.

CAPINERA, J. L. 1979. Qualitative variation in plants and insects: effect of propagule

size on ecological plasticity. Am. Nat. 114:350-361.

CASWELL, H. 1983. Phenotypic plasticity in life-history traits: demographic effects and

evolutionary consequences. Am. Zool. 23:35-46.

CLARK, D. B., and J. W. GIBBONS. 1969. Dietary shift in the turtle Pseudemys scripta

(Schoepff) from youth to maturity. Copeia 1969:704-706.

CONGDON, J. D. 1977. Energetics of the montane lizard Sceloporusjarrovi: a mea-

surement of reproductive effort. Ph.D. diss. Arizona State University, Tempe.

CONGDON, J. D., A. E. DUNHAM, and D. W. TINKLE. 1982. Energy budgets and life

histories of reptiles. Pages 233-271 in C. GANS, ed. Biology of the Reptilia. Vol.

13. Academic Press, New York.


8/18/2019 30156175

16/19


CONGDON, J. D., and J. W. GIBBONs. 1987. Morphological constraint on egg size: a

challenge to optimal egg size theory? Proc. Natl. Acad. Sci. USA 84:4145-4147.

. 1989. Biomass productivity of turtles in freshwater wetlands: a geographic

comparison. Savannah River Ecology Laboratory Symposium. Freshwater Wetlands

(in press).

CONGDON, J. D., J. W. GIBBONS, and J. L. GREENE. 1983b. Parental investment in the

chicken turtle (Deirochelys reticularia). Ecology 64:419-425.

CONGDON, J. D., and D. W. TINKLE. 1982. Reproductive energetics of the painted

turtle (Chrysemyspicta). Herpetologica 38:228-237.

CONGDON, J. D., D. W. TINKLE, and P. C. ROSEN. 1983a. Egg components and utiliza-

tion during development in aquatic turtles. Copeia 1983:264-268.

COOPER, W. S., and R. H. KAPLAN. 1982. Adaptive coin-flipping : a decision-theoretic

examination of natural selection for random individual variation. J. Theor. Biol.

94:135-151.

CRAWFORD, K. M., J. R. SPOTILA, and E. A. STANDORA. 1983. Operative environmental

temperatures and basking behavior of the turtle Pseudemys scripta. Ecology 64:

989-999.

CUNNINGHAM, G. L., J. P. SYVERTSEN, J. F. REYNOLDS, and J. M. WILLSON. 1979. Some

effects of soil-moisture availability on above-ground production and reproductive

allocation in Larrea tridentata (DC) Cov. Oecologia (Berl.) 40:113-123.

DARWIN, C. R. 1859. On the origin of species by means of natural selection; or, the

preservation of favoured traces in the struggle for life. Murray, London.

DUNHAM, A. E. 1978. Food availability as a proximate factor influencing individual

growth rates in the iguanid lizard Sceloporus merriami. Ecology 59:770-778.

1981. Populations in a fluctuating environment: the comparative population

ecology of the iguanid lizards Sceloporus merriami and Urosaurus ornatus. Misc.

Pub. Mus. Zool., Univ. Mich. 158:1-62.

ERNST, C. H. 1971a. Population dynamics and activity cycles of C. picta in SE Penn.

J. Herpetol. 5:151-160.

1971b. Sexual cycles and maturity of the turtle Chrysemyspicta. Biol. Bull.

140:191-200.

1971 c. Growth of the painted turtle, Chrysemyspicta, in SE Penn.J. Herpetol.

5:151-160.

1972. Temperature-activity relationship in the painted turtle, Chrysemys

picta. Copeia 1972:217-222.

EVANARI, M., E. D. SHULTZ, O. L. LANGE, L. KAPPEN, and U. BUSCHBOM. 1976. Plant

production in arid and semi-arid areas. Pages 439-451 in O. L. LANGE, L. KAPPEN,

and E. D. SHULZE, eds. Ecological studies: analysis and synthesis. Vol. 19. Springer-

Verlag, New York.

FISHER, R. A. 1930. The genetical theory of natural selection. Clarendon, Oxford.

GATTEN, R. E. 1974. Effect of nutritional status on the preferred body temperature of

the turtles Pseudemys scripta and Terrapene ornata. Copeia 1974:912-917.

GIBBONS, J. W. 1970. The influence of terrestrial activities on the population dynam-

ics of aquatic turtles. Am. Midl. Nat. 83:404-415.

GRANT, B. W., and A. E. DUNHAM. 1987. Thermally imposed time constraints on the

activity of the desert lizard Sceloporus merriami. Ecology 69:167-176.

HADLEY, N. F., and S. R. SZAREK. 1981. Productivity of desert ecosystems. Biol. Sci.

31:747-753.

HAMMOND, K. A., J. R. SPOTILA, and E. A. STANDORA. 1988. Basking behavior of the


8/18/2019 30156175

17/19


turtle Pseudemys scripta: effects of digestive state, acclimation temperature, sex,

and season. Physiol. Zool. 61:69-77.

HART, D. R. 1983. Dietary and habitat shift with size of red-eared turtles (Pseudemys

scripta) in a southern Louisiana population. Herpetologica 39:285-290.

HIRSHFIELD, M. F., and D. W. TINKLE. 1975. Natural selection and the evolution of

reproductive effort. Proc. Natl. Acad. Sci. USA 72:2227-2231.

HUEY, R. B., and M. SLATKIN. 1976. Costs and benefits of lizard thermoregulation. Q.

Rev. Biol. 51:363-384.

KAPLAN, R. H. 1980. The implication of ovum size variability for offspring fitness and

clutch size in several populations of salamanders (Ambystoma). Evolution 34:51-

6 4 .

KAPLAN, R. H., and W. S. COOPER. 1984. The evolution of developmental plasticity

in the reproductive characteristics: an application of the adaptive coin-flipping

principle. Am. Nat. 123:393-410.

KARASOV, W. H., and R. A. ANDERSON. 1984. Interhabitat differences in energy acquisi-

tion and expenditure in a lizard. Ecology 65:235-247.

KENYON, W. A. 1925. Digestive enzymes in poikilothermal vertebrates: an investiga-

tion of enzymes in fishes with comparative studies of those of amphibians, reptiles

and mammals. U.S. Natl. Mar. Fisheries Ser. Bull. 41:197-200.

KEPENIS, V., and J. J. MCMANUS. 1974. Bioenergetics of young painted turtles, Chry-

semyspicta. Comp. Biochem. Physiol. 48:309-317.

KRAEMER, J. E., and S. H. BENNETT. 1981. Utilization of post-hatching yolk in logger-

head sea turtles, Caretta caretta. Copeia 1981:406-411.

LACK, D. 1948. The significance of clutch size. Ibis 89:302-352; 90:25-45.

--. 1954. The natural regulation of animal numbers. Clarendon, Oxford.

--. 1968. Ecological adaptations for breeding in birds. Methem, London.

LIGHTFOOT, D. C., and W. G. WHITFORD. 1987. Variation in insect densities on creo-

sotebush: is nitrogen a factor? Ecology 68:547-557.

MCPHERSON, R. J., and K. R. MARION. 1982. Seasonal changes of total lipids in the

turtle Sternotherus odoratus. Comp. Biochem. Physiol. 71A:93-98.

MOLL, E. 0., and J. M. LEGLER. 1971. The life history of a neotropical pond slider

turtle, Pseudemys scripta (Schoepff), in Panama. Bull. Los Angeles County Mus.

Nat. Hist. Sci. 11:1-102.

NAGY, K. A. 1982. Ecological energetics of a lizard. Pages 24-54 in R. HUEY, T.

SCHOENER, and E. PIANKA, eds. Lizard ecology: studies of a model organism. Har-

vard University Press, Cambridge.

NAGY, K. A., and P. A. MEDICA. 1986. Physiological ecology of desert tortoises in

southern Nevada. Herpetologica 42:73-92.

NAGY, K. A., and V. H. SHOEMAKER. 1975. Energy and nitrogen budgets of the free-

living desert lizard Sauromalus obesus. Physiol. Zool. 48:252-262.

NAGY, K. A., V. H. SHOEMAKER, and W. R. COSTA. 1976. Water, electrolyte, and nitrogen

budgets of jackrabbits (Lepus californicus) in the Mojave Desert. Physiol. Zool.

49:351-363.

NEILL, W. T., and E. R. ALLEN. 1954. Algae on turtles: some additional considerations.

Ecology 35:581-584.

NoY-MEIR, I. 1973. Desert ecosystems: environment and producers. Annu. Rev. Ecol.

Syst. 4:25-51.

. 1974. Desert ecosystems: higher trophic levels. Annu. Rev. Ecol. Syst. 5:195-

214.


8/18/2019 30156175

18/19


NUSSBAUM, R. A. 1985. The evolution of parental care in salamanders. Misc. Publ.

Mus. Zool. Univ. Mich. 169:1-50.

. 1987. Parental care and egg size in salamanders: an examination of the safe

harbor hypothesis. Res. Pop. Ecol. 29:27-44.

PARKER, G. A., and M. BEGON. 1986. Optimal egg size and clutch size: effects on

environment and maternal phenotype. Am. Nat. 128:573-592.

PARMENTER, R. P. 1981. Digestive turnover rates in freshwater turtles: the influence

of temperature and body size. Comp. Biochem. Physiol. 70:235-238.

PIANKA, E. R. 1974. Evolutionary ecology. Harper & Row, New York.

PRITCHARD, P. C. H., and W. F. GREENHOOD. 1968. The sun and the turtle. Int. Turtle

Tortoise Soc. J. 2:20-25.

RICKLEFS, R. E. 1979. Ecology. 2d ed. Chiron, New York.

ROBERTSON, R. 1971. Lepidoptera genetics. Pergamon, Oxford.

RUBY, D. E. 1981. Phenotypic correlates of male reproductive success in the lizard

Sceloporusjarrovi. Pages 96-107 in R. D. ALEXANDER and D. W. TINKLE, eds. Natu-

ral selection and social behavior. Chiron, New York.

RUBY, D. E., and A. E. DUNHAM. 1984. A population analysis of the ovoviviparous

lizard Sceloporusjarrovi in the Pinaleno Mountains of southeastern Arizona. Her-

petologica 40:425-436.

SCHAFFER, W. M., and M. D. GADGIL. 1975. Selection for optimal life histories in

plants. Pages 142-157 in M. L. CODY and J. M. DIAMOND, eds. Ecology and evolu-

tion of communities. Belknap, Cambridge, Mass.

SCHWARZKOPF, L., and R. J. BROOKS. 1985. Application of operative environmental

temperatures to analysis of basking behavior in Chrysemys picta. Herpetologica

41:206-212.

SEXTON, O. J. 1959. Spatial and temporal movements of a population of the painted

turtle, Chrysemyspicta marginata (Agassiz). Ecol. Monogr. 29:113-140.

SHREVE, F. 1925. Ecological aspects of the deserts of California. Ecology 6:93-103.

- . 1942. The vegetation of Arizona. In T. H. KEARNEY and R. H. PEEBLES, eds.

Flowering plants and ferns of Arizona. U.S. Dept. Agric. Misc. Publ.

SMITH, C. C., and S. D. FRETWELL. 1974. The optimal balance between size and num-

ber of offspring. Am. Nat. 108:499-506.

STANDORA, E. A. 1982. A telemetric study of the thermoregulatory behavior and cli-

mate-space of free-ranging yellow-bellied turtles, Pseudemys scripta. Ph.D. diss.

University of Georgia.

STEWART, J. R., and R. E. CASTILLO. 1984. Nutritional provision of the yolk of two

species of viviparous reptiles. Physiol. Zool. 57:377-383.

SVARDSON, G. 1949. Natural selection and egg number in fish. Rep. Inst. Freshwater

Res. Drottningholm 29:115-122.

SZAREK, S. R. 1979. Primary production in four North American deserts: indices of

efficiency. J. Arid Environ. 2:187-209.

TINKLE, D. W.,J. D. CONGDON, and P. R. ROSEN. 1981. Nesting frequency and success:

implications for the demography of painted turtles. Ecology 62:1426-1432.

TRIVERS, R. L. 1972. Parental investment and sexual selection. Pages 136-179 in

B. G. CAMBELL, ed. Sexual selection and descent of Man. Aldine, Chicago.

TROYER, K. 1983. Posthatchling yolk energy in a lizard: utilization pattern and inter-

clutch variation. Oecologica 58:340-344.

TURNER, F. B. 1973. Rock Valley Validation Site Report. US/IBP Desert Biome Re-

search Memorandum. 73-2. Utah State University, Logan.


8/18/2019 30156175

19/19


1974. Rock Valley Validation Site Report. US/IBP Desert Biome Research

Memorandum. 73-3. Utah State University, Logan.

TURNER, F. B., P. A. MEDICA, and B. W. KOWALEWSKY. 1976. Energy utilization by a

desert lizard (Uta stansburiana). US/IBP Desert Biome Monogr. no. 1. Utah State

University Press, Logan.

WEBB, W., S. SZAREK, W. LAUENROTH, R. KINERSON, and M. SMITH. 1978. Primary pro-

ductivity and water use in native forests, grasslands, and desert ecosystems. Ecol-

ogy 59:1239-1247.

WHITTOW, G. C., and G. H. BALAZS. 1982. Basking behavior of the Hawaiian green

turtle (Chelonia mydas). Pac. Sci. 36:129-139.

WIEGERT, R. G. 1968. Thermodynamic consideration in animal nutrition. Am. Zool.

8:71-81.

WILBUR, H. M., D. W. TINKLE, and J. P. COLLINS. 1974. Environmental certainty, tro-

phic level, and resource availability in life history evolution. Am. Nat. 108:805-

817.

WILHOFT, D. C. 1986. Eggs and hatchling components of the snapping turtle Chely-

dra serpentina. Comp. Biochem. Physiol. 84A:483-486.

WILLIAMS, G. C. 1966. Adaptation and natural selection. Princeton University Press,

Princeton, N.J. 307 pp.

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