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
Published 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
Accessed: 09-04-2016 04:08 UTC
Linked references are available on JSTOR for this article:
You may need to log in to JSTOR to access the linked references.
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted
digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about
JSTOR, please contact support@jstor.org.

Division of Comparative Physiology and Biochemistry, Society for Integrative and
Comparative Biology, The University of Chicago Press are collaborating with JSTOR to digitize,
preserve and extend access to Physiological Zoology

This content downloaded from on Sat, 09 Apr 2016 04:08:26 UTC
All use subject to http://about.jstor.org/terms

of limited value. Because reptile eggs contain all of the chemical energy available to developing embryos. and (4) limitation on harvest orprocessing resources imposed by risk ofpredation. behavior. Introduction A number of evolutionary theories are based on assumed interactions among resource availability. 0031-935X/89/6202-8831$02. 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. occur. Aiken. Tinkle. @ 1989 by The University of Chicago. (2) harvest rate limitations. by definition. (3)process rate limitations. morphology. with regard to many reptiles. interactions between the level ofparental investment in each offspring and egg size must. These interactions presumably determine the association of an organism's life-history traits and energy budgets. optimal egg-size models would be more aptly considered to be optimal offspring-quality models. Turner. Medica. the argument that sim- ilar life-history phenotypes can result from very different selective forces (Wilbur. in the absence of an ecological and evolutionary context. Interactions among trophic level. Drawer E. However. All rights reserved.230. and Collins 1974) seems well founded and can certainly be extended to energy-allocation phenotypes as well. At present. demographic environment. and age-specific demographics.235. Congdon Savannah River Ecology Laboratory. and Kowalewsky Physiological Zoology 62(2):356-373.jstor. morphology. 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. 09 Apr 2016 04:08:26 UTC All use subject to http://about. 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 1975.356 Proximate and Evolutionary Constraints on Energy Relations of Reptiles Justin D. 1989.179 on Sat.org/terms . and phylogeny of an organism combine to make the mere presentation of total energy budgets. 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.00 This content downloaded from 177. Therefore.

Low primary productivity of desert habitats is primarily caused by low wa- ter availability (Noy-Meir 1973. 1978. S. Michigan. 09 Apr 2016 04:08:26 UTC All use subject to http://about. Nagy 1982). the resolution needed to distinguish among various sequential decision-making processes that lead to energy budget phenotypes is. handling. 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). George Reserve (ESGR) in Livingston County. and Tinkle 1982. frequency. Anderson and Karasov 1988). Major Categories of Constraints on Resource Availability Interpretations of ecological energy budgets and most. 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. Dunham. Congdon et al. I. 1974. Congdon. only partially attained. 1982. or processing of resources. and storage (Wiegert 1968. Hadley and Szarek 1981) that indirectly limits secondary production (Dunham 1981). at best. and (3) review life-history theories concerning predictions about energy-allocation decisions of reptiles. life-history theories are based on the assumption that the energy available to an individ- ual is finite.org/terms . 1979.Constraints on Energetics of Reptiles 357 1976. 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. To ac- complish this goal.235. growth. Cunningham et al.179 on Sat. and inThis content downloaded from 177. 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. Nagy 1982. Of secondary influence are the timing. I shall (1) discuss some broad categories of resource constraint on energy acquisition and allocation of desert lizards and temper- ate-zone turtles. The maximum resources that can be harvested by individuals may be set by absolute quantity of resources available or by constraints imposed during foraging. The response of the animal to different types of energy-acquisition constraints may be the same in different habitats or different in similar habitats. reproduction.230.jstor. if not all. Webb et al. (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. As such.

whether herbivorous. The intensity and frequency of these fluctuations can be expected to have major effects on the timing of energy storage and allocation. the chuckwalla (Sauromalus obesus. Hadley and Szarek 1981). but this cannot be processed while there are no alternative sources of water.200 m elevation. and rainfall there averages under 12 cm and occurs almost equally during winter and summer (Shreve 1942).230. both herbivorous reptiles. certainly face resource limitation that fluctuates seasonally and sporadically.179 on Sat. Nagy and Medica 1986). in the Mojave Desert. Dunham 1981). Annual net primary pro- duction averages 14-43 g dry mass/m2.5 cm per year and occurs primarily during the relatively cold winter (Shreve 1925). may have energy available in the form of dried plant material. soil type. 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. 1976. 1979. Cunningham et al. precipitation seldom exceeds 12. Congdon TABLE 1 Possible causes of limitation on energy acquisition and processing of reptiles Limitations Location Absolute resource availability Deserts Harvest rate Deserts.org/terms .jstor. Precipitation has been shown to be tightly linked to resource availability in desert habitats (Turner 1973. or carnivorous. and nitrogen availability (Lightfoot and Whitford 1987) and their relative effects on annual and perennial plants (Evanari et al. For example. Annual net primary production averages 92-129 g dry mass/m2. high latitude. Szarek 1979. 1974. insectivorous. For example. most of the Sonoran Desert is below 600 m elevation. Nagy and Shoemaker 1975) and the desert tortoise (Scaptochelys agassizii. 09 Apr 2016 04:08:26 UTC All use subject to http://about. In contrast. Desert reptiles. A similar condition has also been shown in jackrabbits in the Mojave Desert This content downloaded from 177. 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.235.358 Justin D. which averages approximately 1.

The restricted daily activity period. coupled with the low productivity of desert habitat. displaying from prominent sites (Ruby 1981. 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). Anderson and Karasov 1988). Despite the apparent severity of time constraints on activity. During the breeding season. This content downloaded from 177. and Costa 1976). whereas females have a positive energy balance during vitellogenesis (Anderson and Karasov 1988).235. However. both insectivorous and carnivorous reptiles obtain preformed water in food. Grant and Dunham 1987. Competing demands on restricted activity times can also have a dramatic effect on the short-term energy balance of animals.jstor.179 on Sat. or actively searching for females (Anderson 1986. These constraints can be as obvious as the restrictions placed on activity over a relatively long period by seasonally high or low temperatures. would seem to place the lizard in a very poor environment for food acquisition. Ballinger and Congdon 1980). so reduced rainfall acts primarily to reduce prey abundance rather than quality. In some habitats and situations. 09 Apr 2016 04:08:26 UTC All use subject to http://about. Ruby and Dunham 1984). During summer. 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). In contrast. Shoemaker. and are in a negative energy balance. Unlike herbivores. some male lizards spend much of their time defending boundaries of territories. the thermal environment restricted daily activity to approximately a 2-h period in the morning and a brief period in late afternoon. Two studies have documented reduced growth rates in insectivorous lizards that were associated with low food resources (Dunham 1978. 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.Constraints on Energetics of Reptiles 359 (Nagy. the lizard has an average preferred body temperature lower than that of any other North American iguanid lizard studied (Grant and Dunham 1987).org/terms . For example. male Sceloporusjarrovi are active most of the day every day. 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).230. similar constraints can also occur on a daily basis (Karasov and Anderson 1984. Anderson and Karasov 1988). 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. lose body mass rapidly.

9 X 10-2% of average primary productivity. Standora 1982.7 kg/ha (3.235. however.org/terms . Crawford. Annual biomass production of the entire six species constituting a turtle community in South Carolina averaged 9.500 g/m 2/yr (as cited in Ricklefs 1979). and see review by Moll and Legler [1971]). low water temperatures may constrain the ability of temperate-zone turtles to harvest and process food. 09 Apr 2016 04:08:26 UTC All use subject to http://about. and transfers among. In contrast to desert lizards that are probably not under severe process constraints.3 kg/ha (2. 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. 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). with primary productiv- ity averaging 2. aquatic turtles occupy relatively productive habitats. and a community consisting of three turtle species in Michigan averaged 7. among turtle populations. A suggestion that processing constraints may be influential can be seen in the following comparison of turtle populations from South Carolina and Michigan. and Standora 1983). II. Turtles from the warmer habitats had higher growth rates and attained larger body sizes than did those from the natural environment. 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.jstor. 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. these dual constraints may also limit the total amount of resources consumed by turtles each year. Because of the positive relationship between tempera- ture and rate of digestion and gut clearance (Avery 1987). The potential effect of harvest and processing constraints on the population dynamics of turtles may have been overlooked. In addition. Congdon and Gibbons 1989). energy budget com- partments of many turtles.360 Justin D. Congdon 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. Auth 1975. Spotila. it may be predicted that. This content downloaded from 177.179 on Sat.230.9 X 10-2% of average primary productivity). the severity of constraint will increase with the amount of plant material in the diet and with either latitude or altitude.

The time spent in aerial basking certainly restricts a turtle's ability to engage in other activities.jstor. however.org/terms . Two studies have used the concept of operative environmental temperatures (Te) to study basking behavior of turtles (Crawford et al. Kenyon 1925 Enhanced digestive rates Gatten 1974. (2) may expose the animal to predators.230.235. and Standora 1988. Parmenter 1981 Reproduction: Increased fat mobilization Whittow and Balazs 1982 Increased rate of follicle development Congdon and Tinkle 1982. shape and radiative properties of the animal exposed to the same microclimate" (Bakken and Gates 1975). Schwarzkopf and Brooks 1985). Hammond. and (3) would increase metabolic demands (Huey and Slatkin 1976). A general definition of Te is "the temperature of an inanimate object of zero heat capacity with the same size. A prediction from cost-benefit analysis of basking behavior is that turtles will bask when This content downloaded from 177. Kepenis and McManus 1974. 1983. 09 Apr 2016 04:08:26 UTC All use subject to http://about. 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. Spotila.. basking in a vegeta- tion mat may also provide opportunities to feed.179 on Sat.Constraints on Energetics of Reptiles 361 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 .

The three species attain maximum adult body sizes of 0. so the turtle may be expected to bask only long enough to raise its body temperature high enough to permit efficient foraging). 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. during the summer months at high latitudes. In some years. When water temperatures are below that for efficient absorption of food material and rapid gut clearance. heating rapidly and returning to the water would only be the expected behavior of turtles with little or no food in their guts (i.5 m. After spring emergence.6 kg This content downloaded from 177.3O-30. Thus. This prediction makes the implicit assumption that time free from basking is the factor being optimized or maximized.'s are highest so that basking time can be minimized (Crawford et al.230. Congdon T. recorded at Crane Pond (ESGR) between June 1 and August 31. no resources need processing. 1). if turtles are primarily process limited (table 1)..org/terms . 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. 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.e. Sexton 1959. 1983). 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.179 on Sat. 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). Thus. painted turtles become active at about 8"C but do not begin feeding until water temperatures reach approximately 150 C (Cagle 1950. Ernst 1972) and in Minnesota (26.235. A similar temperature range was attained by basking painted turtles in Pennsylvania (22.5*-29. These temperatures indicate that turtles can harvest food only during the months of May through September. However. monthly means of maximum water temperatures at approximately 1 m depth in East Marsh (ESGR) do not exceed 150 C until May. were 130C and 29"C in 1954 and 18'C and 31 0C in 1957 (Sexton 1959).20C.0 *C. And.jstor. 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. Ernst 1972). The minimum and maximum water temperatures at approx- imately 0. Brattstrom 1965). then time spent at temperatures that promote rather than optimize enhanced digestive efficiencies and rapid gut clearance should be optimized (table 2). Mean minimum temperatures in some parts of East Marsh do not exceed 15 "C during the summer (fig. 09 Apr 2016 04:08:26 UTC All use subject to http://about.362 Justin D.

Growth rates of these juveniles suggest either that C. blandingi. they did not gain in body mass. fig. The proportion of protein in the diet of T scripta dramatically influences growth rates of juve- niles. serpentina is primarily a carnivore. C. 1. serpentina harvests more food or that the animal matter in its diet is of higher quality. Two of the spe- cies. Parmenter 1981. serpentina increased in body mass approximately three times as rapidly (145 g yr-'.org/terms . 2). 1.235.179 on Sat. Allocation of Energy to Reproduction in Turtles In order to understand reproduction in turtles. Juveniles fed a diet with either 25% or 40% protein grew at rates similar to those in the field (Avery 1987). however. each species may occupy different microhabitats. it is necessary to know the total amount of energy allocated to each clutch of eggs. (Chrysemyspicta). Juveniles of all three species occupy aquatic habitats on the ESGR. picta and E. whereas C. The increase in body mass of juveniles of the omnivorous species followed similar trajectories (50 g yr-1). Hart 1983). When fed food with 10% protein. C.7 kg (Emydoidea blandingi). Average minimum and maximum temperatures approximately 1 m deep in East Marsh taken every third day over 2 yr. 09 Apr 2016 04:08:26 UTC All use subject to http://about.jstor. 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. are omnivores. and their plastrons curled.230. the amount allocated This content downloaded from 177. and 13 kg (Chelydra serpentina). Moll and Legler 1971.Constraints on Energetics of Reptiles 363 EAST MARSH (MI) MEAN WATER TEMPERATURE MAX MIN 30 Cn 201 w 6 7 8 9 10 MONTHS (1981-1982) Fig.

400 /* 200 1 2 3 4 5 6 7 8 9 10 11 12 13 14 AGE Fig. 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.179 on Sat. Congdon and Tinkle 1982). The energy allocated to follicles during spring presumably came entirely from stored body lipids. Congdon. and This content downloaded from 177. Follicle sizes of C. 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. 2. Energy allocated to follicle enlargement during summer and early fall was presumably obtained directly from harvested resources. with substantial follicle enlargement taking place from late August through Octo- ber (Ernst 1971a. Data are from hatching to sexual maturity. examination of growth in C. 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). Congdon EMYDOIDEA CHRYSEMYS CHELYDRA 1800 1600 1400' 1200 < 1000 800 600. the time over which the energy was harvested and allocated.364 Justin D. On average. 1971 b. 09 Apr 2016 04:08:26 UTC All use subject to http://about.235. Growth of three species of turtles on the E. Congdon and Tinkle 1982). and Rosen 1981.230. S.org/terms . and the relative contributions of stored versus directly harvested energy to each clutch. George Reserve.jstor. picta from Michigan and Pennsylvania indicated that very little or no growth. to each egg. In addition. because stored lipids in females also increased during this period. picta are smallest just after the nesting season.

235.jstor. At high latitudes. picta in Michigan and T.Constraints on Energetics of Reptiles 365 presumably little or no feeding activity. storage. that portion of an animal's resource budget that is allocated to reproduction (Fisher 1930. 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. complete vitellogenesis during the time the eggs for the first clutch are in the oviducts. scripta in South Carolina is approximately 12 d (J. (2) the quantity of energy to be allocated to each offspring. However. Ernst 1971c). W. and reproduction. 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. where follicles were fully developed (ovulatory size) between August and December. was taking place before June (Sex- ton 1959. The minimum interval between the first and second clutches of C. Central to these theories is the concept of reproductive effort.org/terms . 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. and optimal egg size. and ovulation of the first clutch occurred during late April of the following year (Mc- Pherson and Marion 1982). a female must make three major "determinations": (1) the total amount of energy available for present reproduction. Gibbons. 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. unpublished data). (2) the follicles for the second clutch develop at the same time as those for the first clutch and. growth. Hirshfield and Tinkle 1975). 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. Energy Allocation and Life-History Theories In preparation for reproduction. may be more limiting in some years than is absolute availability of energy.179 on Sat. A similar pattern of follicle development during late summer has been observed in Sternotherus odoratus in Alabama. This content downloaded from 177. and (3) the number of individuals that can be produced by the present level of investment in each offspring. 09 Apr 2016 04:08:26 UTC All use subject to http://about. if necessary. The three determinations fall roughly into the con- ceptual categories of reproductive effort. parental investment. III.230.

179 on Sat. Congdon.235. Since all of the PIC must be added to the contents of the This content downloaded from 177. Congdon.366 Justin D.230. 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. Wil- hoft 1986. Tinkle. 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. Congdon and Tinkle 1982. Congdon and Tinkle 1982. insects [Parker and Begon 1986]) rather than to provide it with posthatching reserves. both categories of in- vestment. 1983a. Troyer 1983. and Greene 1983b. 09 Apr 2016 04:08:26 UTC All use subject to http://about." Under Trivers's definition. 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. In this case all of the material in the egg would be in the form of hatchling tissues or waste products. Congdon All of the energy allocated to each individual turtle hatchling is contained within the egg. 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]. and Rosen 1983a.jstor. that used for embryogenesis and that used for fueling the developed hatchling. and energy invested by the female for parental care (PIC)-that is. Wilhoft 1986. Congdon and Gibbons 1987). 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. 1983b. Parental investment in reptiles should be separated into energy invested in making a complete embryo (PIE). 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. 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. fall under the overall category of PI. Gibbons. this investment is far from trivial (Kraemer and Bennett 1981. energy in excess of that needed to produce a complete hatchling. 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. Congdon et al. Troyer 1983. By lumping together both categories of investment in an egg. 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.org/terms . Stewart and Castillo 1984. Congdon and Gibbons 1987). However.

The models make the following assumptions: (1) parents have a limited amount of resources or energy available for a given reproductive bout.230. and hatchling quality have not been established. increase the size of the egg. if some factor other than absolute energy availability lim- its allocation to reproduction (e. 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. or parental investment that does not primarily influence the size of the hatchling).Constraints on Energetics of Reptiles 367 egg. A major prediction from OES theory is that. 1968. Parker and Begon 1986) attempt to model the relationships and interactions between egg size and number. and (3) the fitness of offspring is not linearly related to the amount of parental investment. A second problem is that the relationships among egg size. 09 Apr 2016 04:08:26 UTC All use subject to http://about.org/terms . 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.. Svardson 1949. However. 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. (2) a minimum amount of energy is required to produce a viable offspring. If assumption (1) is true. then results inconsistent with predictions from OES models can be obtained. by definition. Brockelman 1975. 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. Williams 1966. Optimal egg-size (OES) models (Williams 1966. Smith and Fretwell 1974. Schaffer and Gadgil 1975)..e. 1954. This content downloaded from 177. 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. that is. time constraints or morphological constraints such as volume of a turtle's body cavity.g. it must. as the amount of energy invested in individual offspring goes up.235. it follows that. 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). 1987). size of the pelvic opening. within a population. Nussbaum 1985. Interactions between determinants of size or quality of offspring and off- spring numbers have been considered for some time (Darwin 1859).179 on Sat. the number of individuals produced must be reduced. but it appears to influence hatchling quality in ways not directly related to hatchling size. hatchling size. 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.jstor. There are currently two major categories of evolutionary theories (i.

George Reserve maintenance crew. This content downloaded from 177.. Thus. Capinera 1979. Wiltse.jstor. 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. Congdon Therefore. Kaplan and Cooper 1984). OES models might be better termed optimal offspring-quality models. the additional factor of morphological constraint apparently limits the way reproductive investments can be partitioned in some turtles. picta and D. Kaplan 1980. egg size increased from the smallest to the largest gravid females. processing. i. reticularia). picta and D. who died in May 1988. 09 Apr 2016 04:08:26 UTC All use subject to http://about. and allocation by reptiles can be influenced by extrinsic and intrinsic factors.e. and some less than obvious. The constraint on egg size due to pelvic opening size in C. Caswell 1983. Within these models. reticularia apparently resulted in a situation that is not in accord with that predicted by OES. A study of three species of emydid turtles (Chrysemyspicta. 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. and the degree of limitation is greater in smaller-bodied species.235. foreman of the University of Michigan's E. variation in egg size should occur within a single reproductive bout or among reproductive bouts within a single year (Kaplan and Cooper 1984). In contrast to OES theorists. Acknowledgments This paper is dedicated to Richard M. where pelvic constraint did not exist.org/terms . The preceding discussions have attempted to identify some obvious. In contrast. and the existence supporting data for one theory should not be considered as refuting the other. It might be expected that there are life-history traits and environmen- tal conditions that could result in either strategy. Deirochelys reticularia. ways that energy acquisition. 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). Cooper and Kaplan 1982.368 Justin D. S. In two smaller-bodied species (C. and the slopes of the lines relating egg size and pelvic opening width to body size were essentially equal. 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.230.179 on Sat. substantially more of the variation in reproductive output was due to variation in egg size than was found in T scripta.

ANDERSON.S. GATES and R. Cnemidophorus tigris. Oecologia (Berl.. Dietary shift in the turtle Pseudemys scripta (Schoepff) from youth to maturity. 20:31-54. 1986..230. energetics of reproduction and sexual selection in a widely foraging lizard. R. L. N. Phenotypic plasticity in life-history traits: demographic effects and evolutionary consequences. eds. Ecology 46:99-118. Springer-Verlag. D. Chry- semys scripta scripta (Schoepff). 1982. Monogr. H. 1987.Constraints on Energetics of Reptiles 369 He was a friend and an enthusiastic supporter of the long-term turtle research program on the George Reserve. Monogr. Academic Press. 1975. Ecol. University of California. 09 Apr 2016 04:08:26 UTC All use subject to http://about. D. F. J. Pages 255-290 in D. Y. J. David Scott. 114:350-361. GANS. Biol. Body temperatures of reptiles. The life history of the slider turtle. Foraging behavior. Nat. Pages 233-271 in C. BROCKELMAN. AVERY. CONGDON. ed. Buffalo. State University College at Buffalo. W. R. BALLINGER. D.D. diss. New York. Behavioral ecology of basking in the yellow-bellied turtle. TINKLE. AUTH. E.. 109:677-699.. A. A. Energy budgets and life histories of reptiles. Ecology of the basking habit of turtles. Zool. GIBBONS. B. CAGLE. CLARK. R. BRATTSTROM. and W. 73:376-422. Energetics of the montane lizard Sceloporusjarrovi: a measurement of reproductive effort. SCHMERL. Perspectives of biophysical ecology. Sci. Ph.. Roles of diet protein and temperature in the nutritional energetics of juvenile slider turtles. Florida State Mus. Biology of the Reptilia. Copeia 1980:921-923. CONGDON. Am. J. E. 1969. DUNHAM. Heat transfer analysis of animals: some implica- tions for field ecology. Whitfield Gibbons. W. 1979. 1977. 1965. and optimal clutch size. 13. R. Gary Meffe. Tempe.org/terms . M. Am. Literature Cited ANDERSON. KARASOV. 20:1-45. thesis. 1983. New York.179 on Sat.D. Midl. 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. Ph. S. A. 23:35-46. Earlier drafts of this manuscript were improved by comments from Roger Anderson. Qualitative variation in plants and insects: effect of propagule size on ecological plasticity. Ecol. B. BOYER. M. 1975. Arizona State University. H. and evolution.jstor. Nat. J. diss. R. 58: 79-110. 1975. AVERY. and D. W. the fitness of offspring. and J. Trachemys scripta. and D. B. 1950. physiology. Vol. CAPINERA. Los Angeles. Vitt. W. Am. Copeia 1969:704-706. L. H.) 19:165-170. This content downloaded from 177. Competition. R. D.Y. BAKKEN. Energetics of the lizard Cnemidophorus tigris and life history consequences of food-acquisition mode. D. GATES. 1965. Pseudemys scripta troostii (Holbrook). 1980. Gary Hepp. A. Iguanidae). Bull. G. Nat. CONGDON. M. William Cooper. H. D. CASWELL. 1988. Food resource limitation of body growth rates in Sceloporus scalaris (Sauria. Am. and J. and Laurie J. Clutch size and reproductive effort in the lizard Lacerta vivipara Jacquin. 1975.235.

London.org/terms . HAMMOND. 19. 1978. J. K. C. CONGDON. STANDORA. J. Acad. Biomass productivity of turtles in freshwater wetlands: a geographic comparison. W. . SpringerVerlag. GREENE. 1976. Basking behavior of the This content downloaded from 177. and J. 1974. Vol. 1983. M. DARWIN. 1979. A. E. C. and E. R. Ecological studies: analysis and synthesis. or. Copeia 1974:912-917. M. and J. Ecology 59:770-778. Mus. On the origin of species by means of natural selection. 5:151-160. R. Thermally imposed time constraints on the activity of the desert lizard Sceloporus merriami.. Chrysemyspicta. DUNHAM. R. 1859. L. J. 1981. Biol.jstor. and P. 5:151-160. L. Savannah River Ecology Laboratory Symposium. COOPER. W. GATTEN. WILLSON.. 09 Apr 2016 04:08:26 UTC All use subject to http://about. GIBBONS. P. Population dynamics and activity cycles of C. Biol. SZAREK. Nat. GRANT. Plant production in arid and semi-arid areas.179 on Sat.. Freshwater Wetlands (in press).. Theor. D. M. Some effects of soil-moisture availability on above-ground production and reproductive allocation in Larrea tridentata (DC) Cov. GIBBONS. A.. Sexual cycles and maturity of the turtle Chrysemyspicta. SHULZE. USA 84:4145-4147. J. Herpetol.. in SE Penn. J. J. 1930. Bull. D. J. Food availability as a proximate factor influencing individual growth rates in the iguanid lizard Sceloporus merriami. Operative environmental temperatures and basking behavior of the turtle Pseudemys scripta. C. E. E. Misc. J. and A. 140:191-200. and E. 1981. Copeia 1972:217-222. and U. New York. KAPPEN. O. Reproductive energetics of the painted turtle (Chrysemyspicta). W. 1983a. 94:135-151. Morphological constraint on egg size: a challenge to optimal egg size theory? Proc. 1982. Herpetol. Adaptive "coin-flipping": a decision-theoretic examination of natural selection for random individual variation. 1987. the preservation of favoured traces in the struggle for life. H. Clarendon.. Herpetologica 38:228-237. and E. Midl. ROSEN. Chrysemys picta.370 Justin D. SHULTZ. KAPPEN. 1971a. Pages 439-451 in O. R. 1971 c. DUNHAM. Murray. Sci. Ecology 64: 989-999. Populations in a fluctuating environment: the comparative population ecology of the iguanid lizards Sceloporus merriami and Urosaurus ornatus. CONGDON. 83:404-415. A. Copeia 1983:264-268. 158:1-62.. Pub. The genetical theory of natural selection. L. 1983b. D. D. D. SPOTILA. 1972. J. REYNOLDS.230. Oxford. TINKLE. D. ERNST. SYVERTSEN. Egg components and utiliza- tion during development in aquatic turtles. N. F. GIBBONs. R. 1971b. L. F. TINKLE. CRAWFORD. LANGE. Sci. S. and D.J. STANDORA. CUNNINGHAM.. J. picta in SE Penn. W. W. 1988. J. and J. Univ. Growth of the painted turtle. R.) 40:113-123. HADLEY. A. BUSCHBOM.235. 1987. W. and S. L. B. D. KAPLAN. W. K. EVANARI. CONGDON. G. H. Effect of nutritional status on the preferred body temperature of the turtles Pseudemys scripta and Terrapene ornata. A. 1970. Natl.. J. Temperature-activity relationship in the painted turtle. The influence of terrestrial activities on the population dynam- ics of aquatic turtles. Congdon CONGDON. Ecology 64:419-425. LANGE. Ecology 69:167-176. Parental investment in the chicken turtle (Deirochelys reticularia). 1982. Biol.. L. and R. Zool. FISHER. SPOTILA. eds. Mich. 31:747-753. E. Oecologia (Berl. Productivity of desert ecosystems. Am. 1989..

1983. Physiol. Acad. and J. Bull. 4:25-51. LEGLER. NAGY. eds. R. T. Energy and nitrogen budgets of the free- living desert lizard Sauromalus obesus. Ecological adaptations for breeding in birds. M. W. Physiol. Ecological energetics of a lizard. R. Ecol. and M.. KARASOV. Comp. Methem. 5:195- 214. A.S.jstor. G. R. Mar. and W. MOLL. 1982. Nat.. SLATKIN.. R. HART. PIANKA. Digestive enzymes in poikilothermal vertebrates: an investigation of enzymes in fishes with comparative studies of those of amphibians.. 1976. Interhabitat differences in energy acquisi- tion and expenditure in a lizard. 1987. 1971. The evolution of developmental plasticity in the reproductive characteristics: an application of the "adaptive coin-flipping" principle. R. Caretta caretta. Comp. Chry- semyspicta. M. MCMANUS. I. and P. KENYON. Natl. Ibis 89:302-352. 1954. Evolution 34:5164. W. Copeia 1981:406-411.. Seasonal changes of total lipids in the turtle Sternotherus odoratus. WHITFORD. Natural selection and the evolution of reproductive effort. A. acclimation temperature. Annu. A. HIRSHFIELD. in Panama. K. Sci. Rev. Biol. 1984. Rev. R.. E.230. Q. 1974. Clarendon. COSTA. 1975. W. Physiol. Rev. V. 48:252-262. NAGY. 41:197-200. Natl. Physiol. SHOEMAKER. K. The natural regulation of animal numbers. T.. Zool. USA 72:2227-2231. S. Harvard University Press. Utilization of post-hatching yolk in logger- head sea turtles.Constraints on Energetics of Reptiles 371 turtle Pseudemys scripta: effects of digestive state. MCPHERSON. Herpetologica 42:73-92. D. HUEY. W. and R. J. and J. Bull. H. Biochem. KRAEMER. Proc. J. MARION. 1986. 1948. and E. H. V. 90:25-45..235. Los Angeles County Mus. 0. and S. and E. electrolyte. A. Fisheries Ser. Ecology 65:235-247.. SHOEMAKER. BENNETT. Cambridge. Syst. 71A:93-98. Hist. 123:393-410. K.. H. HUEY. NAGY. and V. Costs and benefits of lizard thermoregulation. Pseudemys scripta (Schoepff). TINKLE. 49:351-363. 1954. E. A. Biochem. Nat. 61:69-77. 1982. ANDERSON. 1975. 1976. Desert ecosystems: environment and producers. 1925. LIGHTFOOT. COOPER.org/terms . KAPLAN.. Syst. Ecology 35:581-584. and nitrogen budgets of jackrabbits (Lepus californicus) in the Mojave Desert. Algae on turtles: some additional considerations. London. NoY-MEIR. Am.. sex. 1968.. 09 Apr 2016 04:08:26 UTC All use subject to http://about. Herpetologica 39:285-290. Sci. --. Pages 24-54 in R.179 on Sat. 48:309-317. Lizard ecology: studies of a model organism. H. C. The implication of ovum size variability for offspring fitness and clutch size in several populations of salamanders (Ambystoma). and W. A. J. H. F. --. 1980. and W. Dietary and habitat shift with size of red-eared turtles (Pseudemys scripta) in a southern Louisiana population. The life history of a neotropical pond slider turtle. Bioenergetics of young painted turtles. H. Zool. Water. The significance of clutch size. ALLEN. Physiological ecology of desert tortoises in southern Nevada. KAPLAN. Desert ecosystems: higher trophic levels. and K. 1974. D. This content downloaded from 177. KEPENIS. R. U. 51:363-384. SCHOENER. 1984. NEILL. Zool. Annu. R. 1973. D. reptiles and mammals. Oxford. . Variation in insect densities on creosotebush: is nitrogen a factor? Ecology 68:547-557. A. NAGY. B. LACK. 11:1-102. and season. and D. K. 1981. Ecol. Physiol. MEDICA.

Am. Agric. eds. and R. M. eds. 1981. Nat. E. 29:113-140. Publ. C. Belknap. New York. E. TINKLE. J.372 Justin D. J. E. F. 57:377-383. Chicago. G. R. Comp. Rock Valley Validation Site Report. Physiol. R. 1987. 1925. and R. Cambridge. D. Ecology 62:1426-1432. Turtle Tortoise Soc. Publ. E. 1979. Application of operative environmental temperatures to analysis of basking behavior in Chrysemys picta. Univ. 128:573-592. eds. Pop. University of Georgia. 1959. ALEXANDER and D. R. and M. 169:1-50. DIAMOND. 1981. Selection for optimal life histories in plants. Ecology 6:93-103. Monogr. KEARNEY and R. E. Flowering plants and ferns of Arizona. 09 Apr 2016 04:08:26 UTC All use subject to http://about. DUNHAM. Mus. SEXTON. Natural selection and social behavior. H. SVARDSON. D. L. 70:235-238. A population analysis of the ovoviviparous lizard Sceloporusjarrovi in the Pinaleno Mountains of southeastern Arizona. U. Freshwater Res. Ecol. 2:20-25. W. R. Oecologica 58:340-344. R. S.. The vegetation of Arizona. Physiol.S. Ecology. Posthatchling yolk energy in a lizard: utilization pattern and inter- clutch variation. Mass. Pages 96-107 in R.jstor. Primary production in four North American deserts: indices of efficiency.. O. D. BEGON. Pages 136-179 in B. E.D. Misc. ed. Optimal egg size and clutch size: effects on environment and maternal phenotype. Pergamon. 1984. P. Rep. The evolution of parental care in salamanders. ROSEN. R. C. US/IBP Desert Biome Research Memorandum. Logan. Ecological aspects of the deserts of California. 1942. and M. CASTILLO. D. Parental investment and sexual selection. 1983. 108:499-506. RICKLEFS. Drottningholm 29:115-122. and S. Nutritional provision of the yolk of two species of viviparous reptiles. Evolutionary ecology. 29:27-44.org/terms . PARKER. Arid Environ. A. Harper & Row. Sexual selection and descent of Man. The optimal balance between size and number of offspring. A. G. 1972. 1986. Zool. New York. 2:187-209. SHREVE. M. Am. CAMBELL. Res. 1974. Inst. 1985.235. 2d ed. . Parental care and egg size in salamanders: an examination of the safe harbor hypothesis. The sun and the turtle. TROYER. Ecol. CONGDON. CODY and J. A. K. 1975. Lepidoptera genetics. BROOKS. R. In T. R. Mich. SCHAFFER. Her- petologica 40:425-436. R. J. D. PARMENTER. Ecology and evolution of communities.. C. GADGIL. J. diss. and P. 1979.. 1974. L. Chiron. Aldine. F. 1968.179 on Sat. F. ROBERTSON. E. D. Ph. Zool. G. Congdon NUSSBAUM.. 1971. 1985. .. Pages 142-157 in M. W. 1973. PEEBLES. Utah State University. SMITH. B. Nat. Phenotypic correlates of male reproductive success in the lizard Sceloporusjarrovi. Pseudemys scripta. L. H. Natural selection and egg number in fish. PIANKA. FRETWELL. TINKLE. RUBY. RUBY. D.230.J. Chiron. 1984. TURNER. P. STEWART. New York.. SCHWARZKOPF. Biochem. J. Dept. A telemetric study of the thermoregulatory behavior and cli- mate-space of free-ranging yellow-bellied turtles. STANDORA. GREENHOOD. Herpetologica 41:206-212. Oxford. 1949. 1981. Int. Chrysemyspicta marginata (Agassiz). and W. TRIVERS. H. W. and A. SZAREK. 73-2. PRITCHARD.. This content downloaded from 177. Spatial and temporal movements of a population of the painted turtle. 1982. Misc.. Digestive turnover rates in freshwater turtles: the influence of temperature and body size. Nesting frequency and success: implications for the demography of painted turtles.

WILLIAMS. C. F. R. 1966. Energy utilization by a desert lizard (Uta stansburiana). Thermodynamic consideration in animal nutrition. G. H. S. Logan. Utah State University. W. C. Biochem. 1974. N.. D. Utah State University Press. Am. and G. G.179 on Sat. tro- phic level. WILHOFT. G. P. Rock Valley Validation Site Report.230. 09 Apr 2016 04:08:26 UTC All use subject to http://about. 307 pp. and B. Eggs and hatchling components of the snapping turtle Chelydra serpentina. and resource availability in life history evolution. 1968. Comp. grasslands. Physiol. Nat. KINERSON. Am. Sci. Logan. C. H. and J. BALAZS. P. 1. 1986. W. Environmental certainty. Adaptation and natural selection. and desert ecosystems.Constraints on Energetics of Reptiles 373 1974.org/terms . Zool. Princeton University Press. KOWALEWSKY. Pac. Primary pro- ductivity and water use in native forests. US/IBP Desert Biome Research Memorandum. WEBB. Ecol- ogy 59:1239-1247. and M. MEDICA. TINKLE. D. 1976. 1978.. no. TURNER. WIEGERT. This content downloaded from 177. Princeton. 73-3. SMITH. LAUENROTH.. B. 108:805817. WILBUR. 8:71-81. COLLINS. 1982. US/IBP Desert Biome Monogr. R. A. M.235.J. WHITTOW.jstor. 84A:483-486. Basking behavior of the Hawaiian green turtle (Chelonia mydas). W. 36:129-139.. W. SZAREK.