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Lizard Ecology: Historical and Experimental Perspectives

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In a collection rich in implications for all fields of ecology, leading lizard ecologists demonstrate the utility of the phylogenetic approach in understanding the evolution of morphology, physiology, behavior, and life histories. Lizards, which are valued for their amenability to field experiments, have been the subject of reciprocal transplant experiments and of manipulations of resource availability, habitat structure, population density, and entire sections of food webs. Such experiments are rapidly ...
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Overview

In a collection rich in implications for all fields of ecology, leading lizard ecologists demonstrate the utility of the phylogenetic approach in understanding the evolution of morphology, physiology, behavior, and life histories. Lizards, which are valued for their amenability to field experiments, have been the subject of reciprocal transplant experiments and of manipulations of resource availability, habitat structure, population density, and entire sections of food webs. Such experiments are rapidly rebuilding ecological theories as they apply to all organisms. As a demonstration of state-of-the-art historical and experimental research and as a call for philosophical engagement, this volume will join its predecessors--Lizard Ecology: A Symposium Missouri, 1967 and Lizard Ecology: Studies of a Model Organism Harvard, 1983--in directing ecological research for years to come.Lizard Ecology contains essays on reproductive ecology Arthur E. Dunham, Lin Schwarzkopf, Peter H. Niewiarowski, Karen Overall, and Barry Sinervo, behavioral ecology A. Stanley Rand, William E. Cooper, Jr., Em¡lia P. Martins, Craig Guyer, and C. Michael Bull, evolutionary ecology Raymond B. Huey, Jean Clobert et al., Donald B. Miles, and Theodore Garland, Jr., and population and community ecology Ted Case, Robin M. Andrews and S. Joseph Wright, Craig D. James, and Jonathan B. Losos.
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Editorial Reviews

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"Organized into four theme areas containing a total of 14 topics, each [paper] is preceded by an insightful introduction written by a specialist in that area [and] . . . includes a section on future work and new questions that should be explored. . . . a welcome addition for anyone wishing to examne research in this fascinating field."--Choice

"The topics, [in this volume] represent an impressive diversity of approaches, ranging from detailed life-history studies of single species and in-depth analyses of lizard communities to broad-based comparisons of multiple traits across all groups of lizards. . . . [Lizard Ecology] not only provides a context in which to view these individual studies but opens a unique window on lizard ecology past, present, and future."--Science

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Product Details

  • ISBN-13: 9780691036496
  • Publisher: Princeton University Press
  • Publication date: 6/13/1994
  • Pages: 416
  • Product dimensions: 6.55 (w) x 9.63 (h) x 1.23 (d)

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Lizard Ecology

Historical and Experimental Perspectives


By Laurie J. Vitt, Eric R. Pianka

PRINCETON UNIVERSITY PRESS

Copyright © 1994 Princeton University Press
All rights reserved.
ISBN: 978-0-691-03649-6



CHAPTER 1

MEASURING TRADE-OFFS: A REVIEW OF STUDIES OF COSTS OF REPRODUCTION IN LIZARDS

Lin Schwarzkopf


The life history of an organism may be defined as a co-adapted complex of traits (Stearns 1976, 1989a; Ballinger 1983). If life-history traits are co-adapted, the concept of trade-offs is central to the understanding of life-history evolution. This is because the optimization of a single aspect of reproduction cannot occur except at the expense of other, related aspects. Thus, natural selection should produce phenotypes that are compromises between the costs and benefits of changing any particular character.

The concept of costs of reproduction first arose to address an apparent contradiction between theory and observation. All things being equal, it is assume that organisms producing more offspring should have higher reproductive fitness (i.e., they leave more descendants) than those that do not. Thus, natural selection should maximize lifetime production of offspring. Total lifetime production of offspring could be maximized by maturing early and devoting all resources to the production of one very large clutch of offspring (Cole 1954). Many organisms, however, do not seem to follow this strategy; instead, maturity is often delayed, organisms are iteroparous, and fecundity at any particular reproductive episode is lower than that which is physiologically possible. Williams (1966a) suggested that the solution to this apparent contradiction lies in the existence of costs of reproduction. These costs can be seen as the negative aspects, or disadvantages, of any particular level of reproductive expenditure and they are measured in terms of future reproductive output. An individual's expected future reproductive success (probable number of offspring produced during the rest of its life) may be defined as "residual reproductive value" (Fisher 1930; Williams 1966a; Pianka 1976). Costs of reproduction are decrements to residual reproductive value accruing from a given act of current reproduction (Fisher 1930; Williams 1966a). For instance, in iteroparous organisms, an increase in current reproductive expenditure may decrease the probability of survival of the reproducing individual or the amount of energy it has available for reproduction in the future. In this case, lifetime production of offspring may be maximized by a strategy of relatively low reproductive expenditure in any one reproductive episode. By keeping reproductive expenditure relatively low at any particular reproductive event, an organism may reproduce many times in its lifetime, thereby increasing lifetime reproductive success relative to an organism that devotes more to a single reproductive bout (e.g., Pianka and Parker 1975). In this view, reproductive output is determined by trade-offs between the costs to future reproduction arising from the benefits of present reproduction.

Two components to reproductive costs are "survival costs" and "fecundity costs" (Bell 1980). Survival costs reduce the survival of reproducing organisms. Fecundity costs may reduce an organism s ability to reproduce in the future in two ways. They may directly reduce energy stores that could otherwise be used for future reproduction (Stearns 1989a). I refer to this type of fecundity cost as a "direct fecundity cost." In organisms that grow after maturity, and in which fecundity is related to body size, fecundity will be reduced if growth rate is reduced (Williams 1966b). In this case, fecundity is reduced through an indirect effect of reproduction on growth rate, and I refer to this as an "indirect fecundity cost" or a "growth cost." Survival costs and fecundity costs may function separately, or they may be linked. For example, if energy stores are depleted by reproduction, reproducing individuals may need to forage more frequently, and hence may be exposed to increased risks of predation.


Measuring the Costs of Reproduction

There has been controversy in the literature concerning the best way to measure costs of reproduction. A variety of reviews found supporting evidence for the existence of costs of reproduction (Clutton-Brock 1984; Partridge and Harvey 1985; Reznick 1985; Bell and Koufopanou 1986; Stearns 1992). However, these studies also found several circumstances under which negative effects of reproduction do not occur or cannot be measured. These circumstances may be summarized as follows: (1) Positive correlations between survival and reproduction, or between past and future reproduction have often been observed in field studies of costs (Reznick 1985). Positive correlations are usually explained in terms of variation among individuals in resource acquisition abilities, i.e., if some individuals can acquire more resources than others, they may be better able to survive and reproduce, or they may be able to reproduce more frequently than individuals that are less able to acquire these resources (Clutton-Brock 1984; van Noordwijk and de Jong 1986). Positive correlations among phenotypic characters measured in the field can mask underlying negative genetic correlations that can be measured in the laboratory (Rose and Charlesworth 1981a, b), and are not evidence for the nonexistence of costs. (2) Reproduction may not be energetically costly. If energy is not a limiting resource, or if investment in reproduction can be made without a concurrent decrement in growth or energy stores, then there is no direct fecundity cost of reproduction (Stearns 1992).

Reznick (1985) and Bell and Koufopanou (1986) evaluated four different methods that have been used to measure costs of reproduction. (1) Phenotypic correlations are most commonly used to study costs. This type of study correlates some index of reproductive expenditure (e.g., clutch size, parental care) with some index of a cost, and can be done in the field (e.g., Reznick and Endler 1982). (2) Experimental manipulations are another way that costs can be studied. In this case, some aspect of reproduction is manipulated, Eind a cost-related response is monitored. Experimental manipulations have often been performed in the field, or in the laboratory under seminatural situations (Calow and Woollhead 1977; Marler and Moore 1988; Roitberg 1989). (3) Alternatively, genetic correlations may be used to study costs. These studies have used quantitative genetic designs to determine genetic correlations between reproductive expenditure and cost (e.g., Rose and Charlesworth 1981a; Reznick 1983). These studies are usually conducted in the laboratory under controlled conditions. (4) Finally, selection experiments may be used to measure costs. This type of study observes correlated responses to selection pressures on particular characters in the laboratory (Rose and Charlesworth 1981b).

Reznick (1985, 1992) strongly recommends that selection experiments be conducted to verify the basic assumption that observable variation in life-history characteristics has a genetic basis. Evolution cannot occur in response to variation with no genetic basis. Although selection experiments are critical to validate the basic assumption behind studies of costs, observational, and especially experimental field studies of phenotypic variation are necessary to study costs that are mediated by the environment (e.g., increased predation) and also to elucidate ways that organisms avoid costs (Reznick 1992; Stearns 1992). Various authors have stressed the need for field manipulations of reproductive allocation to understand environmental influences on costs (Pianka 1976; Partridge and Harvey 1985; Bell and Koufopanou 1986; Partridge 1992; Stearns 1992). In these experiments, the presence of sufficient genetic variation to allow evolutionary response to selection is assumed to exist. There is strong evidence from artificial selection (Maynard Smith 1978) and from selection experiments conducted under field conditions (e.g., Reznick et al. 1990) that this assumption is justified, although there are circumstances under which available variation is constrained by antagonistic pleiotropy and linkage disequilibrium (Stearns 1992).


Lizards as Model Organisms

Most field studies of costs of reproduction have been conducted using birds (reviewed by Lindén and Møller 1989). This concentration of studies on birds has limited the kinds of questions that researchers have asked to those prescribed by bird life histories. In particular, studies of costs in birds have measured the costs of parental care, and how these costs vary with fecundity. In certain ways, lizard life-history characteristics are more variable than those of birds. All birds are oviparous and most have some form of parental care (Blackburn and Evans 1986). Lizard species, however, span the range from oviparous to viviparous, and oviparous species may or may not have parental care (Shine 1988). Also, unlike birds, lizards may grow significantly after sexual maturity, so that there is the potential for indirect fecundity costs to be important in determining their reproductive output. Because of these differences in life-history characteristics between birds and lizards, studies of lizards allow us to address different questions about costs of reproduction.

Lizards make good subjects for the study of costs of reproduction because both survival costs and direct and indirect fecundity costs can influence reproductive investment in lizards. Many species store resources as fat over long periods (e.g., Derickson 1976), and therefore direct fecundity costs may be important determinants of reproductive investment. As mentioned above, many species show significant growth after reproduction (BaIIinger 1983). In most species without fixed clutch sizes, clutch mass increases with body size (reviewed by Tinkle et al. 1970; Barbault 1976; Vitt and Congdon 1978; Vitt and Price 1982), so that indirect fecundity costs may influence reproductive allocation.

Another feature of lizard natural history that makes them suitable subjects for the study of costs, is that the ecology of juvenile lizards is similar to that of their parents. Lizards do not have larval phases during development as do many amphibians, fish, and invertebrates. It is possible to capture, mark, and determine the fate of offspring of particular individuals in the field, and therefore one can measure the fitness of particular traits or reproductive strategies (Sinervo 1990a; Brodie 1992).

Lizards have generally been considered too long-lived, and too large to be practical subjects for genetic correlation or selection studies of life-history characters. More recently, common-environment experiments have been used to determine the genetic contribution to variation in growth rates and life-history characteristics (Sinervo and Adolph 1989; Adolph and Porter 1993; Ferguson and Talent 1993). There have also been some interesting studies of selection on morphological and performance characters in juvenile snakes (Brodie 1992). Similar studies could be conducted using lizards as subjects. Studies of the genetic basis for life-history characteristics are limited in scope, as they must be confined to smaller bodied, short-lived species. However, it is critical to determine the extent of the genetic contribution to variation in life-history characters, because a variety of factors other than trade-offs among life-history characters can influence reproductive investment.


Factors Influencing Evolution of Reproductive Investment

Of course, trade-offs among life-history characters are not the only factors determining reproductive output in lizards (Ballinger 1983). To a varying degree, we expect the evolution of characters to be constrained by history (Gould and Lewontin 1979). Although life-history characteristics vary among and within species (Tinkle 1969; Vitt and Congdon 1978; Vitt and Price 1982; Dunham and Miles 1985; Barbault 1988; Dunham et al. 1988a) there is a strong tendency for most species in any particular group (family, genus) to have similar life-history characteristics (Vitt and Congdon 1978; Vitt and Price 1982; Dunham et al. 1988a). Thus, phylogenetic lineage appears to have an important constraining influence on patterns of life-history characteristics (Stearns 1980; Ballinger 1983; Dunham and Miles 1985; Dunham et al. 1988a; Vitt 1992). However, despite constraints, lizard life-history characters can evolve (Adolph and Porter 1993). Variation in life-history characters not accounted for by phylogenetic lineage will include evolved responses to different environments. For example, species in lineages with small, fixed clutch sizes (e.g., geckos, anoles) would not be expected to have large clutches in any environment where they occur, but evolution of egg size and clutch frequency in these species in various environments is expected (e.g., Andrews 1979).

Low survival rates in populations of lizards are often associated with early maturity and a relatively high reproductive output, and the latter characteristics are assumed to be an evolved response to the former (e.g., Pianka 1970; Tinkle and Ballinger 1972; Ballinger 1973; Vinegar 1975b; Barbault 1976; Ballinger 1977; Ballinger and Congdon 1981; Tinkle and Dunham 1986; Jones et al. 1987a). Recently, Adolph and Porter (1993) have suggested that similar relationships among survival and reproductive output can be explained as environmentally induced variation in these characters. The length of the activity period (daily and seasonal), and therefore, the energy acquisition rate, may be influenced by temperature, and this may in turn determine important variables such as growth rate and total clutch mass produced per year (Adolph and Porter 1993). In addition, survival rate may be related to the length of the activity period (Marler and Moore 1991; Adolph and Porter 1993). In at least one lizard species, Scelopoms undulatus, a significant proportion of the variation in important life-history traits such as survival rate and total annual fecundity and egg mass can be explained by the length of the activity season (Adolph and Porter 1993). However, it appears that other important life-history characters such as size at maturity are not explained by the length of the activity season in some populations of S. undulatus, suggesting that evolution may have influenced these characters (Adolph and Porter 1993). Similarly, Ferguson and Talent (1993) found genetically based differences among populations of this species in growth rate, egg size, and age of maturity.

An understanding of patterns of life-history characteristics occurring among species of lizards requires knowledge of the phylogenetic background of the species being considered. In addition, experiments to determine environmental influences on these characteristics among populations within species are also necessary. However, the presence of constraints due to phylogeny or the environment does not mean that costs cannot be important determinants of individual reproductive output. Phylogeny and environment provide the bounds within which a cost structure may operate. It is important to be aware of the influence of these two factors on patterns of reproductive characteristics at the species level and above.


Behavioral and Morphological Changes Associated with Reproduction Likely To Be Costly in Lizards

Reproduction may reduce survival and/or energy stores in lizards in several ways. In both sexes of most species of lizards, obvious behavioral and morphological changes associated with reproduction increase mortality, either by increasing the probability that individuals will be detected and captured by predators, or by decreasing energy available for maintenance. If mortality is not increased due to these changes, energy stores may be depleted, and growth rate and future fecundity may be compromised. I have listed these changes in Table 1.1, and now discuss each in more detail.


(Continues...)

Excerpted from Lizard Ecology by Laurie J. Vitt, Eric R. Pianka. Copyright © 1994 Princeton University Press. Excerpted by permission of PRINCETON UNIVERSITY PRESS.
All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.

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Table of Contents

Contributors
Introduction and Acknowledgments
1 Measuring Trade-offs: A Review of Studies of Costs of Reproduction in Lizards 7
2 Understanding Geographic Life-History Variation in Lizards 31
3 Lizard Egg Environments 51
4 Experimental Tests of Reproductive Allocation Paradigms 73
5 Prey Chemical Discrimination, Foraging Mode, and Phylogeny 95
6 Phylogenetic Perspectives on the Evolution of Lizard Territoriality 117
7 Mate Limitation in Male Norops humilis 145
8 Population Dynamics and Pair Fidelity in Sleepy Lizards 159
9 Determinants of Dispersal Behavior: The Common Lizard as a Case Study 183
10 Covariation between Morphology and Locomotory Performance in Sceloporine Lizards 207
11 Phylogenetic Analyses of Lizard Endurance Capacity in Relation to Body Size and Body Temperature 237
12 Long-Term Population Fluctuations of a Tropical Lizard: A Test of Causality 267
13 Spatial and Temporal Variation in Structure of a Diverse Lizard Assemblage in Arid Australia 287
14 Historical Contingency and Lizard Community Ecology 319
References 335
Author Index 389
Species Index 397
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