INTEG.
AND
COMP. BIOL., 42:278–290 (2002)
Evolutionary Approaches for Studying Functional Morphology: Examples from Studies of Performance Capacity1 DUNCAN J. IRSCHICK2 Department of Ecology and Evolutionary Biology, 310 Dinwiddie Hall, Tulane University, New Orleans, Louisiana 70118
SYNOPSIS. Performance studies have long been a cornerstone of evolutionary studies of adaptation because of their purported importance for fitness. Nevertheless, for most systems, the mechanistic link among habitat use, morphology and performance is poorly understood. Further, few studies consider how behavior affects the relationship between morphology and performance. Here, I highlight the utility of considering both of these neglected areas by discussing studies in two systems: (1) the evolution of habitat use in Caribbean Anolis lizards, and (2) the evolution of limb function in desert lizards. Caribbean Anolis lizards partition the habitat via selection of different perch diameters, and surface diameter also exerts a strong effect on locomotor performance. Phylogenetic analyses show that Anolis species tend to avoid using perches in which their performance is submaximal, and also show that species with large performance breadths use a greater range of habitats. The underlying basis of this performance to habitat use link is a trade-off between the ability to sprint quickly on broad surfaces and the ability to move effectively on narrow surfaces. Studies of the kinematics of high-speed locomotion in five morphologically distinct lizard species reveal that some species exhibited behaviors that greatly enhanced their performance abilities relative to other species, suggesting that behavior can play a key role in the link between morphology and performance. Overall, these findings underscore the value of using a mechanistic approach for studying the links between habitat use, morphology and behavior.
INTRODUCTION The ability of organisms to perform specific ecological ‘‘tasks,’’ such as capturing prey or escaping predators, may have far-reaching effects on organismal survival, reproduction, and growth (Arnold, 1983; Pough, 1989; Irschick and Garland, Jr., 2001). Because of the potential importance of performance ability to fitness, studies of performance ability have been a cornerstone of evolutionary biology for over 30 yr (see recent overviews in Pough, 1989; Garland and Losos, 1994; Aerts et al., 2000; Irschick and Garland, Jr., 2001). Arnold (1983) suggested studying this performance paradigm in two steps: first, by understanding the relationship between morphology and performance, and second, by understanding the relationship between performance and fitness. By far, the first of these two steps has proven to be the most popular, while only a few studies have investigated the second question, probably because quantifying fitness in nature is both timeconsuming and difficult, whereas studies that relate morphology and performance can be fairly easily completed in the laboratory. This first pass at establishing relationships between performance, morphology and fitness was intended for within-species studies, but other researchers have extrapolated this approach for among-species comparisons (Emerson and Arnold, 1989; Garland and Losos, 1994). Further, two key factors, behavior and habitat use, were not explicitly considered in Arnold’s (1983) paradigm, yet are important for both within- and
among-species comparisons. Differences in morphology lead to differences in performance capacity, which, in turn result in differences in habitat use. Behavior, in turn, mediates the relationships between both morphology and performance, and between performance and habitat use (Garland et al., 1990). Thus, among-species studies should focus on four key characteristics: morphology, performance, behavior and habitat use for fully understanding how species adapt to their habitats. It is important to note that fitness information is largely irrelevant to this among-species approach, as one cannot compare the fitness of different species and relate fitness of each species to interspecific differences in performance. An exception to this might come from comparative studies of fitness of different species in different habitats. Information about the relative fitness of each species in different habitats might shed light on adaptive processes. A persistent debate within evolutionary studies has been the debate concerning whether intraspecific information on fitness and genetic and phenotypic correlations is superior to comparative studies for testing adaptationist hypotheses (for recent examples, see Leroi et al., 1994; Larson and Losos, 1996). Clearly, these two approaches are complementary rather than antagonistic, as they use different methods for addressing the common question of whether trait variation is adaptive. Despite the large numbers of studies of performance, several key areas have received little attention. First, few studies have drawn a direct link between performance and habitat use, particularly in a quantitative and phylogenetic context, although some exceptions exist (e.g., Lepomis sunfish, Lauder, 1983; Mittelbach, 1984; Wainwright et al., 1991a, b). Neverthe-
1 From the Symposium Molecules, Muscles, and Macroevolution: Integrative Functional Morphology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois. 2 E-mail:
[email protected]
278
STUDIES
OF
PERFORMANCE CAPACITY
279
less, for most animal groups, the mechanistic basis for habitat segregation is poorly understood, primarily because the biomechanical basis for morphology and performance has not been investigated. Here, I demonstrate the utility of this approach (Phylogenetic tests of optimality) by outlining an evolutionary approach for testing adaptation to environments. Specifically, I describe tests of whether species of Anolis lizards avoid habitats in which their performance capacities are submaximal, and whether performance generalists are habitat generalists (Irschick and Losos, 1999). Second, the link between behavior and performance is poorly understood for most organisms, as biologists have been preoccupied with establishing relationships between morphology and performance. In the second part of this paper, I discuss studies that attempt to quantitatively relate behavior, morphology and performance by examining the evolution of limb function in a group of lizard species (Morphology, performance and behavior). PHYLOGENETIC TESTS OF OPTIMALITY A key component of any concept of adaptation is the assumption that species will use habitats in which a key performance trait is maximized (such as maximum sprinting ability), and avoid habitats in which that (and potentially other linked performance traits) are submaximal. This idea is not new, and was first widely tested in studies of optimality (Rosen, 1967; Stephens and Krebs, 1986), which persist to this day, but are controversial (Diamond, 1992). An underlying assumption of optimality studies is that certain activities are critically important to animals (i.e., feeding), and individuals cannot afford to be inefficient in that activity. Numerous studies have examined whether organisms forage optimally (Schoener, 1971; Stephens and Krebs, 1986), have different foraging behaviors (Perry and Pianka, 1997) or move at speeds that are optimal for energetic savings (Welham, 1994; Pennycuick, 1997; Weinstein and Full, 2000). A number of studies have successfully used optimality approaches to predict whether one or a few species use particular microhabitats, but few studies have used modern comparative methods to investigate this issue. However, some studies have profitably used phylogenetic methods to test whether species prefer temperatures in which they sprint maximally (Huey and Bennett, 1987). I am aware of no studies that have used this comparative approach to test whether species use structural habitats in which their performance is maximal. More generally, few studies have used a phylogenetic approach to address a basic ecological question, what is the mechanistic basis for interspecific differences in habitat use? Ecologists have most often attempted to answer this question by considering the relationships of a particular species to other species in their environment, or to abiotic factors (e.g., temperature) (Whittaker and Levin, 1975; Ricklefs and Schluter, 1993). However, a less frequently used approach
FIG. 1. Hypothesized relationships between habitat use and performance based on the habitat constraint model (A) or habitat breadth (B) models. Performance sensitivity refers to how well species perform in different habitats. Thus, high values of performance sensitivity means the species has a low performance breadth. Individual points are theoretical species values.
is to ask whether species use habitats based on their functional requirements. In this vein, studies of performance capacity hold particular promise as certain performance abilities may be critical for organismal fitness, and species may be constrained to use habitats in which their performance capacities are maximized. Two conceptual models relate variation in habitat use to variation in performance capacity among species (Irschick and Losos, 1999). The ‘‘habitat constraint’’ model proposes that as the performance decrement in a habitat increases (relative to a more favorable habitat), then the percent use of that habitat should decrease relative to the more favorable habitat. This pattern should lead to a positive relationship among species between performance decrement and percent habitat use (Fig. 1). The exact shape of this relationship may change depending on the performance variable of interest. This model can be rejected if there is no significant relationship among taxa between the comparative measures of habitat use and performance. What I term the ‘‘habitat breadth model’’ (see also Huey and Stevenson, 1979; Sinervo and Losos, 1989) posits that as performance sensitivity decreases (ability to perform well in a variety of environments), then habitat breath, or the diversity of habitats used, should increase (Fig. 1). In other words, performance generalists should be habitat generalists. The two models are not mutually exclusive. One might also test these ideas among populations within a well-
280
DUNCAN J. IRSCHICK
defined species, or even among individuals within a species, although the interspecific comparisons specifically test the hypothesis that each species has evolved to use the habitat in which it performs best. Naturally, both models could be rejected for a multitude of reasons. First, species may use habitats that are submaximal for an important performance measure because of competitive interactions with other species, or because a performance variable may not be as important to the species as the researcher believes. Field studies that document whether species actually use their performance capacities in nature, and in which ecological contexts they do so, are thus vitally important in studies relating habitat use to performance (Irschick and Losos, 1998; Irschick, 2000a, b). BACKGROUND AND KEY FINDINGS As an example of a key habitat variable which is also important functionally, I discuss the adaptations of arboreal Caribbean Anolis lizards to perch diameter, which is a key axis along which Anolis lizard species segregate. Perch diameter has a strong effect on locomotor performance (lizards: Losos and Irschick, 1996); rodents: (Thompson, 1990); marsupials: (Pridmore, 1994), but only in Anolis lizards has the link between performance and habitat use been studied extensively. Caribbean Anolis lizards are an excellent group for examining how maximal sprinting ability is related to structural habitat use. Anolis lizards have diversified tremendously, producing nearly 150 species in the Caribbean, including extensive radiations on each of the Greater Antillean islands of Cuba, Hispaniola, Jamaica, and Puerto Rico (Williams, 1983; Jackman et al., 1999). In many ways, Caribbean Anolis lizards have been a model system for studying how species adapt morphologically and behaviorally to different habitats (Roughgarden, 1995; Losos et al., 1998). Numerous studies on Caribbean Anolis lizards over the past 30 yr have shown that Anolis species on each Greater Antillean island have independently evolved into a series of ecologically and morphologically distinct habitat specialists (Rand, 1964, 1967; Moermond, 1979; Losos, 1990; Irschick and Losos, 1996, 1998, 1999; Irschick et al., 1997) which partition the environment by perch height and diameter (Schoener, 1968; Schoener and Schoener, 1971a, b; Losos, 1990; Irschick et al., 1997), and other characteristics (Lister, 1981). Although the habitat use of these species has been extensively investigated, most studies have focused on the mean ecological characteristics of species when they are initially spotted (but see Pounds [1988] for work on Central American anoles), and few attempts have been made to systematically quantify the range of perch heights and perch diameters that Caribbean anoles use as they move throughout their habitats. Consequently, such ‘‘first sighting’’ studies may provide a biased view of anole habitat use if perch locations are not a random sample of the substrates used during locomotion (Pounds, 1988).
FIG. 2. Phylogenetic tree for eight Anolis lizard species (see Jackman et al. [1999] for details). Locality headings next to species names represent the Caribbean islands on which these species occur, although A. carolinensis was studied in Louisiana. JAM 5 Jamaica, PR 5 Puerto Rico, BAH 5 Bahamas. From Irschick and Losos (1998).
Field studies of performance in nature have shown that anoles utilize their maximal sprinting capabilities to escape predators and, to a lesser extent, to capture prey (Irschick and Losos, 1998). However, in some anole species, maximum sprinting performance is markedly affected by surface diameter (Losos and Irschick, 1996; Losos and Sinervo, 1989). Thus, if the habitat constraint model is valid, then those affected species should limit their activities to those surfaces upon which they sprint well (i.e., close to their physiological maximum). By contrast, species whose sprint speed is affected minimally by surface diameter are free to use whatever perches they need, and they should also utilize a greater variety of surfaces in nature (i.e., have greater habitat breadth). These hypotheses were tested by focusing on a group of eight Anolis lizard species whose phylogeny is well corroborated (Fig. 2) (Irschick and Losos, 1999). This group consists of three representatives of the trunk-ground and trunk-crown ecomorphs, as well as two twig anoles (Fig. 2), thus providing reasonable statistical power for elucidating evolutionary relationships among habitat use, performance and behavior. The habitat constraint and habitat breadth models were tested by first establishing the maximal speeds of these Anolis species on a variety of surface diameters under optimal laboratory conditions. Next, focal animal surveys were conducted to establish the range of habitats that anoles used as they moved throughout their habitats. Evolutionary tests were then used to establish the link among performance and habitat use (see Irschick and Losos [1999] for details). The fundamental relationship central to habitat use
STUDIES
OF
PERFORMANCE CAPACITY
FIG. 3. Log-log plots of mean values of maximum speed (y-axis) versus dowel diameter (x-axis) for eight Anolis lizard species. Plot A is for species that were examined on dowels ranging from 0.7– 5.1 cm in diameter, whereas plot B is for species that were examined on dowels ranging from 1.2–4.6 cm in diameter. The regression lines are linear least-squares. From Irschick and Losos (1999).
is the significant and positive relationship between surface diameter and maximal speed within each species (Fig. 3), with the exception of A. valencienni. Regression slopes ranged from 0.056 (A. valencienni) to 0.445 (A. gundlachi). An overall ANCOVA revealed significant differences among slopes of the eight species (F7,20 5 3.2, P , 0.025). Of the 28 possible comparisons of slopes between species, one was significant at P , 0.01, and eight were different at P , 0.05. Two species (A. gundlachi and A. valencienni) accounted for all of these significant differences, whereas the remaining six species did not differ significantly in sprint sensitivity. Thus, the eight slopes among the species can be divided into three categories: low (A. valencienni), medium (A. grahami, A. lineatopus, A. sagrei, A. carolinensis, A. evermanni, and A. angusticeps), and high (A. gundlachi). Hereafter, the slope between surface diameter and speed will be referred to as sprint sensitivity as it defines both the degree to which each species declines in performance across different habi-
281
tats, and also is an indirect measure of performance breadth. A key finding from the focal observations was that initial sightings did not always accurately reflect the entire distribution of perch diameters that a species used. In particular, initial perch diameters tended to underestimate the amount of time two species (A. valencienni and A. angusticeps) used narrow (0–2 cm diameter) perches. For example, only 44% of the individual A. valencienni were initially sighted on perches between 0 and 2 cm, but this species spent 71% of its time on perches of this size class. This discrepancy occurred because A. valencienni was frequently initially sighted on broad perches (e.g., trees), but subsequently would move onto narrow branches where they are less easily detected. This finding underscores the importance of quantifying the entire distribution of perch diameters by filming animals. The eight species also differed significantly in the percentage of time they spent on different perch diameters. For example, the two twig anoles, A. valencienni and A. angusticeps, spent most of their time (71% and 42%, respectively) on perches #2 cm in diameter. By contrast, the trunk-ground anoles spent only 19% (A. lineatopus), 21% (A. gundlachi), and 31% (A. sagrei) of their time on perches #2 cm in diameter (the trunk-crown anoles tended to be intermediate in both performance and habitat characteristics). Evolutionary tests also showed that habitat breadth (Fig. 4C) and the percentages of time each species spent on narrow perches #2 (Fig. 4A), or #3 (Fig. 4B) cm in diameter were significantly and negatively correlated with sprint sensitivity. Thus, species that sprint relatively poorly on narrow dowels (high values of sprint sensitivity) spend little time on narrow perches. Further, species whose sprint capabilities are not strongly affected by dowel diameter (broad performance breadth) tend to utilize a broader range of perch diameters in nature than species that do not sprint well on dowels of different diameters. These findings are consistent with both the habitat constraint and habitat breadth hypotheses, but there are several complexities in the data that were not originally predicted by the models. First, although there was a significant relationship between habitat breadth and performance breadth, it would be misleading to state that the anoles with the greatest habitat breadths (the twig anoles) are habitat ‘‘generalists.’’ These species (A. valencienni and A. angusticeps) spend the majority of their time on narrow perches, but will venture out onto broad perches. This stands in contrast to the trunk-ground anoles (A. gundlachi, A. lineatopus and A. sagrei) that are constrained much more severely to use only very broad perches. Indeed, trunk-ground anoles move on narrow perches with great difficulty, and when encountered on narrow perches in nature, they quickly vacate the perch by jumping, rather than attempting to run at sub-maximal speeds on the perch (Losos and Irschick, 1996). Another approach to the one taken here would be to
282
DUNCAN J. IRSCHICK
FIG. 4. Sprint sensitivity versus (A) the percentage of time each anole species spends on supports #2 cm in diameter, (B) the percentage of time each anole species spends on supports #3 cm in diameter, and (C) habitat breadth. Values are independent contrasts. From Irschick and Losos (1999).
first link performance and habitat use and then derive an index of relatively specialization or generalization. This approach may more effectively test whether some
species are specialists along one niche axis while being generalists along other axes. The relative specialization of the different Anolis species may have resulted from competitive interactions among species. A large body of evidence suggests that interspecific competition may have been a driving force in the diversification of Caribbean anoles (Losos, 1994). Intense interspecific competition should result in extreme specialization (Levin, 1970; Pianka, 1974), and thus one would not expect the presence of habitat generalists in this setting. Therefore, a better test of the habitat constraint and habitat breadth models would be to examine a group in which interspecific competition is not intense, so as to determine whether performance generalists can be true habitat generalists. A key issue in evolutionary biology is trade-offs among morphological and behavioral attributes, which can form an important component of evolutionary diversification (Huey and Hertz, 1984; Webb, 1984; Macrini and Irschick, 1998). Classic studies of trade-offs between morphology and performance in Lepomis sunfish have provided a mechanistic basis for habitat segregation (Lauder, 1983; Mittelbach, 1984; Wainwright et al., 1991a; Wainwright et al., 1991b). Here, a trade-off in sprinting performance appears to partially explain the evolutionary relationships among habitat use and performance. Trunk-ground anoles possess long hindlimbs that result in high-speed locomotion, but impair movement on narrow perches, presumably because of the difficulty of maintaining the lizard’s center of mass directly over the narrow branch. Consequently, trunk-ground anoles achieve the highest speeds on the broadest surfaces, but also decline the most in speed from the broadest to the narrowest surface. On the other extreme, the short foreand hindlimbs of the twig anoles enables them to move effectively on narrow surfaces, but at the cost of slow speeds on broad surfaces. This trade-off between stability and speed has substantial ecological and behavioral implications for anole species. Several lines of evidence suggest that twig anoles rely more on stealth than speed to capture prey and evade predators (Moermond, 1981; Hicks and Trivers, 1983; Irschick and Losos, 1996). Many twig anoles are cryptically colored, rarely display, and move slowly through their habitat to evade detection (Irschick and Losos, 1996). On the other hand, trunkground anoles rely on speed to capture prey and escape predators, and are much more conspicuous in their environment, because of their propensity to perch on large tree-trunks in full view. These behavioral and ecological differences may also explain why trunk-ground anoles actively avoid narrow perches on which their sprinting performance is similar to twig anoles. If absolute speed was most important for capturing prey and escaping predators, then twig and trunk-ground anoles should experience equal success at these tasks in habitats with narrow perches. However, this assumption ignores the fact that each species is accustomed to performing at particular
STUDIES
OF
PERFORMANCE CAPACITY
FIG. 5. A plot of independent contrasts between maximum speed (x-axis) and proportion maximal speed used during field escape (yaxis) for eight anole species. The correlation value is Pearsons’ (six df, P , 0.05). From Irschick and Losos (1998).
levels. Trunk-ground anoles are accustomed to moving at high speeds for many of their daily activities, so a substantial reduction in their maximum sprinting performance (Fig. 3), even if the reduced level is similar to other sympatric species, could result in a reduced ability to capture prey and escape predators. Because trunk-ground anoles do not normally use habitats with narrow perches, it would be difficult to rigorously test this hypothesis in nature. However, enclosure experiments in which trunk-ground anoles were forced to use matrices of narrow perches in the presence of a natural predator or prey could shed light on this issue (e.g., Pounds [1988]). If trunk-ground anoles were less successful at evading the predator or capturing prey in ‘‘narrow-perch’’ environments than in their typical ‘‘broad-perch’’ environment, then this would be consistent with the notion that a reduction in sprinting performance is harmful. Once discovered by a predator, do both the twig and trunk-ground anoles perform at similar levels of maximum performance? One might predict that species with a poor intrinsic capacity would ‘‘compensate’’ by sprinting close to 100% of their maximum performance. Further, species with high maximum capacities may only sprint fast enough to effectively escape a predator. The hypothesis of compensation thus predicts a negative relationship between performance capacity and the percentage of maximum capacity that each species uses. However, species may also behaviorally compensate for their poor performance capacities by either moving less, or escaping into nearby refuges (Bauwens and Thoen, 1981; Martin and Lopez, 1995). On the other hand, each species might either sprint as close to their maximum capacities as possible, or at least there will be no relationship between performance capacity and percent maximum speed used in nature. Either possibility might be correct if predator evasion success is a direct function of speed. The
283
available data support the hypothesis of compensation based on field measurements of escape speeds for the eight anole species (Fig. 5) (Irschick and Losos, 1998). In essence, anoles with limited sprinting capacities used a greater fraction of their abilities than species with greater capacities when escaping from a threat in the field (a human). The theory of compensation also has limited support based on intraspecific studies of sprinting in A. lineatopus, as juveniles generally escape in nature by sprinting to greater proportions of their maximum capacity than adults, who are capable of running at higher absolute speeds (Irschick, 2000b). Overall, these findings are consistent with the notion that there is a ‘‘threshold’’ speed which anoles use for evading predators. The approach outlined here provides a novel departure from traditional performance studies, but, the mechanistic basis for habitat segregation is still not fully resolved. For instance, why do long-legged anoles struggle to run on narrow perches? Why do shortlegged anoles not decline in speed from broad to narrow surfaces? Studies of kinematics and kinetics of both short- and long-legged anoles on both broad and narrow perches would shed light on the mechanistic basis for the documented relationships among habitat use, morphology and performance. In this vein, a much better understanding of the functional problems that anoles face in different habitats would be generated, and the link between habitat and performance would be strengthened. MORPHOLOGY, PERFORMANCE AND BEHAVIOR A key assumption in many studies that relate morphology to performance, or that extrapolate performance from morphology alone, is that behavior is not a substantial confounding factor. Many functional morphologists implicitly assume a direct link between morphology and function (Rudwick, 1964; Dullemeijer, 1974; Lauder, 1995; Lauder, 1996). Thus, an open question in many comparative studies is the degree to which behavior mediates the relationship between morphology and performance. Depending on the performance variable being measured, behavior could exert a profound effect on the relationship between morphology and performance. For example, limb length is widely considered to be directly correlated with maximum speed among animal species, but this assumption ignores the fact that different animal species frequently have different postures, and that posture in many species changes with speed (Gatesy and Biewener, 1991; Fieler and Jayne, 1998; Gatesy, 1999). Quantifying the kinematics of limb movement provides information on the behavioral aspects of locomotion, and provides a test of the assumption that the morphological length of the hindlimbs is proportional to how they are used during locomotion. More generally, quantifying behavior may be particularly important for performance studies because some animals may use their morphological features to enhance performance, while other species may not.
284
DUNCAN J. IRSCHICK
Another unresolved issue is the degree to which behavioral characteristics can predict morphology (Lauder and Reilly, 1996). Most studies have focused on relating morphology to performance, and in many cases, have found strong relationships between them, but an open question is whether morphology is more tightly linked with behavior or performance (Lauder, 1996; Lauder and Reilly, 1996). On the one hand, one might expect that behavior and morphology will be coupled if motor output is intimately related to variation in structure. Alternatively, some studies have shown that differences in structure can result in fundamentally similar motor outputs, leading to little or no relationship between morphology and behavior (e.g., Lauder and Shaffer, 1988). Overall, however, there is little evidence that behavioral traits are more evolutionarily plastic than other traits (Gittleman et al., 1996). Thus, I here highlight the utility of explicitly quantifying morphology, behavior and performance simultaneously by specifically considering several issues. (1) How does behavior affect the relationship between morphology and performance? (2) Can behavior be predicted from morphology? To address these two issues, I discuss studies on the 3-D kinematics of highspeed locomotion in a group of five morphologically and behaviorally distinctive lizard species (Irschick and Jayne, 1999a). In addition to yielding information on the above two issues, this work also sheds light on more basic issues in animal locomotion in several ways. First, most studies of locomotion are carried out at either very slow speeds, or at the walk-run transition in mammals (Taylor and Heglund, 1982; Taylor et al., 1980, 1982; Gatesy, 1991; Reilly and Delancey, 1997a, b). Focusing on the walk-run transition in mammals was necessary for standardizing across species of different sizes, but many kinematic variables change dramatically with speed (Gatesy and Biewener, 1991; Fieler and Jayne, 1998; Gatesy, 1999), thus highlighting the need for more studies that measure kinematics at maximum speeds. Second, nearly all studies of locomotion in ‘‘sprawling’’ tetrapods (salamanders and lizards) have used two-dimensional kinematics, despite the three-dimensional nature of their limb movements (Brinkman, 1981; Ashley-Ross, 1994a, b; White and Anderson, 1994). These first studies were pioneering in establishing the basic kinematics of these poorly understood groups, but three-dimensional studies are clearly needed for both lizards and salamanders. BACKGROUND AND KEY FINDINGS Lizards are an excellent group for examining the evolution of locomotion because they exhibit tremendous diversity in morphology, locomotor mode (bipedal, quadrupedal), and the ability to move at different speeds. Numerous studies have investigated the maximum sprinting speeds of lizards (Garland and Losos, 1994), but far fewer studies have investigated the associated kinematics of locomotion. Lizards have several morphological and behavioral characteristics,
which could enhance their sprinting performance. First, many lizard species have elongated distal tarsal elements particularly on the fourth toe of their hindlimb, which some authors have suggested provides a performance advantage during sprinting (Snyder, 1962). Elongation of distal elements in mammals and other vertebrates is widely considered a specialization for running at high speeds (Coombs, 1978; Hildebrand, 1985; Garland and Janis, 1993). Second, bipedal locomotion is widespread among divergent lizard taxa. Bipedal locomotion of lizards is generally believed to maximize speed and stride length (Snyder, 1962). However, except for Urban (1965), few data are available to test if the kinematics of bipedal and quadrupedal running differ. The lizard species discussed here are the desert iguana (Dipsosaurus dorsalis), the zebra-tailed lizard (Callisaurus draconoides), the Mojave fringe-toed lizard (Uma scoparia), the desert horned lizard (Phrynosoma platyrhinos), and the western whiptail (Cnemidophorus tigris tigris) (Fig. 6). These five species span a wide range of different terrestrial lizard phenotypes, and their phylogenetic relationships are well resolved (Fig. 7). Four of the five species (all except D. dorsalis) are similar in size (see Table 1 of Irschick and Jayne, 1999), but subadult male D. dorsalis were used that were similar in size to these other species. These species also occur sympatrically in large regions of the Southwestern Mojave desert, and have differing degrees of specialization for bipedality and sprinting performance. On the one hand, C. draconoides runs very quickly, frequently runs bipedally in nature, and has many of the morphological characteristics of a bipedal specialist (Irschick and Jayne, 1998; Snyder, 1962). On the other hand, P. platyrhinos is a relatively slow runner, has never been observed to run bipedally, and is morphologically adapted for a cryptic existence (Fig. 6). All five lizard species were induced to run at maximum speeds on a high-speed treadmill, and a total of 23 two- and three-dimensional kinematic variables were measured for each species (Fig. 8) (see Irschick and Jayne [1999a] for details), as well as maximum speeds. DOES BEHAVIOR AFFECT THE RELATIONSHIP BETWEEN MORPHOLOGY AND PERFORMANCE? The five species differ dramatically in both their maximum speeds (Fig. 9) and morphology (Fig. 10). For example, the zebra-tailed lizard (Callisaurus draconoides) typically runs about twice as fast as the horned lizard (Phrynosoma platyrhinos), despite both species being of similar size. These differences in speed are closely linked to differences in stride length, with faster speeds being associated with longer strides (Fig. 9). The lizard species exhibited preferential use of several behaviors that affected performance. These included (a) differential use of the elongated tarsals of their fourth toe to propel themselves during locomotion, (b) increased forward extension of the hindlimbs
STUDIES
OF
PERFORMANCE CAPACITY
285
FIG. 7. A phylogeny of the five lizard species examined in this study from analyses by Estes et al. (1988), Frost and Etheridge (1989), and Reeder and Wiens (1996). For graphical clarity several additional lizard taxa are not shown; hence, none of the groups of species shown in the phylogeny are monophyletic. From Irschick and Jayne (1999a).
FIG. 6. Dorsal views of anesthetized specimens of the five lizard species for which kinematics were analyzed. Note the similarity in overall body size but the considerable differences in body shape. All specimens have the same magnification. From Irschick and Jayne (1999a).
to increase stride length, and (c) increased amounts of knee and ankle extension to facilitate forward extension. Bivariate correlations between morphology and performance revealed several interesting facets of their behavior. The total length of the hindlimb is strongly and positively correlated with stride length (r 5 0.87, P , 0.05), with two species (Callisaurus draconoides and Dipsosaurus dorsalis) having the longest hindlimbs and running at the fastest speeds. Bonine and Garland (1999) have also showed evidence of a positive relationship among species between hindlimb length and maximum speed on a treadmill, although they did not examine individual limb elements. Interestingly, the length of the femur is unrelated to stride length for current study (r 5 0.16, P . 0.25), but the morphological length of the fourth toe (the most distal element of the hindlimb) shows a nearly 1:1 relationship with stride length (r 5 0.96, P , 0.05). These correlations remained significant even after adjusting for the confounding effects of phylogeny via use of the independent contrasts method tested with custommade software by J. Losos (Felsenstein, 1985). These correlations suggest that some species are using portions of their limbs differently from other species. Observations revealed that Callisaurus and Dipsosaurus both actively used their long fourth toes to propel themselves during locomotion by flexing and then pushing off the treadmill with their toe, and during particularly fast locomotion, the heel rarely touched the ground. By contrast, the slowest species, P. platyrhinos moved exclusively via plantigrade locomotion. Thus, the strong correlation between the length of the distal hindlimb elements and performance partly reflects how good performers use their morphological characteristics (long fourth toes) in different ways than species with shorter fourth toes. It is possible that
286
DUNCAN J. IRSCHICK
FIG. 8. Images of five lizard species running at maximum speeds during quadrupedal (first column) and bipedal (second column) locomotion. All lizards are shown at the moment of footfall. From top to bottom in each column: Cnemidophorus tigris, Dipsosaurus dorsalis, Callisaurus draconoides, Uma scoparia, and Phrynosma platyrhinos. No images of bipedal locomotion are shown for P. platyrhinos because this species did not run bipedally.
Phrynosoma was unable to use its fourth toe during locomotion, but this is unlikely, as the fourth toe in this species is not substantially shorter than for D. dorsalis. Both Callisaurus and Dipsosaurus increased their effective limb length by increasing the forward extension of the hindlimb and also increasing the amount of knee and ankle extension. These behaviors allowed both species to achieve greater stride lengths, and hence greater speeds than the other species. Interestingly, only P. platyrhinos showed any resemblance to the prototypical model of a ‘‘sprawling’’ lizard, in which knee and ankle angles are close to 908. The remaining lizard species had knee and ankle angles that were closer to 1308 (Fig. 8), which are similar to angles seen in humans and birds, two groups that are considered to be ‘‘erect.’’ While one cannot directly compare these findings to recent work on the slow– speed locomotion for semi-arboreal Sceloporus lizards (Reilly and Delancey, 1997a, b), the kinematics of Dipsosaurus at slow speeds shows that this species
undergoes a dramatic transformation in locomotor posture from slow (duty factor ,50%) to fast speeds (Fieler and Jayne, 1998). Thus, while some lizard species may be obligately ‘‘sprawling’’ (e.g., Phrynosoma, and possibly Sceloporus), four of the five species in this study exhibited a remarkably erect posture at high speeds, casting doubt on the widespread assumption that lizards necessarily adopt a sprawling posture. Inspection of Figure 10 also reveals that bipedal strides clustered with quadrupedal strides within each species, and that interspecific differences were generally much greater than differences in locomotor mode. This kinematic similarity between quadrupedal and bipedal strides may partly explain why so many lizard species are able to run bipedally (D. Irschick, personal observation), as few adjustments to limb posture during quadrupedal locomotion are needed. Even more surprisingly, species differed in the degree to which performance changed between bipedal and quadrupedal locomotion. In Callisaurus, bipedal strides tended to be about 12% faster than quadrupedal strides, but
STUDIES
OF
PERFORMANCE CAPACITY
287
FIG. 9. Mean (11 SE) values of speed (A) and stride length (B) for five lizard species during maximum speed locomotion. Interspecific differences were significant for both variables. Cd 5 Callisaurus draconoides, Us 5 Uma scoparia, Pp 5 Phrynosoma platyrhinos, Dd 5 Dipsosaurus dorsalis, and Ct 5 Cnemidophorus tigris.
in several other species (Uma, Dipsosaurus, and Cenmidophorus), the performance differences between the two modes were negligible. Field studies have shown that Callisaurus also exhibits stride lengths that are about 12% longer for bipedal compared to quadrupedal locomotion (Irschick and Jayne, 1999b), but field data are not available for other species. Overall, it appears that bipedal locomotion does not uniformly provide a performance advantage for all lizard species, but that for certain specialized species, bipedal locomotion may provide a potentially significant advantage. DOES MORPHOLOGY PREDICT BEHAVIOR? The five species differ significantly in a number of morphological variables. Figure 10A shows the result of a discriminant function analysis including 11 linear morphological variables. These variables were not adjusted for size because the five species are similar in size. DF 1 primarily represents tibia length, which differs significantly among species. DF 2 is a composite variable with high loadings for a number of variables, including tail length, fourth toe, the humerus, ulna, and the pelvic and body widths. While key morphological variables are excellent predictors of performance, morphology appears to be a poor predictor of overall kinematics. Comparisons of
FIG. 10. Discriminant function 1 versus discriminant function 2 from three separate analyses of (A) 11 morphological variables, (B) a total of 23 angular, timing and linear kinematic variables, and (B) 16 angular variables. Each species (N 5 5) was used as a category in the analysis. Each point is either an individual lizard (A), or a stride (B, C). Different symbol shapes represent different lizard species. For panels B and C, filled symbols are quadrupedal strides, and open symbols are bipedal strides. From Irschick and Jayne (1999a).
Malhanalobis distances from discriminant function analyses of both morphology and kinematics (Fig. 10) show that morphological and kinematic variation are not positively correlated among species, either when all kinematic variables (angular and linear) (Mantel randomization test, P . 0.50), or when only angular variables are considered (P . 0.50). One might argue that this result is not surprising, as the functional relationships among many of the 23 measured kinematic
288
DUNCAN J. IRSCHICK
variables and morphology either may not exist, or are weak. In sum, certain behaviors played a key role in enabling certain lizard species to achieve high levels of performance, underscoring the importance of quantifying behavioral variables in performance studies. However, while certain morphological variables were excellent predictors of performance, there was no global correlation between morphology and behavior, which may have resulted because of the lack of functional relationships between kinematic and morphological variables. CONCLUSIONS Performance studies have been a stable of functional morphologists and evolutionary biologists for many years, but to a large extent, the commonly used approach of correlating morphology to performance, particularly for studies of maximum speed, may have run its course, although novel approaches will continue to be welcome (e.g., Vanhooydonck et al., 2001). Similarly, eco-morphological studies (Wainwright and Reilly, 1994), while likely to remain valuable in the general area of community ecology, will need to be integrated with more functional information to provide general insights into adaptation. In general, too much emphasis has been placed on the functional relationships between morphology and performance at the exclusion of information on the ecology and behavior of organisms. In this vein, I briefly outline several unresolved areas for performance studies that extend this already productive approach, and relate directly to the examples discussed above. First, more studies that explicitly quantify performance in nature are needed, particularly those that simultaneously link field performance to both traditional laboratory measures and fitness. A glaring weakness of the first example mentioned here was the lack of fitness information regarding sprinting performance in Anolis lizards, which is currently being investigated (D. Irschick, research in progress). A recent review of field studies of locomotion shows that many organisms exhibit behaviors in nature that are not apparent in laboratory settings, resulting in fundamentally different levels and kinds of performance in natural settings (Irschick and Garland, Jr., 2001). For example, recent studies on the sand dune dwelling lizard Uma scoparia show that this species displays a bimodal distribution of speeds in nature, in which the slow-speed locomotion occurs around vegetation and other refuges, and the high-speed movements typically occur in open areas (Jayne and Irschick, 2000). Surprisingly, the mean of the high-speed field mode was approximately 75% of the maximum speed of this species (Jayne and Ellis, 1998; Jayne and Irschick, 2000). Thus, in contrast to the expectation that many animal species move slowly about their habitats when undisturbed, the majority of movements for Uma scoparia were extremely fast and showed striking relationships with the habitat. This example showcases the potential influence of the struc-
tural environment on performance, and emphasizes that studying the effects of habitat on performance is best accomplished in nature, where technically feasible. Second, more studies are needed that draw a direct mechanistic link between habitat use, performance and morphology. For example, few studies have directly tested either the habitat constraint or habitat breadth models, in part because the functional relationship between the habitat and performance is poorly understood for most animal groups. However, these models offer a testable and rigorous method for testing whether species have specialized to different environments. Indeed, where mechanistic approaches have been applied, substantial progress has been made in understanding why species use different habitats, such as in Lepomis sunfish and Anolis lizards. However, the necessary requirements for establishing such a mechanistic link is for biologists to have both a substantial laboratory and field component to their research, which currently is not a top priority for most functional morphologists. ACKNOWLEDGMENTS I thank the organizers of this symposium, M. Ashley-Ross, L. Ferry-Graham, and A. Gibbs for discussions and advice, and two anonymous reviewers for helpful comments. This paper was supported by a grant from the National Science Foundation (IBN 9983003). REFERENCES Aerts, P., R. Van damme, and B. Vanhooydonck. 2000. Lizard locomotion: How morphology meets ecology. Neth. J. Zool. 50: 261–277. Arnold, S. J. 1983. Morphology, performance and fitness. Amer. Zool. 23:347–361. Ashley-Ross, M. A. 1994a. Hind limb kinematics during terrestrial locomotion in a salamander (Dicamptodon tenebrosus). J. Exp. Biol. 193:255–283. Ashley-Ross, M. A. 1994b. Metamorphic and speed effects on hind limb kinematics during terrestrial locomotion in the salamander (Dicamptodon tenebrosus). J. Exp. Biol. 193:285–305. Bauwens, D. and C. Thoen. 1981. Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara. J. Animal Ecol. 50:733–743. Brinkman, D. 1981. The hind limb step cycle of Iguana and primitive reptiles. J. Zool. 181:91–103. Bonine, K. E. and T. Garland, Jr. 1999. Sprint performance of phrynostomatid lizards, measured on a high-speed treadmill, correlates with hindlimb length. J. Zool., (Lond.) 248:255–265. Coombs, W. P. J. 1978. Theoretical aspects of cursorial adaptations in dinosaurs. The Q. Rev. Biol. 53:393–418. Diamond, J. M. 1992. The red flag of optimality. Nature 355:204– 206. Dullemeijer, P. 1974. Concepts and approaches in animal morphology. Van Grocum Press, Van Gorcum. Emerson, S. B. and S. J. Arnold. 1989. Intra- and interspecific relationships between morphology, performance, and fitness. In D. B. Wake and G. Roth (eds.), Complex organismal functions: Integration and evolution in vertebrates, pp. 295–314. John Wiley, New York. Estes, R., K. de Queiroz, and J. Gauthier. 1988. Phylogenetic relationships within Squamata. In R. Estes and G. Pregill (eds.), Phylogenetic relationships of the lizard families, pp. 119–282. Stanford University Press, California.
STUDIES
OF
PERFORMANCE CAPACITY
Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Natur. 125:1–15. Fieler, C. L. and B. C. Jayne. 1998. Effects of speed on the hindlimb kinematics of the lizard Dipsosaurus dorsalis. J. Exp. Biol. 201: 609–622. Frost, D. R. and R. Etheridge. 1989. A phylogentic analysis and taxonomy of iguanian lizards. Misc. Publ. Univ. Kansas 81:1– 65. Garland, T., Jr., E. Hankins, and R. B. Huey. 1990. Locomotor capacity and social dominance in male lizards. Func. Ecol. 4:243– 250. Garland, T., Jr. and C. M. Janis. 1993. Does metatarsal/femur ratio predict maximal running speed in cursorial mammals? J. Zool., London 229:133–151. Garland, T., Jr. and J. B. Losos. 1994. Ecological morphology of locomotor performance in squamate reptiles. In P. C. Wainwright and S. M. Reilly (eds.), Ecological morphology integrative organismal biology, pp. 240–302. The University of Chicago Press, Illinois. Gatesy, S. M. 1991. Hind limb movements of the American alligator (Alligator mississippiensis) and postural grades. J. Zool., London 224:577–588. Gatesy, S. M. 1999. Guineafowl hind limb function. I: Cineradiographic analysis and speed effects. J. Morph. 240:115–125. Gatesy, S. M., and A. A. Biewener. 1991. Bipedal locomotion: Effects of speed, size and limb posture in birds and humans. J. Zool., London 224:127–147. Gittleman, J. L., C. G. Anderson, M. Kot, and H. K. Luh. 1996. Phylogenetic lability and rates of evolution: A comparison of behavioral, morphological and life-history traits. In E. P. Martins (ed.), Phylogenies and the comparative method, pp. 415– 422, Oxford University Press, New York. Herrel, A., J. Meyers, and B. Vanhooydonck. 2001. Correlations between habitat use and body shape in a phrynostomatid lizard. Biol. J. Linn. Soc. 74:305–314. Hicks, R. A. and R. L. Trivers. 1983. The social behavior of Anolis valencienni. In A. G. J. Rhodin and K. I. Miyata (eds.), Advances in herpetology and evolutionary biology: Essays in honor of Ernest E. Williams, pp. 575–595. Museum of Comparative Zoology, Massachusetts. Huey, R. B. and A. F. Bennett. 1987. Phylogenetic studies of coadaptation: Preferred temperatures verus optimal temperatures of lizards. Evolution 41:1098–1115. Huey, R. B. and P. E. Hertz. 1984. Is a jack-of-all-temperatures a master of none? Evolution 38:441–444. Huey, R. B. and R. D. Stevenson. 1979. Integrating thermal physiology and ecology of ectotherms: A discussion of approaches. Amer. Zool. 19:357–366. Irschick, D. J. 2000a. Comparative and behavioral analyses of preferred speed: Anolis lizards as a model system. Phys. Biochem. Zool. 73:428–437. Irschick, D. J. 2000b. Effects of behaviour and ontogeny on the locomotor performance of a West Indian lizard, Anolis lineatopus. Func. Ecol. 14:438–444. Irschick, D. J. and T. Garland, Jr. 2001. Integrating function and ecology in studies of adaptation: Investigations of locomotor capacity as a model system. Ann. Rev. Ecol. Syst. 32:367–396. Irschick, D. J. and B. C. Jayne. 1998. Effects of incline on speed, acceleration, body posture, and hindlimb kinematics in two species of lizard, Callisaurus draconoides and Uma scoparia. J. Exp. Biol. 201:273–287. Irschick, D. J. and B. C. Jayne. 1999a. Comparative three-dimensional kinematics of the hindlimb for high-speed bipedal and quadrupedal locomotion of lizards. J. Exp. Biol. 202:1047– 1065. Irschick, D. J. and B. C. Jayne. 1999b. A field study of effects of incline on the escape locomotion of a bipedal lizard, Callisaurus draconoides. Phys. Biochem. Zool. 72:44–56. Irschick, D. J. and J. B. Losos. 1996. Morphology, ecology, and behavior of the twig anole, Anolis angusticeps. In R. Powell and R. W. Henderson (eds.), Contributions to West Indian herpetology: A tribute to Albert Schwartz, pp. 291–301. Society for the Study of Amphibians and Reptiles, Ithaca.
289
Irschick, D. J. and J. B. Losos. 1998. A comparative analysis of the ecological significance of maximal locomotor performance in Caribbean Anolis lizards. Evolution 52:219–226. Irschick, D. J. and J. B. Losos. 1999. Do lizards avoid habitats in which performance is submaximal? The relationship between sprinting capabilities and structural habitat use in Caribbean anoles. Am. Nat. 154:293–305. Irschick, D. J., L. J. Vitt, P. A. Zani, and J. B. Losos. 1997. A comparison of evolutionary radiations in mainland and Caribbean Anolis lizards. Ecology 78:2191–2203. Jackman, T. R., A. Larson, K. De Queiroz, and J. B. Losos. 1999. Phylogenetic relationships and tempo of early diversification in Anolis Lizards. Syst. Biol. 48:254–285. Jayne, B. C. and R. V. Ellis. 1998. How inclines affect the escape behaviour of a dune dwelling lizard, Uma scoparia. Anim. Behav. 55:1115–1130. Jayne, B. C. and D. J. Irschick. 2000. A field study of incline use and preferred speeds for the locomotion of lizards. Ecology 81: 126–140. Larson, A. and J. B. Losos. 1996. Phylogenetic systematics of adaptation. In M. R. Rose and G. V. Lauder (eds.), Adaptation, pp. 187–220. Academic Press, San Diego. Lauder, G. V. 1983. Functional and morphological bases of trophic specialization in sunfishes (Teleostei, Centrarchidae). J. Morph. 178:1–21. Lauder, G. V. 1995. On the inference of function from structure. In J. J. Thomason (ed.), Functional morphology in vertebrate paleontology, pp. 1–18. Cambridge University Press, Cambridge. Lauder, G. V. 1996. The argument from design. In M. R. Rose and G. V. Lauder (eds.), Adaptation, pp. 187–220. Academic Press, San Diego. Lauder, G. V. and S. M. Reilly. 1996. The mechanistic basis of behavioral evolution: Comparative analysis of muscoskeletal function. In E. Martins (ed.), Phylogenies and the comparative method in animal behavior. pp. 105–137. Oxford University Press, Oxford. Lauder, G. V. and H. B. Shaffer. 1988. Ontogeny of functional design in tiger salamanders (Ambystoma tigrinum): Are motor patterns conserved during major morphological transformations? J. Morph. 197:249–268. Leroi, A. M., M. R. Rose, and G. V. Lauder. 1994. What does the comparative method reveal about adaptation? Am. Nat. 143: 381–402. Levin, S. A. 1970. Community equilibria and stability, and an extension of the competitive exclusion principle. Am. Nat. 104: 413–423. Lister, B. C. 1981. Seasonal niche relationships of rain forest anoles. Ecology 62:1548–1560. Losos, J. B. 1990. Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: An evolutionary analysis. Ecol. Mon. 60:369–388. Losos, J. B. 1994. Integrative approaches to evolutionary ecology: Anolis lizards as model systems. Ann. Rev. Ecol. Syst. 25:467– 493. Losos, J. B. and D. J. Irschick. 1996. The effect of perch diameter on escape behaviour of Anolis lizards: Laboratory predictions and field tests. Anim. Behav. 51:593–602. Losos, J. B., T. R. Jackman, A. Larson, K. De Querioz, and L. Rodriguez-Schettino. 1998. Historical contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–2118. Losos, J. B. and B. Sinervo. 1989. The effects of morphology and perch diameter on sprint performance of Anolis lizards. J. Exp. Biol. 145:23–30. Macrini, T. E. and D. J. Irschick. 1998. An intraspecific analysis of trade-offs in sprinting performance in a West Indian Lizard (Anolis lineatopus). Biol. J. Linn. Society 63:579–591. Martin, J. and P. Lopez. 1995. Escape behaviour of juvenile Psammodromus algirus lizards: Constraint of or compensation for limitations in body size? Behavior 132:181–192. Mittelbach, G. G. 1984. Predation and resource use in two sunfishes (Centrarchidae). Ecology 65:499–513. Moermond, T. 1979. Habitat constraints on the behavior, morphol-
290
DUNCAN J. IRSCHICK
ogy, and community structure of Anolis lizards. Ecology 60: 152–164. Moermond, T. 1981. Prey-attack behavior of Anolis lizards. Z. Tierpsychol. 56:128–136. Pennycuick, C. J. 1997. Actual and ‘optimum’ flight speeds: Field data reassessed. J. Exp. Biol. 200:2355–2361. Perry, G. and E. R. Pianka. 1997. Foraging behaviour: Past, present and future. Trends. Ecol. Evol. 12:360–364. Pianka, E. R. 1974. Niche overlap and diffuse competition. Proc. Natl. Acad. Sci. U.S.A. 71:2141–2145. Pough, F. H. 1989. Organismal performance and darwinian fitness: Approaches and interpretations. Phys. Zool. 62:199–236. Pounds, J. A. 1988. Ecomorphology, locomotion, and microhabitat structure in a tropical mainland Anolis community. Ecology 58: 299–320. Pridmore, P. A. 1994. Locomotion in Dromicops australis (Marsupalia: Microbotheriidae). Aust. J. Zool. 42:679–699. Rand, A. S. 1964. Ecological distribution in anoline lizards of Puerto Rico. Ecology 45:745–752. Rand, A. S. 1967. The ecological distribution of the anoline lizards around Kingston, Jamaica. Breviora 272:1–18. Reeder, T. W. and J. J. Wiens. 1996. Evolution of the lizard family Phynosomatidae as inferred from diverse types of data. Herp. Mon. 10:43–84. Reilly, S. M. and M. J. Delancey. 1997a. Sprawling locomotion in the lizard Sceloporus clarkii: Quantitative kinematics of a walking trot. J. Exp. Biol. 200:753–765. Reilly, S. M. and M. J. Delancey. 1997b. Sprawling locomotion in the lizard Sceloporus clarkii: The effects of speed on gait, hindlimb kinematics, and axial bending during walking. J. Zool., London 243:417–433. Ricklefs, R. E. and S. D. Schluter. 1993. Species diversity in ecological communities: Historical and geographical perspectives. University of Chicago Press, Chicago. Rosen, R. 1967. Optimality principles in biology. New York, Plenum Press. Roughgarden, J. 1995. Anolis lizards of the Caribbean: Ecology, evolution, and plate tectonics. Oxford University Press, New York. Rudwick, M. J. S. 1964. The inference of function from structure in fossils. British J. of the Phil. Society 15:27–40. Schoener, T. W. 1968. The Anolis lizards of Bimini: Resource partitioning in a complex fauna. Ecology 49:704–726. Schoener, T. W. 1971. Theory of feeding strategies. Ann. Rev. Ecol. Syst. 2:369–404. Schoener, T. W. and A. Schoener. 1971a. Structural habitats of West Indian Anolis lizards I. Lowland Jamaica. Breviora 368:1–53. Schoener, T. W. and A. Schoener. 1971b. Structural habitats of West
Indian Anolis lizards II. Puerto Rican uplands. Breviora 375:1– 39. Snyder, R. C. 1962. Adaptations for bipedal locomotion of lizards. Am. Zool. 2:191–203. Stephens, D. W. and J. R. Krebs. 1986. Foraging theory. Princeton, Princeton University Press. Taylor, C. R. and N. C. Heglund. 1982. Energetics and mechanics of terrestrial locomotion. Ann. Rev. Physiology 44:97–107. Taylor, C. R., N. C. Heglund, and G. M. O. Maloiy. 1982. Energetics and mechanics of terrestrial locomotion I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J. Exp. Biol. 97:1–21. Taylor, C. R., N. C. Heglund, T. C. McMahon, and T. R. Looney. 1980. Energetic cost of generating muscular force during running a comparison of large and small animals. J. Exp. Biol. 86: 9–18. Thompson, D. B. 1990. Different scales of adaptation in the climbing behavior or Peromyscus maniculatus: Geographic variation, natural selection, and gene flow. Evolution 44:952–965. Urban, E. K. 1965. Quantitative study of locomotion in teiid lizards. Anim. Behav. 13:513–529. Vanhooydonck, B., R. Van Damme, and P. Aerts. 2001. Speed and stamina trade-off in lacertid lizards. Evolution 55:1040–1048. Wainwright, P. C., G. V. Lauder, C. W. Osenberg, and G. G. Mittelbach. 1991a. The functional basis of intraspecific tropic diversification in sunfishes. Functional Morphology, Biomechanics, and the evolutionary Process-Symposium, pp. 515–529. Wainwright, P. C., C. W. Osenberg, and G. G. Mittelbach. 1991b. Trophic polymorphism in the pumpkinseed sunfish (Lepomis gibbosus Linnaeus): Effects of environment on ontogeny. Func. Ecol. 5:40–55. Wainwright, P. C. and S. M. Reilly. 1994. Ecological morphology: Integrative organismal biology. The University of Chicago Press, Chicago. Webb, P. W. 1984. Body form, locomotion and foraging in aquatic vertebrates. Amer. Zool. 24:107–120. Weinstein, R. B. and R. J. Full. 2000. Intermittent locomotion increases endurance in a gecko. Phys. Biochem. Zool. 72:732– 739. Welham, C. V. J. 1994. Flight speeds of migrating birds: A test of maximum range predictions from three aerodynamic equations. Behav. Ecol. Soc. 5:1–8. White, T. D. and R. A. Anderson. 1994. Locomotor patterns and costs as related to body size and form in teiid lizards. J. Zool. 233:107–128. Whittaker, R. H. and S. A. Levin. 1975. Niche: Theory and application. Halsted Press, Pennsylvania. Williams, E. E. 1983. Ecomorphs, faunas, island size, and diverse end points in island radiations of Anolis. In R. B. Huey, E. R. Pianka, and T. W. Schoener (eds.), Lizard ecology: Studies of a model organism. Harvard University Press, Cambridge.
