LocomotorPerformance in SquamateReptiles 241

demographic study andbehavioral observalionin the field. Measurementof per- formance is crucial, and reptiles Ere certainly easier subjectsthan are someother Ecological Morphology of Locomotor vertebrate grcups,such as birds or bats (Ric~lefsand Miles, cha?. 2, this volume; Norberg, cha?. 9, this volume). Performance in Squamate Reptiles The Morphology + Performance -+ Fitness Paradigm Theodore Garland, Jr., and Jonathan B . Losos "Not infrequently,performancecharacteristics, measured as maximalspeed or endurance, make the differencektween eating and being caten" (Tenney, 1967, p. 1-71, The Foregoing quotation certainly contains sometruth, but actual data indicating thefrequencyof"close:ncountesof the worst kind" betweenpredators andpreyare few and farbetween(:f. Castillaand Bauwens, 199.,p. 78;Christian and Tracy, 1981; Hertz et al., 1988;Jayne 2nd Bennett, 1990b). Relationshipsbetween morphology,physiology, or biochemistry, onthe one Studies of ecological morphology impl.citlyconcern fitness and adaptation. hand, and behavior and ecology,on theother, have been widely documented, as Within populations,individual variation in morphology may be related to varia- tion in Darw~nianfitness; . , this volume attests. Such relationshipsprovide aidencethat most, if not all, or- .. . . . ganisms are to some extent"adapted" to their current environment.Quantifying among populationsand highertaxa, morphologi- how well adapted an organism is,or testing the biological and statist~calsignifi- cal variation may indicate adaptztion to diferent lifestyles.Arnold (1983) pro- cance of putative adaptations, may, however, be very difficult (Brooks and posed a conceptual and statisti:al-and hence operational-framework for McLennan, 1991; Harvey and Pagel, 1991; Losos and Miles, chap.4, this vol- using data on individual variaticn to study adaptation within populations (fig. ume). As well, many studies in ecological morphology,and in the conceptually 10.1). This paradigm addresses the questicn of whether naturd selection is cur- related fieldsof phqsiological ecology (Federet al., 1987) and comparative bio- rently actingon morphologyor performance within asingle population. Arnold's chemistry (Hochachka andSomero, 1984), have ignoredthe crucial intermediate (1983) discussion consideredm~ltiple morphological characlers and multiple step of organismal performance (Arnold,1983; Huey and Stevenson, 1979; measures of performance, as well as corrslations within these two levels. He Losos, 1990b)when trying to correlatemorphology with ecology. In this chapter, pointed out that multiple regression and path analysis couldbe used to estimate we review the literaturepertaining to the ecological morphology of locomotor and test the significance ofperformance gradients (quantifyingthe effects of mor- performance in repiles and relate this knowledgeto current paradigms and ana- phology on performance), whichcan be studied in the laboratory (but see Wain- lytical techniques in organismal and evolutionary biology.We will argue that wright, chap 3, this volume), a3d fitness gradients (quantify~ngthe effects of both maximal whole-animalperformame abilities (what an animal can do when performanceon fitness), whichrequire field studies (see alsoEmerson and Ar- pushed to its limits; generallymeasured in the laboratory, and not to be confused nold, 1989; Wainwright, 1991). with ejiciency;see Gans, 1991; Lauder, 1991)and behavior (whatan animal ac- This perspectivesuggests thatintrapopulational variation inmorphologymay tually does when fxed with behavioral options; best measured in the field) must have significant influences on fitness only to the extent that it affects perfor- be considered when attempting tounderstand the mechanistic basesof relation- mance. Measuresof organismal performancecapacities thus become central(cf. ships between morphology and ecologj. Bennett, 1989; Bennett and Huey, 1990; Emerson andAmod, 1989; Pough, Locomotion is inmany ways ideally suited for studiesof ecological morphol- ogy. Most behaviorinvolves locomotion,and measures of both locornotorperfor- mance (e.g.. speec, stamina? andits morphological bases(e.g., limb length, Morphology - Performance - Fitness heart size) come eadyto mind. Somereptiles aregood subjects for measurement t t perfoancegradlent gradlentfitness of locomotor performancein the laborarory(e.g., with racetracks or ireadmills), for quantifyingits morphological, physiological,and biochemicalbases, and for FIGURE10. I Simplified \ersion of Arnold's (1983) original paradigm 242 Theodore Garland, Jr., and Jonathan B. Losos Locomotor Performance in Squamate Reptiles 243

1989).and measuresof locomotorperformance falleasily into the paradigm.The Physiology focus onorganisrnal performanceas pivotal is insharpcontrast tomany previous Morphology - Pedorrnance -Behavior - Fitness Biochemistry studies of locomot~recology, in which the starting point (and sometimes theend- FIGURE10.2 Ex2ansion of Arnold's (19E3)paradigm to include behavior, as proposed by Garland ing point) has been measurementof limb proport.ons(see "Case Studies"below). (1994a). Moreover,the realization that it is easier to studyone or the other rather than both gradients simultaneously, andthat both parts of the equation are of interest, has stimulated researc?. Garland et al., 1990a; Gatten et al., 1992: Gleason, 1979a; Hertz et al., 1988; Physiological2nd biochemical traits may be included within the category of MacArthur, 1992; Morgan, 1988; Pough et al., 1992; Seymour,1982, 1989; van "morphology," and we will subsequently usemorphology as shorthand for all Berkum et al , 1986, Wyneken and Salmor,,1992.) Thus, morphology limitsor- three types of traits. This is not to implythat morphology, physiology, and bio- ganismal peiormance,which in turn constrains behavior, andnatural and sexual chemistry are eq~ivalent,nor are we trying to deny the distinction between selection actmost directly on bel-avior-what an animal actually does (Garland, "form" and "funct~on."The point is simply that all three types of traitsare (gener- 1994a).This modification of Arnold's(1953) original paradigm adds one more ally) at a level of biological organization belowthe whole-organism,and all may level of analysis and placesspec~fic emphasis on behavior astie focus of selec- influence organisrnalperformance. Calling all three types of traits "morphology" tion. Behavior is seen as a potential "filter" between selectionand performance serves to emphasizethat similar tools and approachesare useful for sludying their (Garland et al., 1990b). effects on organismalperformance (cf. Wainwright, 1991 ). Further Extensionsof the Paradigm Arnold's (l98?) paradigm was designed spe:ifically to interface with multi- variate quantitativz genetics theory (Landeand Arnold, 1933).In thequantitative Inserting sehavior betweenperformanc: and fitness seems relatively straight- genetic frameworc (e.g., Boake, 1994; Brodie and Garland, 1993; Falconer, forward (fig. 10.2).But this add~tiondoes not necessarily mean the paradigm is 19891, adaptive phenotypic evolutior consistsof two parts: natural selection, completeor general. Many morepossible links can be imagine'l,and a relatively which is a purely phenotypic phenomenon,and genetic response,which involves simple chainrapidly becomesa complicatedweb (e.g., fig. 10.3). inheritance. Some do not like this se~arationof selectionand inheritance (e.g., In particular, habitat, broadly defined, is another important factorwhich may Endler, 1986), bur we agree with Lande and Arnold (1983) that it has consider- influence be~avior,performance capabili:ies, and even morphology (see also able operational advantages inallowing the twoelementsto be studied indepen- Dunson andTravis, 1991;Huey. 1991). For example, availab~lityof perches or dently. It also emphasizes thatselection may be futile; if a trait is not heritable, basking sites, their size, and their distribution may affect both what an animal then selection can7ot lead to or improve adaptation. does (e.g.,Adolph, 1990b;Grant, 1990; Moermond, 1986; Pounds, 1988;Wald- schmidt andTracy, 1983; see discussion of the "habitat matnx" model below) How Does Behavior Fit into the Paradigm? and what it is capable of doing (s.g., sprint speed in lizards is affected by perch The place of behaviorin the paradigm of figure 10.1 is ambiguous. Arnold diameter anc substrate: Carothe~s,1986; Losos and Sinervo, 1989; Losos et a]., (1983) did not mention behavior as a distinc: level; subsequently, however, 1993; Miles and Althoff, 1990;Sinervo adLosos, 1991). Temperatureis a hab- Emerson and Arnold (1989;also Schluter, 1980) have included behavior within itat characteristic thatmay affect performance indirectly thrcugh its effects on the categoryof mrrphology. We offer an alternat~vecategorization, as depicted in various physiological processes, and by laving direct influexes on behavior, figure 10.2(modi!ied from Garland, 1994a). such as the switchesin defensive behaviorat low body tcmpcmturc thatoccur in Many b~ologistsimagine that selection acts most directly onwhat an an~mal some lizards and snakes (Arnold and Bennett. 1984; Crowley and Pietruszka, actually does in nature, that is, its behavior. Performance,on the other hand, as 1983; Hertzst al., 1982;Mautz et al., 1992. Van Darnme, Bauwenset al., 1990; defined operationally by laboratory measurements,generally indexes an ani- Schiefflen and de Queiroz, 1991). Temperature affects locomotorperformance mal's ability to dn something when plshed to its morphological, physiological, both in absolute terms (Bauwenret al., in press; Bennett, 199C;Garland, 1994b) or biochemical limits.(Whether animals routinely behaveat or near physiologi- and, to a lesser extent, relative to other individuals or species. Individualdiffer- cal limits under natural conditions is an impcrtant empirical issue for which ences in locomotor performance areconsistent across temperatures (i.e., fast in- precious few dataexist:Daniels and Heatwole, 1990;Dial, 1987; Garland, 1993; dividuals tend to be fast at all temperatures),but not perfectly so (references in 244 TheodoreGarland, Jr., and Jonathan B. Losos Locomotor Performancein SquamateReptiles 245

Interspecific any populat.on (Emerson and Arnold, 1989).Second, tothe extentthat different Interactions morphologizsfunction best in different habitats, then naturalselection will tend to favortheir evolution in the ap?ropriatehabitats. If one has an understandingof which morphologies are bestsu.ted in given habitats (basedon biomechanical or Morphology-+ Performance -+ Behavior -+ Fitness functional analyses, including cptimality models,or on empirical studies of nat- ural selecticn within populations),then one can testthe prediction that taxa have adapted to different envir0nmer.t~(Baum andLarson, 1991 ; Bock and von Wah- lert, 1965; Losos and Miles, chap. 4, this volume). Caution must be exercised FIGURE10.3 Inclusion of some other factorsthat may affec:elements of Arnold's (1983) paradigm. when taking this view, however, as we have little empirical evidencethat any Habitat characteristics, suchas temperature, may affect basc physiolog~caland biochemical given trait(s) in any given popu.ationwill have reached its selectiveoptimum by properries as well as behavior (see text). (Of course, behavior and physiology may affect an the time westudy it (Arnold, 1987; Ware, 1982). Moreover,multiple (sub)opti- animal's body temperature; the present diagram is extremely simplified.) ma1 solutions, whichconfer equivalent fitness, may exist (Denny,chap. 8, this volume; Feder et al., 1987; Ware, 1982) depending on the shape of the fitness Bennett, 1990; Bennettand Huey, 1993). Thus, he temperatureat which an indi- surface, movement fromone peak to anothermay be difficult. vidual happensto be when it encounters a predatormay affect its relative fitness Althougn Arnold (1983)suggested path analysis for study ng the causes(per- (e.g., Christianand Tracy, 19811, and individualdifferences in thermoregulatory formance gradients, e.g., fig. 10.5 below) and consequences(fitness gradients) behavior may become crucial (cf. Christian et al , 1985;Waldschmidt and Tracy, of individuslvariation in performance(and behavior),path analysis mightalso be 1983). employed to study species-level sclcction processes(cf. Emerson and Arnold, More subtle habitat effects are also possible Food in {hestomach (Fordand 1989). For example, ratherthan values for individuals, datapints could be pop- Shuttlesworth, 1936; Garland and Arnold, 1983; Huey eta!., 19841,nutritional ulation, species, or clade means for morphological, performance, behavioral,or state (for experimentswith mammals, seeBrooks and Fahey, 1984,and Astrand ecologicaltraits. As componentsof the "fitness" of a population, speciesor clade and Rodahl, 1986), hydrational stat2 (Moore and Gatten, 1989; Preest and (cf. Futuyma, 1986;Vrba, 1989), one might consider geographicrange (cf. Jab- Pough, 1987; Wilson and Havel, 1989, but see Crowley, 1985b; Gatten and lonski, 1985), evolutionarylongevity, andlor number of descendant populations Clark, 1989; Stefanski et al., 1989), as well as disease or parasite infection or species (thelatter might require palecntologicalinformat~on; but see Nee et (Schall, 1986,1990; Schall et al., 1932: but see Daniels, 1985b) all may affect al., 1992). Alternatively, some measureof a population's or of a species' "fit- performance ability. Hydrational (Crowley, 1987; Federand Londos, 1984; ness" or "adaptedness" (Michod, 1986) ts its current environment might alsobe Pough et al., 1985; Putnam andHillman, 1977)ornutritional state may also af- possible, s~chas physiological tolerances, breadth of the Grinnellian niche fect activity levels,that is, behavior. Inter- and intraspecific interactionscan also (James et d., 1984), or demographictraits (e.g., population density, intrinsic affect behavior in numerous ways (e.g., Fox et al., 1981; Garland et al., 1990a; rate of natural increase: cf.Baker, 1978;Birch et al., 1963).To quoteStini ( 1979, Henrich and Bartholomew, 1979; Schall and Dearing, 1987; Stamps,1984). p. 388): "A well-adapted population wouldbe . . . one thatenjoys a relatively Even hydrationalor thermalconditions during incubationor pregnancycan affect high probability ofsurvival under conditionshighly likelyto occur." Of course, a locomotor performance of offspring (Milleret a]., 1987; Van Damme et al., path analysis ofcomparative data would requireproper allowancefor phylogene- 1992). tic non-independence (seebelow). As noted by Emerson and Arnold (1989, p. 302), "there are no strong theoretical grounds for expec:ing similar perfor- Extending the Paradigm to Population and Species Variation mance topographiesat the intri- and interspecific levels andthere has been vir- The paradigm in figure 10.2 can also be applied to understand or predict a tually no empirical exploration." relationshipbetween morphology andhabitat use among populationsor species. Does Morphology Affect Fitness Directly? The logic of this extension isas follows. First, to the extent that morphological differences among individualswithin populationslead to differences in perfor- Regardless of how complicateda paradigm one wishes 10 consider, an out- mance abilities that affect fitness, then, assuming the absence of constraints standing conceptualand empirical issue is whether directpaths exist from mor- (Maynard Smithet al., 1985), the most "fit" morphology should evolve within phology to fitness (fig. 10.4). Returning to the original formulation, themost 246 TheodoreGarland, Jr., and Jonathan B. Losos Locomotor Performance in SquamateReptiles 247

Interspecific come of an agonistic interactionbefore any actual fightingoccurs. This example Interactions suggests a direct effect of am~rphological trait (body size)on behavior, and hence on a component offitness (dominance rank). Some m~ghtconsider it 1ogi;ally impossible thatmorpho ogy can affect fit- Morphology -+ Performance -+ Behavior ---t Fitness ness other than through its effects on organismalperformance(and hence behav- ior). The idea is that form only matters if it affects function and hence performance; otherwise, morphological variationis selectively neutral. We would prefer to consider theabsence of direct morphology-+ fitness paths as an hypothesis,subject to empirical test. Such tests might involve measurement of vertebral numbers (in snakes) or limb length (in lizards), as well as locomotor FIGURE10.4 An outsandingconceptual and empiricalissre is whetheranydirect paths from performance and survivorship(cf. Arnold andBennett, 1988; Iayneand Bennett, morphologyto fitnessaresignificant (see text). 1990b; Tsuji et a]., 1989). A significantpath from morphologyto (a component of) fitness (Sg. 10.4) would incicate eithera direct effectof morphology on fit- general path model is one in which all possiblz effects are depicted, including ness or the presence of some unmeasured (latent)performance variable. those directly from morphology to firness (Arrold [1983, fig. 31 omitted these paths). Consider some hypotheticalpossibilities. Some individual gartersnakes are born with a sixgle or no eyes, an external heart, or a severely kinked tail or Interpopulation spine (Garland, 1988, pers. obs.; Arnold and Bennett, 1988, pers. comm.). Although analyses relating morphology,performance, behavior, and fitness These morpholog:caldeformities greatly impai: locomotor capacities, whichin (broadly defined) most commonlyinvolve interspecificcomparisons (to be dis- turn limit behavioral options (as compared with "normal" individuals), and cussed below) or, more recentlj, individual variation, studiesof interpopulation would certainlyhave fitness consequencesin nature. In this case, a direct path differences are essential to evdutionary analyses (Garlandad Adolph, 1991; from morphologyto fitness seems unnecessary. James, 1991). Most previous studies of population (geographic) variationfocus But contemplate two other examples.First, all else being equal (i.e., as- on morphornetricor allozymic characters(e.g., Zink, 1986), dthough studies of suming behavioris unaffected), an albino snakewill likely suffer afitness decre- variation in mitochondria1 DNA are now common (e.g., Avise et al., 1987; ment relativeto a normally pigmentedindividual, becausethe former will more Lamb et a]., 1989). Consequently, phylogeneticanalyses of ppulationdifferen- likely be discoveredand eaten by a predator prior to its reproduc~ng.Thus, a tiation cannot be far off (cf. Schluter,1989; Snell et al., 1984),and we encourage direct path appears to exists from morphology (pigmentation)to fitness. Alter- such studies of population differences inlocomotor performance andits corre- natively, if one considers some measure of crypsis as a "performance" variable, lates. If possible, such studies should include a "common garden" approach, in then albinism acts through its effects on cryps.s (cf. King, 1992), and perfor- which animnls are raised in the laboratoryfor at least one generationto maximize mance, but not morphology,would se-m to have a direct path to fitness, bypass- the probability that observed phenotypis differences are actually genetically ing behavior. But, if an animal could somehow become "aware' that it was based (Garland and Adolph, 1991). Common garden control;are important for differently colored and so alter its behavior to compensate (cf.Morey, 1990). studies of differentspecies as well, although mostbiologists seem less concerned then the effect of albinismmight be entirely throughthe performance- behavior at this level.Population differences in locomotor performancemay be consistent link. Albinismwould also affect thermoregulat.on,making it more difficultfor across years (Huey and Dunham, 1987), but year-to-year variationin perfor- the snaketo warmby basking, hence causingit to bask forlonger periods of time mance exists (Huey et al., 1990) and may confound attempts to correlate mor- and increasing its exposure to predators (cf. Andren and Nilson, 1981). phology with ecology(cf. Wier.s and Rotznbeny, 1980). Second,in mary species,body size affectsthe outcomeofintraspecific behav- Intrapopulation: Individual, Ontogenetic,and Sexual Variation ioral interactions (Tokarz, 1985;references in Garland eta]., 1990a; Faber and Baylis, 1993). This effect may occur simply because size affects strengthand Arnold (1983, fig. 10.1) considered studiesof individual variation within stamina, and hence performanceat fighting.Butin somecases differences in size populations, includingeffects or morphology on performance(e.g.,mechanistic alone may influenze decisions to fight or not, a1.d hence may determine theout- physio1ogy)andthe effects of performanceon fitness (e.g.,direct studiesof natu- 248 Theodore Garland,Jr., and Jonathan B. Losos Locomotor Performancein Squamate Reptiles 249 ral selection in ths wild). Quite a few such stuciesof reptilian locomotion have 1987), all studies to date have bund sign:ficantamong-family varlance for mea- been completed since 1983. A major conclusior.of these studies isthat measures sures of locomotor performancein reptiles. of locomotor performanceshow sub~tantialand repeatable individual variation within single pop~lations(Bennett, 1987; Bennettand Huey, 1990;Huey et al., Experimental Approaches 1990; Jayneand Eennett, 1990a;see also Djawcan, 1993;Friedmanetal., 1992, Experimental approachescan be usedin several ways, forexample:(I) to ex- on mammals). This variation and repeatability is, of course, a prerequisite for aminethe mechanistic basesof performancevariation; (2) to mimic the effects of attempts to quantifyrelationships between morphologyand performance(perfor- short- or long-term changes that may ocxr naturally withinindividuals; (3) to mance gradients) or betweenperformance and behavior, fitness or ecology examine the effect of conditions duringdevelopment on morphology and perfor- (e.g., fitness gradients). mance abil~ties;and (4) to increase the range of variation in organismal perfor- One advantageof studying individual variationis that phylogenetic effectsare mance and so increase statistizal power to detect its ecolo~icaland selective not a concern. So,for example,the effects of body size can be studied by examin- importance. Experimental app-oacheshave the advantage that they can isolate ing an ontogenetic series(e.g., Garland, 1984,1985; Jayne and Bennett, 1990a; and studythe effectsof variatio? in one variable independentof correlationswith Pough, 1977, 1978) rather than multiple species. Similarly, the mechanistic other variables (cf. Lande and Arnold, 1983;Mitchell-Olds and Shah, 1987; correlates of performance variationcln be studied (e.g.,Garland, 1984, 1985; Slinker anc Glantz, 1985; Wade and Kalisz, 1990). Experimental approaches Garland and Else. 1987; Losos et al., 1989; Tsl~jiet al., 1989) without concern have been underutilized for analyzing links in the morpholog;~-+ locomotorper- that phylogeneticeffects may confound the results (cf. Losos, 1990a, b, c). formance+ behavior-+ fitness chain (orweb) and in ecomorphologyin general QuantitativeGenetic Analysis (but see Benkman and Lindholm, 1991 Carothers, 1986; Hanken and Wake, 1991; Hillnan and Withers, 1379; Hueg et al., 1991; James, 1991; Jayne and Individualswithin a population may not provide statisticallyindependent data Bennett, 1589; Lauder and Reilly, 1988;Ruben et al., 1987;Webster and Web- points, becausethey are related tovarying extents.Quantitative genetics uses this ster, 1988). fact to partition observed phenotypicvariances 2nd covariancesintogenetic (due Causal mechanistic relationships suggestedby correlatiie studies of indi- to inheritance,which is analogous to phylogeneticdescent; cf. Lynch, 1991) and vidual variation in locomotor abilities (fig. 10.5:e.g., Garland and Else, 1987; environmental sources,each of which can be more fine:y partitioned (Boake, Gleesonand Harrison, 1988;John-Alder, 1984a, b, 1990)canbe tested with such 1994; Brodieand Garland, 1993;Falconer, 1983;Garland, 1994a). physiological techniquesas blood doping (cf. Withers and Hillman, 1988),but Quantitativegenetic analyses arenot a traditionalpart of ecological morphol- this has scarcely been attempted in reptiles (Gleeson, 1991). Hormonal (John- ogy. They must become an integralpart, however, if we are to movc towards an Alder, 1990; Joos and John-Alder, 1990,Moore and Marler, 1987; Moore and understandingof hemechanisms of microevolution.We will not consider quan- Thompson,1990) or pharmacoiogical (e.g., John-Alderet al., 1986b)manipula- titative geneticanalyses ofreptilian locomotor performancein detail. Only a few tion to change metabolismand performance is also possible. (Levels of some studies have been completed, all on garter snakes (Thamnophis) or lizards hormonesfluctuate rapidly in reptiles, wtereas some measures oflocomotor per- (Sceloporus,Laccrta; reviews in Bennett andHuey, 1990;,Brodie and Garland, formanceare quite repeatable,which suggests thatthe former may have little ef- 1993; Garland, 1994a). All studies to date have relied on analyses of presumed fect on the .atter.) With respectto morphology, the importance of tail length and full-siblingfamiliss to estimate heritabilities. For many reptiles, gravid females loss, toe loss, toe fringes, and skin flaps forsprinting andgliding performancein can be captured ir relatively large numbersin the field. After offspring are born lizards and snakeshas also been assessed experimentally(e.g., Arnold, 1984a; or hatched in the laboratory, measurements oflocomotor performanceare made Carothers, 1986; Daniels et al., 1986; Formanicwiz et al., 1990; Huey et al., on each. Unforturately, heritabilityestimates from sets of full-siblingsrepresent 1990;Jayne and Bennett, 1989:Losos et a]., 1989;Marcellini and Keefer, 1976; neither a "narrow-sense" nor a "broad-sense" heritability;in addition, multiple Pond, 1981). paternity willlead to an underestimationof additivegenetic effectsin full-sibling Within-.ndividualvariation in reptilian locomotor performance has been ex- data sets (Brodieand Garland, 1993; Falconer, 1989; Garland, 1994a; Schwartz amined as a consequenceof seheral facto-s, such as physical conditioning(train- et al., 1989).Thus, significant among-familyvariance in studies of full-siblings ing), feeding, reproductivestate, and hormonal state. Physical conditioning suggests heritability, but does not prode it. With one exception (Bauwenset al., studies of the type so common in mammalian exercise physic~logy(e.g., Brooks ?SO Theodore Garland, Jr., and Jonathan B. Losos Locarnotor Performance in Squamate Reptiles 251

automated aseasily as they can with mamrrals.An outstandingissueis the extent to which "natural training" occurs inthe wild (Burghardt, 1984; Garland et al., 1987). Acclimationand acclimalizationof reptilian locomotor performancehas been studied onlyrarely (Gatten et a]., 1988; Hailey and Da~~ies,1986; Kauf- mann and Bennett, 1989;Payne and Gatten, 1988), as has seasonal variation, which is in some cases significant (Garland, 1985; Garland and Else, 1987; Gleeson, 1979b; Huey et al., 1990; John-Alder, 1984b). Infection with patho- gens or parasites could also be used to loher performance (Sclall, 1990; Schall and Dearing,1987; but see Danizls, 198511; Schall, 1986). FIGURE10.5 Path analyzis of performance gradients for treadmill endurance at 1.0kmlh (ENDUR) Body size, which often correlates with locomotorperformance (see below), md max~maldistance running capacity (MAXDIS)around a circular trackin the lizardctenosaura can be manipulated in a varietyof ways. For example,variation in diet or in ther- rimilis (data from Garland, 1984). For this analysis, only thosc variables that entered into multiple mal regimen(Sinervo andAdolph, 1989)may affect growth rate and hence age- regression equations as significant predictor (independent)variables andlor that could be explained to a significant extentas ,dependentvariables were considered(seeTable 4of Garland, 1984:SMR specific body size; such experimentally induced variation may be useful in was also excluded). Pathcoefficients wereestimzed in two ways: first, from standardized partial studies of static allometry (i.e., within an age class). Sinervoand Huey (1990; regression coefficients asdescribed in Nie et al. (1975); second, from the standardizedsolution Sinervo, 19%; Sinervoet al., 1592; see also Bernardo, 199 1;Hahn and Tinkle, output by LlSREL Version 4 (Joreskogand Sorbcm, 1978). an iterative, maximum likelihood fitting procedure. These :wo approaches yielded virtually identicalresults;the figure showsthe 1965;Janzen, 1993;Sineno and Licht, 199I) have used experimentalmanipula- LISREL results. A variety of path analytic models were fittedwith LISRELin order toobtain the tion of egg size in an attempt to separatethe effects of body size per se from other model which wasjudged to best fit the data basedon an approximatechi-square-goodnzss-of-fit factors that may affect speed or stamina. Embryo manipulationstudies are com- statistic and contained no nonsignificant (i.e., P > .05) path coefficients (approximate2-tailed I-tests with 14 degrees of freedom). The path analytic model shownhere had a chi-square of 22.4 mon in mammals (e.g., Atchley et al., 1993; Cowley et al , 1989; Hill and (df = 20, P = .3199), ird~cat~ngan acceptable filto the data. Individual path coefficients had Mackay, 1969; Kirkpatrick and Rutledge, 1988) but apparently have not been t-values of between 2.57and 14.8, which, by comparisonwith t,,,, 05, = 2.145, suggests that all attempted in reptiles. paths are significant.CSTHI = thigh citrate synthase activity [pergram of tissue), Hct= hematocrit, CSLIV= liver citrate synthaseactivity, THIGH = total mass of right thigh muscles, Hydric ard thermal conditions duringincubation can affectlocomotor perfor- LDHHRT = lactate dehydrogenase activityin the heart, HEART= heart nass (including atria), mance of reptiles (Miller et al., 1987; Van Dammeet al., 1992),and such effects PKTHI = thigh pyruvate kinase activity, U = unexplained variation. (See Arnold, 1983; also Sokal may not be uncommon (references in Garland and Adolph, 1991). For example, and Rohlf, 1981; Bulova, in press; and assumpticnsin Emerson and Arnold, 1989, p. ?99.) thermal conditions during pregnancycan affect the numberof body and tail CSLIV is significantly relatedto ENDUR,~0,max, and Q~0,max(see also multiple regressions in Table 4 ofGarland, 1984). DeletingCSLIV fron these predictive models resulted in vertebrae developedby garter snakes (Fox, 1948;Fox et al., 1961; Osgood, lower coefficients ofdetermination for the multiple regressionequations or a higher chi square for 1978; C. R. Peterson andS. J. Arnold, pers. comm.),which In turn may affect the LISRELfitted path analytic model. Garland (1984) interpretedthese results (and data for locomotorperformance (Arnoldand Bennett, 1988;Jayne and Bennett,1989; M. mammals)as suggestingthat liver oxidative capxity plays a significantrole in the activity metabolism of ctenosauIs, perhaps via conversion of metabol,tesduring or after activily. Recent R. Dohm anil T. Garland, in preparation). Many otherfactorsmay affect mater- studies, however, suggest that the liver is not an importantsite of lactate metabolism during nal size andlor condition and in turn affect offspring size andlor performance; recovery in amphibians or reptiles (Gleesonand Dalessio, 1989: Gleeson 1991). someof these effects canbe controlled for statistically via regressionanalysis and and Fahey, 1984; Astrand and Rodahl, 1986) have been attempted only twice computationof residuals (Brodie, 1989b;Brodie and Garland, 1993;Garland, with reptiles. Thesetwo studiesemployed very different training regimensand 1988;Garland and Bennett, 1990; Tsuji eta]., 1989). species from different families, yet both failed to improve organismalperfor- Truly evolutionary experiments, invol~ingorganismal performance or com- mance (speed, stamina, maximaloxy;en consumption: Garland et al., 1987; ponents thereof, are possible using artificial selection (e.g., Bennett et al., 1990; Gleeson, 1979b;but see Gleeson, 1991, p. 189). On the other hand, captivity and Garland andCarter, 1994; Hill andCaballero, 1992; Huey et il., 1991 ; Rose et the accompanyingrelative inactivity may decrease maximal oxygen consump- al., 1987;Schlager and Weibust, 1976),but such experimentshave not yetbeen tion (~0,max)(Bennett and John-Alder, 1984; Garland et a]., 1987; but see reported for locomotor performancein any organism.Relativeiy long generation John-Alder, 1984bi.Training studies&finitely deserve further attention; unfor- times may preclude such possibilities for reptiles, althoughexperiments with tunately, they can be quite labor-intensive becausetraining regimens cannot be mice are now being conducted( Garland, unpubl.).Direct manipulation ofthe 252 TheodoreGarland, Jr., and Jonathan B. Losos LocomotorPerformance in SquarnateReptiles 253 germ line (e.g., gznetic engineering to produce transgenicmice) is now routine variation in performance is duz solely to differencesin motivationor willingness in many animals (see Hill and Mackay, 1989) but has nct been attempted with to run. To date, publishedstudizs of individual variation havebeen somewhatmore reptiles. successful in identifying physiological correlates of endurance than of sprint speed (see "Case Studies"below), whicn suggests thatit may be easier to obtain CONFOUNDINGISSUES IN THE STUDYOF PERFORMANCE measures of physiologically limited performance capacities instamina- than AND ECOLOGICALMORPHOLOGY in sprint-type activities. Measuring "Perbrmance" as Opposed to "Behavior" Somestudies of individualvariation indicatethat measures of "behavior"ma) Arnold ( 1983,p. 352) defined perflxmanceas "the scorein someecologically show correlations with measures of "performance." For example, antipredator relevant activity, such as running speed. . . ." Most estimates of maximal loco- display (Arnold and Bennett, 1984),scored at theend of trezdmill endurance tri- motor performancein reptiles are made in the laboratory, althoughsome field als, showed significantly positivecorrelations with both treamjmillendurance and estimates areavailable (e.g., Belkin, 1961; on mammalssee Djawdan and Gar- sprint speed in the garter snakeThamnophis sirtalis (Garland, 1988; see alsoAr- land, 1988;Garland et al., 1988). In either laboratoryor field, however, defini- nold and Bennett, 1988,on T. radix and Brodie, 1992,on T ordinoides concern- tion and measurementof "performance" as opposed to "behavior" IS not always ing the correlation between speed and distance crawled p-ior to assuming an simple (cf. Friedrnan et a]., 1992; Garland, 1994a, b). For example, if maximal antipredator display). Arnoldand Bennett (1984)previously showed that whole- sprint speedis measured by chasing an animal along a race track, how can one be body lactic acid concentrationsof T radlx exhibitingantipredator displays (atthe sure that each individual actually runs at its morphological, physiological, or end of staninatrials) weresirrilar to those of snakes forced:o exercise forthirty biochemical limit;? Animals mayvary in their response to stimuli(their "motiva- minutes. Thus,one might expect the antipredatordisplay tobe partly dependent tion"), such thatrome run at their physiological limits and others do not. Thus, on, and hence limited by, physiologiczl capacities. However, Garland, et al. behavioral variation,just like morphological or physiological variation, can af- (1990b) found that, whereas speed and endurance showed significant (although fect laboratory measurementsof performance (see also Wainwright, chap.3, this weak) correlationswith lower-level morphological, physiological,or biochemi- volume). cal traits, antipredator displaj, did not (see also Arnoldand Bennett, 1988). In the laboratclry,repeated testingof individualsand use of the fastest trial(s) Thus, an alternative interpretation is that underlying variation in some axis of as an index of maximalspeed (e.g., Bennett, L980; Formanowiczetal., 1990; "motivation" (Bolles, 1975) has effects on measures of speed, endurance, and Garland, 1984,1385, 1988;Gleeson and Harrison, 1988; Huey 1982a;Losos et antipredatordisplay (higherscores are more offensive and seemto require more al., 1989; Marsh, 1988; Marsh andBennett, 1985, 1986;Sineno et al., 1991;but physical e~.ertion),leading to somepositive correlation. see Jayne and Bennett, 1990a, b) mzy help circumventmotivational problems. The foregoing examplesemphasize that caution must be exercised when de- (It is well known in human, horse,and dog racing that performances of individ- signing or interpreting measuresof loccmotor "performanc-." Our discussions uals vary significantly withthe competitionand setting.) Forsome performance of Arnold's (1983) paradigm and extensions thereofassume that true measuresof measures, it may be possible toverify by supplementarytests that physiological morphologicallyor physiologically limitedperformance can be obtained. limits have been reached.Thus, physiological exhaustionin endurance trialscan Atlometryand its Importance be supported by testing for loss of righting response (e g., Huey et al., 1984, 1990), or by m-asuring whole-body (Arnolj and Bennett, 1984) or blood Body size affects many traits, includinglocomotor performance(e.g., Dun- (Djawdan, 1993) lactic acid concentrations.Alternatively, measuresof "race ham et al., 1988; Garland, 1964, 1985;Garland and Huey, 1987;Losos, 1990a, quality" can be used in statistical analyses (Tsuji et al., 1989).In any case, what b, c). Variation in body size may therefcre obscureor enhawe relationships be- some workers term "performance" others term,'behaviorp' (e.g., Bennett, 1980). tween other traits (Emerson etd., chap. 5, this volume). Unfortunately, much of Another possibility is to test for correlations between indivicual(or inter- the older ecomorphologicallitcrature has attempted to remove the effect of size specific) differencesin performanceand traits thought to affect performance. If by using riitios, which is generally ineffectiveand potentially misleading (cf. underlying morphological, physiological, orbiochemical traits evplain (statis- Packard and Boardman, 1988): tically) a large fraction (e.g., 47789%; Garland, 1984, fig. 10.5,Garland and The importance ofconsidering allometry can be illustrated with a hypotheti- Else, 1987) of the variance in locomotor performance,then it is unlikely that cal examplz. Supposethat sprint abilitiesdetermine habitat Lse in lizards. Many 254 Theodore Garland,Jr., and Jonathan B. Losos Locomotor Pcrforrnancein Squamate Reptiles 255 studies of lizards have noted correlationsbetween relative limb length (expressed dent variable for a series of dependent variablesmay result in correlated errors as a proportion of snout-vent length)and variols habitat variables (see "Limb being introduced into all residuals. Such correlated errors can be avoided by tak- Length and Habitat Use" below), and have imp,icateddifferences in locomotor ing several measurementsof body size (e.g., when speed is measured, when ability as the underlyingcause of the relationships.Both wlthin and between spe- stamina is measured, when lim3 length is measured; Garland 1984; Garlandand cies, limb lengthrsrely scales isometricallywith snout-vent length(~.e., as indi- Else, 1987:. Third, when corre:atingthe residuals, one degree of freedom should viduals or species increasein size, limb length either becomes relativelylonger perhaps be lost for each dependentvariable for which residualsare computed. or shorter; see below, figs. 10.7c, 10.B~).Furthzr, withinand betweenspecies, One alternative to the residual approachoutlined aboveis to simply use mul- sprint ability usuallyincreases with body size. Consequently, a relationship may tiple regression of the dependentvariable (e.g.,sprint speed1on both a measure exist between habitatuse and body size due to the effect of size on sprint speed. of body sizz and, say, limb length (e.g., Snell et al., 1988). -he problem here is Because relativelimb length is partly a functionof bodysize (except when limb that body srze and limb length will generally be highly correlated,and the results length scales isometrically with size), a spurious relationship would exist be- of multipleregressionanalysesare unreliable in the face of such multicollinearity tween relative leg iength and habitat use. Our reanalysisofPiankals(1969, 1986) (Slinker and Glantz, 1985). W believe that regressionof b~hspeed and limb data illustrates this problem (see discussion below and figs. 10.7, 10.8). length on body size, then testing for correlation betweentheirresiduals, is a more Confoundingeffects of body sizecan be controlled in a variety of ways. Per- reliable prccedure. Alternatively, experimental manipulations thatchange mass haps the most common way is to regress each variableof interest (e.g., sprint or limb 1en;th-but not both-could be helpful in reducing the correlationsbe- speed, limb length) onsome measure of body size (e.g.,body mass, snout-vent tween independent variables(zf. Lande and Arnold, 1983; Mitchell-Olds and length) and then computeresiduals. These residualscan then be used in correla- Shaw, 198:; Slinkerand Glantz, 1985). tion or regression analyses or various multivariatetechniques, suchas principal In some cases, the actual value of rhe allornetric exponent ISof interest, components analysis (e.g., Garland, 1984, 1985, 1988; Jayne and Bennett, perhaps in relation to theoretical modelsof scaling (e.g.,Emerson, 1985; Gar- 1990a,b; Losos, 1990a, b, c). If the effects of additionalcovariates (e.g., tem- land, 1985; Harvey and Pagel, 1991; LaBarbera, 1989; Mush, 1988). Unfor- perature) or categorical variables (e.g., sex, season,population) need to be re- tunately, h3w best to estimat allometric relationships is unclear. As noted moved as well, [hen residuals can be computed from multiple regressions above, the independentvariable in allom~etricstudies always incorporatessome includingdummy independent variablzs (e.g.,Garland and Else, 1957;Gatten et "error vari~nce,"which means thatslopes will tend to be underestimated. More- a]., 1991; Jackson, 1973b; Packard and Boardman, 1988; Sokal and Rohlf, over, for comparisons of population adlor species means, allometric slopes 1981). Regressiorsto compute residuals need rot be restricted to linear models should be estimated phylogenetically, lot merely by a regression involving (cf. table 3 of Garland and Else, 1487; Jackson, 1973b; Jayne and Bennett, values for !ips of a phylogeny (Garlandet al., 1992, 1993; Garland and Janis, 1990a;see also Chappell,1989). With interspecificdata, methods that allow for 1993; Har~eyand Pagel, 1991; Losos, 1990~;Lynch, 199 1;Martins and Gar- statistical complicationsdue to phylogeny must be used when computing resid- land, 1991 Purvis and Garlanc, 1993). uals (Garland et al., 1992; Harvey and Pagel, 1991; Losos and Miles, chap. 4, Phylogeny and its Importance this volume;Martins and Garland, 1991). The foregoing approachis not witlout problems, however. We will mention Inheritance of a phenotypictrait cannot be studied without knowledge of the three here (cf. Huey and Bennett, 1887; Tracy and Sugar, 1989). First, least- relatednessof individuals. An~logously,the evolution of a plenotypic trait can- squares regression analysis assumesthat the independentvariable containsno not properly be studied witho~tknowledge of phylogenetic relationships.That measurementerrcr. This assumptionis not true of measures of bod) size, result- all organisms are descended in a hierarchical fashionfrom common ancestors ing in underestimatesof true structural relatiorships (Harvey and Pagel, 1991; means that no set of taxacan k assumed to be biologically or statistically inde- LaBarbera,1989; Pagel and Harvey,1988; Riska, 1991 ; Sokal and Rohlf, 1981). pendent. Phylogenetic non-independencehas implications for all aspects of sta- Unfortunately, alternativesto least-squares regressionslopes (e.g., reduced tistical analyses, includinghypothesis testing, power to detect significant major axis, majoraxis) arenot easily employed,where multiple independent vari- relationships between traits,a-7d estimarion of the magnitude of such relation- ables need to be considered. Second,using thesame inditidual measurement of ships (Felsenstein, 1985;Harvey and Pagel, 1991; Losos andMiles,chap. 4, this body size (e.g.,each animal weighedor measured asingle time)as the indepen- volume; Lynch, 1991; Martins and Garland, 1991; Pag-I, 1993). Several 256 Theodore Garland, Jr.,and Jonathan B. Losos Locomotor Performance inSquarnate Reptiles 257 methods now exist For incorporatingphylogenetic information into comparative (Arnold, 1983), although special assumptions arerequired when individuals of analyses, and various examples exist in which phylogenetic analyses leadto multiple ages are studied (Eme~sonand Arnold, 1989). qualitatively different conclusions (Garland et al., 1991, 1993; Harvey and Pagel, 1991; Nee etal., 1992). It shoulc also benoted that phylogeneticmethods Endurance. Variation in endurancehas been less studiedthan has variation in for estimating and testing,for example, character correlations, cansometimes sprinting ability (see "Sprint Speed" below). Most commonly,endurance is mea- increase-not just decrease-statistical significance as compared with an inap- sured as running time to exhaustion on a motorizedtreadmill. Interspecific com- propriate nonphylogenetic analysis. parisons of lizards indicate that treadmill endurance capacity has evolved in As the vast majority of previous coniparativestudies have been analyzed with concert with both body mass and body temperature (Autumnet al., 1994; Gar- inadequate allowarce for phylogenetic non-independence,conclus~ons drawn land, 1994b). Interspecificcorrelates of endurancehave not been studied in de- from them must be viewed with caution. Forexample, many of the allometric tail, but appear to include the energeticcost of locomotion (iower cost leads to studies we discuss were done nonphylogenetically; practical constraints(e.g., higher stamina at a given speed),i/02max, and indices of blood oxygen carrying lack of suitable phylogenies: seefigs. 10.7, 10 8 below) and time limitations capacity (Autumnet al., 1994:Bennett ?t al., 1984; Garland, 1993;Gleeson, have precluded our trying to redo all of them! Nevertheless, futurepopulation- or 1991; Gleeson and Bennett, 1985; Gleeson and Dalessio, 1989; John-Alder et species-level examinationof the morphology-;, performance-;, behavior-+ fit- al., 1983; :ohn-Alder et al., 1986a; Secor et al., 1992). Two populations of ness paradigmsho~ld be done with appropriatea.lowance for phylogeneticnon- Sceloporus merriami, which d~fferin maximal sprint speed, apparently do not independence (e.g., Losos, 1990b). An interspecific path analysis, comparable differ in treadmill endurance(Huey et al.. 1990). to Arnold's ( 1983) ~aradigmfor microevolutionarystudies (cf.Emerson and Ar- Within populations, treadmill endurance increasesontogenetically in most nold, 1989), would be particularly desirable. species of lizards (Garland, 1984, 1994b, unpubl.; Huey et al., 1990; see also Daniels anc Heatwole, 1990) and in the two species of snates that have been studied (Jayneand Bennett, 1990a;Secor et al., 1992), although not necessarily Morphology-+ Performance in a linearly allometric fashion (Garland and Else, 1987; Jayne and Bennett, Interspecific differencesin locomotor performance are well established in 1990a). Positive static allometry occurs in garter snakes (Garland, 1988; Jayne reptiles (e.g., Bennett, 1980;Garland, 1994b; Huey and Bennett, 1987; Losos, and Bennett, 1990b). 1990b,; van Berkum, 1988;referent-s therein). Population differences have Morphological,physiological, andbi,>chemical correlates of individual dif- been shown a number of times as well le.g., Garland and Adolph, 1991;Huey et ferencesin treadmill endurancehave been studied in the lizards Ctenosaura sim- al., 1990; Sinervoet al., 1991; Snell et al. 1988; but see Bennett and Ruben, ilis (fig. 10.5) and Crenophords nucha1;s (Garland, 1984; Garland and Else, 1975). A somewhzt surprising finding has been the substantial variation in per- 1987). Comlationsof each variablewith bodymass wereremoved by computing formance amongindividuals within single populations(Bznnett, 1987; Bennett residuals f13m regression equstions. Af:er this procedure, several underlying and Huey, 1990; Huey et al., 1990; Pough, IS89). Sex differences in perfor- variables w?re shown to correlatesignificantly withenduranle (e.g., ~0,max, mance exist and are in some cases due to sex differences in body size; unfor- thigh muscl- mass, enzymeactivities). Correlationswith ~0,rnaxand with thigh tunately, few studies have actually tested for sex differences wi:h adequate muscle mass occur in three of five specks studied to date (Garland,1984; un- sample sizes (e.g..Garland, 1985; Huey et al., 1990;Jayne and Bennett, 1989; published data on Callisaurus draconoides and Cnemidophwus tigris; Garland Tsuji et al., 1989). Some individual variation in performance ability is due to and Else, 1987; John-Alder, 1984b). Thzse studies were the first to document differencesin age and/or size (Garlandand Else, 1987;Halley and Davies, 1986; performanc~gradients forrepti!ian locomotion.

Marsh, 1988; Pough, 1977, 1978);their effects have beenthoroughly separated Treadmill endurance does not correate with residual hindlimb length in in only two studies of reptiles (Hueyet al., 1990; Sinemand Adolph, 1989). Sceloporusmerriami (Huey et al., 1990)or in hatchling S. occidentalis (Tsuji et Variation inperformance calls for both proximateand ultimate erplanations. al., 1989). However, asmall (r = ,218)but significant correlationexists between In this section, Re consider the former-studies exam~ningthe mechanistic treadmill enduranceand residual tail length in hatchlingScelcporus occidentalis bases of performaxe variation. Note thatstudies of individual variationin per- (Tsuji et al., 1989). Treadmillendurance correlates positively with ~0,maxin formanceand morphology constituteattempts to quantify performancegradients Thamnophis sirtalis (Garland and Bennett, 1990; Garland et al., 1990b). 258 TheodoreGarland, Jr., and Jonathan B. ~0.s.os Locomotor Performancein SquamateReptiles 259

Stamina can also be measured by chasing animals around a circulartrack at Many studies have investigated whetherthe predicted positiverelationship top speed until exhaustionand recording total distanceandlor time run. Several between limb length and sprint speed exists in lizards. Given the oft-observed species of lizards have been so tested, but generalitiesare not yet apparent (Ben- correlation between size and speed,most studies removethe effect of size (see nett, 1980, 1989; Garland, 1993;Mautz et al., 1992). Studiesof individual varia- above) on both limb length and speed to examine whetherdative limb length tion have also dccumented morpholsgical and physiological correlates of correlateswith relative sprints?eed. Intrapopulational studies have beenevenly maximal distancerunning (or crawling] capacityin both lizards (Garland,1984, split: a conelation between relative limk length and sprint speed exists in Tro- unpub.) and garter snakes(Arnold and Bennett, 1988; Dohm and Garland, un- pidurus albemarlensis (Snell et al., 1988 but see discussion below), Sceloporus pub.) (see also Gztten et al., 1991, on alligators). Less useful measures of occidentali; (Sineno, 1990; Sinervo and Losos, 1991 ), Sceloporus merriami stamina, in terms of comparability andecological relevance, canbe obtained by (Huey eta],,1990), and Urosaarusornutus (D. B. Miles, pers. comm.),but not holding animalsin any type of container, proddingthem tostruggle,and record- in Ctenosanra sirnilis (Garland, 1984), Ctenophorus (Amphibolurus)nuchalis ing the time until cessation of activity,loss of righ~ingresponse, etc. (Daniels and (Garland, 1985),Leiolepis br1l;ani(Losos et al., 1989),or hatchlingSceloporus Heatwole, 1990;Snyder and Weathers, 1977). occidentali;(Tsuji et al., 1989). Positive interpopulationalor interspecific cor- relations have been reported several times (Bauwenset al., in press; J. Herron Sprint Speed. Sprint speed is the most comm~nlystudied aspect of reptilian and B. S. Wilson, pers.comm.; Losos, 1990~;Miles, 1987,pers.comm.; Sin- locomotor abilities:and a considerablebody of research addressesthe mechanis- ervo and Lcsos, 1991; Sinervo2t al., 1991; Snell et al., 1988). tic basis of variation in sprinting. At this point, differences in body size and in Although several theories(e.g., geometric similarity,elsstic similarity, dy- relative limb length seem to be the most importartcausal factors. namic similarity) have been proposedthat predict the relatio~shipbetween size Within populationsof lizardsand snakes,sprint speed generally increases with and sprint speed, none adequa:ely explains the available da:a for mammals or body size (mixed samples: Daniels and Heatwols, 1990;Garland, 1985; Huey, lizards (Chappell, 1989;Garland, 1985).The relationshipbetween limb length, 1982a;Huey and Hertz, 1982;Huey eta..,1990;Losos, 1990c; Lososetal., 1989; stride lengtn, and sprint speedis perhaps simpler and more ~ntuitivethan these Marsh, 1988;Secoret al., 1992; Sinervc,1990;Snelletal., 1988; staticallometry: theories im?ly. Snell et al. (1988) argue[hat the relationshipbetweenbody size Arnold andBennetl, 1988; Garland, 1988; Garland and Arnold, 1983;Jayne and and sprint speed in Tropiduruszlbernarlensis (pooling individuals of both sexes Bennett, 1990b; Sinervo, 1990; Sineno and Adolph, 1989;Sinervo and Huey, and from two populations) results from the correlationof both variables with 1990;Tsuji et al., 1989).Severalexceptionsexist (Garland, 1984, unpub.; Brodie, hindlimb length, rather than there existing a direct relationship between body 1989a),however, and the snakeTharhncphissirtalis shows acurviline~rallometry size and splint speed. Stepwisemultiple regression analysis indicated that, after (Jayne and Bennett, 1990a). allowing for the positivecorrelation betw~ensprint speed and snout-ventlength, Evidence for a lat ti on shipbetween speedanc size is more equivocalin inter- individual variation inhindlimh length predicts a significant emount of variation specific comparisons.In a phylogenetic analysis of fifteen CaribbeanAnolis spe- in sprintspeed. However,in a secondaria-ysis, after hindlimblengthis removed, cies, Losos (1990b) has shown that sprint speedandsnou:-vent length evolved no relationship exists betweensize and sprint speed. The strong correlation(r = together. By contrzst, van Berkum (1986) found no relationshipbetween sprint .93) between hindlimb length 2nd mass in Tropidurus suggests extremecaution speed and size among seven speciesof Costa Rican Anolis. At higher taxonomic in interpreting these results (cf. Slinker and Glantz, 1985). Nonetheless,a rean- levels, no simple linear relationshipbetween speed and sizeappearsto exist (Gar- alysis ofdata for fourteen speciesof Anolis (from Losos, 199Cb,c) reveals a sim- land, 1982,unpub.; but see Marsh, 1988, p. 131). ilar pattern when residuals ar, taken from regressions on snout-vent length, Biomechanical models predicta positive relationship between limb length hindlimblength and sprint speed are still ~ignificantlyrelated, but when residuals and sprint speed (discussionsin Garland, 1985;Losos, 1990b; Marsh, 1988). are taken from regressions on hindlimb length, snout-vent length and speed are Indeed, most "cursorial" mammals ha\e elongated legs resulting primarily from not significantlycorrelated (see also Bauwenset al., in press). increased length of the distal elements (Garlandand Janis. 1993;Hildebrand et The rela:ionship between other morphological variablesand sprint speedhas al., 1985;Janis, in press; references therein). Cu-sorial lizards also exhibit elon- been less studied. Lizardsare renowned for their ability to drop their tails to gated limbs, but, by contrast, alllimb elements seem to increase in length, with thwart predation;a number of studies habe experimentallyassessed the effect of no apparent regularity as to which elementinc~eases the most (Rieser, 1977). tail loss on sprint speed (reviewed in E. V. Arnold, 1988; see also Russell and 260 Theodore Garland, Jr., and Jonathan B. Laos Locomotor Performance in Squamate Reptiles 261

Bauer, 1992). Many lizards with exper~mentallyreduced tails run more slowly speed. First, some animals appear not to sprint at top speed in a race track. For [Arnold, 1984a; Ballinger et al., 1979;Formanovicz et al., 1990; Pond, 1981; example, maximal reported speeds of desertiguanas (Dipso~aurusdorsalis) in Punzo, 1982),but not Phyllodactylusmarrnoratus(which does not useits tail as a race tracks (single fastest indiy/iduals) xe 10.1 kmlh (Ben~ett,1980; higher 2ounterbalance: Daniels, 1983), Sphcnomorphus quoyii (Daniels, 1985a), speeds were reportedfor somecther specks), 18kmlh (Marst, 1988;Marsh and Sceloporus merriami (Hueyet al., 1990), or the snake Thamnophis sirralis Bennett, 1955), and 15.0 kmlh (Gleeson and Harrison, 1988), whereas Belkin [ Jayne and Bennett, 1989).Although a negative effect or sprint performance (1961) reports a maximal field s?eed of almost 30 kmlh and J. A. Peterson (pers. may have long-termrepercussions,the importanceof tail loss in a given predator- comm.) reports observing simlar speeds on a high-speed treadmill (compare prey encounter is probably more a functlon of predator distractionthan of altered also speeds recorded for Uma notata in the laboratory [Carotters, 19861and the lizard escape speed (Dialand Fitzpatricc, 1984; Cooperand Vitt, 1991). field [Nonis, 19511). Why some speciesdo not perform well in a race track is The biomechanicsof legless locomotion are poorly understood (Gans, 1975; unclear. Alternative techniquesfor measuring sprint speed, such as high-speed Jayne and Davis, 1931; Secoret al., 1992). Verteb:al numbers may relate to inter- treadmills(!. A. Peterson, pers.comm.; Garland, unpubl.)mzy circumventsuch specific differences in locomotor performance in snakes (Jayne, 1985, 1986, problems. 1988a, b). Within apopulation of Thamnophis radix, numbersof body and tail Second, measuring acceleration in racetracks is much mor, difficult than ob- vertebrae correlatein an interactivefashion with speed in juveniles (Arnoldand taining sprirt speed alone, because lizards must sitmotionlessjust in front of the Bennett, 1988). Relstivetail length alsomay affect snakesprint speed (Jayneand first photocell, then burst along the track when startled. Many species arenot so Bennett, 1989). cooperative(but see Carothers, 1986; Huey and Hertz, 1984a), instead strug- The effect of muccle size and composition on sprintperformance would seem gling and running as soon as being placed in the track. It is unfortunate that mea- to be an obvious aresfor study, but littlework has been donetodate. Gleeson and sures of accelerationare difficult to obtain, because accelerat~on,as opposed to Harrison ( 1988) report significant inversecorrela:ions bet~eensprinl speed and just maximal steady-state sprintspeed, may be of prime importance in predator- muscle fiber areas in desert iguanas(C'ipsosaurns dorsali~). The low maximal prey interactions (Elliottet al., 1977; Huey and Hertz, 1984a;Webb, 1976). speeds of chameleons appear at lemt partly related to their having slow- contracting muscle: (Abu-Ghalyuneta.. , 1988; see also Peterson, 1984). Jumping.Biomechanical models suggest thatbody and muscle mass, limb Sprint speed is also affected by temporary changes in body cond~tion.Both length, 1oca:ionof center of mass, muscle composition, andbehavior allcan af- gravidity andrecent ingestionof food rejult in inc~easedmass and decreased flex- fect jumping performance (Alexander, 1968;Emerson, 1985; Losos, 1990b; ibility and so may have similar effects on sprint performance.Gravidity generally Pounds, 1958).The biomechanicsofjumping have been investigatedonly in the lowers sprint performancein both lizards and snates (e.g., Brodie, 1989a;Coo- legless pygclpodid lizard Delma tincta (Bwer, 1986) and in Xnolis carolinensis per et al., 1990; Garland, 1985;Huey et al., 1990; Van Damme, Bauwens, and (Bels and Theys, 1989;Bels et al., 1992). Verheyen, 1989). Fopulationdifferenes in the effect of gravidity on maximal Considerable variationin jumping ability exists both within and among lizard sprint speed existin Sceloporusoccidentalis (Sinewo et al , 1991). Similarly, a species (Losos, 1990~;Losos et al., 1983; Losos et al., 1991). Among fifteen full stomachhas, in some cases,been shown to lower speed and/or endurancein species of Anolis, body size anc jumping ability arepositively related (Lososet lizards and snakes [Fordand Shuttlesworth, 1986; Garland and Arnold, 1983; al., 1991; Losos, unpubl.).Withn species,jumping ability increases withsize in Huey et al., 1984).Apparently, burstspeed may 3e less sensitive to such effects Leiolepis belliani (Losos et al., 1989) an'i in seven species of Anolis (Lososet than is endurance (cf. Cooperet al., 1990; Garland, 1985; Garland and Else, al., 1991,unpubl.). In addition, positivebut nonsignificant relationships alsoex- 1987). Furtherstudies of the effects on locomotor capacities of recent feeding, ist in nine of eleven other speciesof Anolis (Losos, unpubl.). especially in relation to models of optimal foraging, allocation of time and en- With theeffectof sizeremoved, relativsly long-leggedspecies ofAnolisjump ergy to foragingversus reproduction,and associated costs and trade-offs, should relatively farther than do shorter-legged species.Lesser and negative effectsof prove interesting.Brodie and Brodie (1990) used sprint speed as a bioassay for tail and forelimb lengthon jum?ing abilily also exist in anoles (Losos, 1990~). the effects of tetrodotoxin on garter snakes. By contrast, norelationship between relative limb lengthandjumping ability is Two caveats must be kept in mind when considering investigations of sprint evident in Lciolepis belliani (Losos et al., 1989). No differences have beende- 262 TheodoreGarland, Jr., and Jonathan B. Losos Locomotor Performancein SquamateReptiles 263 tected betweenmales and femalesin Leiolepisbzlliani (Losos et al., 1989)or in avoiding predators by jumping from trees, gliding to the ground,and running Anolisfrenarus (Lososet al., 1991), although saxplesizes were small in the lat- away. Similarbehavior is displayed by a number of geckos (Russell, 1979). and ter study. perhaps, by spiny-tailed iguanas(Ctenosaura sirnilis) over 1 kg in body mass (Garland, pers.obs .). Gliding and Parachuting. Glidilg reptiles, includ~ngthe enchantingly named Icarosaurus and Daedalosaurus, date to the Permian (Ricqles, 1980). Concksions. A variety of ecologically relevant measures ofperformance Gliding abilities have been noted in a considerable number of snakes (e.g., have been studied in lizards and snakes. Most attention tas been focused on Chrysopelea: Shelford, 1906; Heyer and Pongsapipatana, 1970)and lizards sprint speed, perhapsbecause it is relatively easy to measure. Althoughthe ef- (Ptychozoon: MeCens, 1960; Heyer and Pongsapipatana, 1970; Marcelliniand fects of mxphologyand physiologyon sprinting (andon gliding) capabilityare Keefer, 1976; Hdapsis: Schiotze and Volsoe 1959). The prem.er reptilian theoretica.1~the simplest,we seem to have more empirical information on the gliders arethe members of theSoutheast Asian genus Dracn, which have evolved mechanistic correlatesof variation in zndurance. For all measures of perfor- flight membranes formed from a pataglum stretched over elongated and movable mance, tkeffect of many variables remainsto be assessed. Other importan: ribs. These lizards can glide for considerable d~stances;"flights" of over 20 m aspects oflocomotorperform~nce, suchas burrowing (Gansetal., 1978),climb- have been observed in nature, and 60 m in experimental trials (see Colbert, ing (Losos and Sinervo, 1989; Sineno and Losos, 1991; see also Thompson. 1967). In other reptiles, gliding ability appearsto be enhanced by the presence of 1990,on mdents), and swimmingability (Bartholomewet al., 1976; Danielsand flaps of skin alongthe sides of the body, neck, and tail and between the toes; the Heatwole,1990; Gans, 1977;Gatten et al., 1991; Schoener 2nd Schoener, 1984, ability to increase ventral surfacearea; and the tendencytoadopt an outstretched Tracy andChristian, 1985;Turner et al.. 1985; Vlecket al., 1981) have received posture (Mertens, 1960; Oliver, 1951;Russell, 1979). Because the distinction is little atten:ion. often not clear, we will use "gliding" throughoutthepaper :o refer toboth gliding Performance -+ Behavior or Fitness/Ecology and parachuting from one arboreal ~ositionto another or to the ground (see Rayner, 1981, 1967). Studies using quantitativedata to correlate interspecific variationin locomo- Several studies have experimentalljl investigated the rale of morphology and tor abilities with ecologyor behavior are relativelyrare. In th~ssection, we briefly behavior on gliding ability.Larger individuals of Leiolepis belliani have greater summarizethe datarelating enmjurance and sprint capabilities tobehavior, fitness, wing loading(i.e.. mass/surface area) and fall more rapidly (Lososet al., 1989). and ecology, and then addresstwo topics in which the relevance ofperformance Wing loading and glide performance were also inversely correlated in has been more extensively examined:the context-specificityof performance and Prychozoonlionarm (Marcellini andKeefer, 1976).When surfacearea is exper- the relationshipof variation in performance capabilities toforaging mode. imentally decreased (by preventing dorsoventral flattening inLeiolrpis belliani [Losos et al., 19891and tying lateral cutaneousfolds to the body inPtychozoon Endurance, ~0,max,and Anaerobic Metabolism. The relevance of en- lionatum [Marcellini and Keefer, 1976]), gliding performance was diminished. durance czpacity for squamate naturalhistory is just becoming apparent (Gar- The importance of body posture on rate of descent was suggested inLeiolepis land, 1993, 1994). Treadmill enduranceat 1.0 km/h appears to be related to belliani. Dead lizards, which tumbled rather than falling in a horizontal, out- averagedaily movementdistance (cf. Garland, 1983)among nine speciesof liz- stretched position,fell faster than didlive lizards. Further,for a given wing load- ards (table2 of Hertz et al., 1988). Si~ilarly,Loumbourdis and Hailey (1985) ing, live lizardsfell slower, whichsuggests thatbehavioral adjustments,such as suggesteda correlation between both active (notverified ~0,max)and resting creating a concave (rather than flat) ventral surface while falling, enhancepara- metabolic rates and "lifestyle" of lizards, though further corroboration is neces- chuting abilities(:he snake Chrysopelea ornatu also adepts a sim~larconcave sary (see also Kame1 and Gat~en,1983:. Various adaptive explanations for the posture when falling[Shelford, 190611.The importanceof gliding as a means of high aerobic capacities (~0,max)of Cnsmidophorusfigris, Helodermu susprc- moving through the environment is 3bvious, particularly in forests in which rum, and Varanus species have been offered(Bennett, 1983; Bicklerand Ander- movement fromtree to tree would otherwise require alizard to cl~mbinto the son, 1986. Garland, 1993;John-Alder et al., 1983). The uses of anaerobic metabolism in nature, and possible correlations between anaerobiccapacities crown or to the ground. Further,Ol~ver (195 1) observed Anolis carolinensis 264 Theodore Garland, Jr., and Jonathan B. Losos Locomotor Performance in Squamate Reptiles 265 and lifestyle in reptiles, have been reviewed elsewhere (e.g., Bennett et al., and Shine, 992). For example,in laboratory enclosures,Garland et al. (1990a) 1985; Gatten, 1985; Pough and Andrews, 1985a, b; Seymour, 1982, 1989; studied whether social dominancemighi be related to capacities for speed or Ultsch et al., 1985) stamina inSceloporus occidentalis. In paired encountersbetween males compet- ing for access to a basking site, winners were significantl;/ faster than were Sprint Speed. Population differencesin wariness have been documentedin losers, but did not have highertreadmill endurance (see also Hews, 1990; Wilson lizards (Bulova, in ?less; Shallenberger,19701, kut possiblz performance corre- and Gatten, 1989;Wilson et al., 1989). lates have been studied only once. In more open ueas on the eastern end of Isla Plaza Sur, Galapagos lava lizards (Tropidurus abermarlensis)are warier (i.e., Context-Specificity of Perf~rmance.3volutionary specia.ization to a partic- they flee further and earlier when approached by humans) than are lizards from ular "niche' may come at the expenseof bwered fitness (including lower"effec- the more vegetated ;vestern end of the island (Snellet al., 1988).Lizards living in tiveness" [Gans, 19911 or energetic efficiency [e.g., Andrews et al., 19871) in the more open areas are presumed to be more vulnerable to predation, although other "niches" ("the jack-of-all tradesis master of none" idea [Huey and Hertz, data on predation rates are lacking. Males from the eastern populationare, in- 1984b; Jackson and Hallas, 15861). If so, then one might predict that perfor- deed, faster than western males, but fmales dc not differ; the morphological mance capability would be context-specific;species, for example, mightperform basis for the difference in speed amongmales is unclear. a task best under conditions most similar to those they experience most often in Four studies have attempted tomeasure natural selection actingon individual nature (see also Bauwens eta]., in press). variation in locomotor performance in the field (see Bennett and Huey, 1990). To test this idea, Losos and Sinervo (1989) measured sprint speed of four spe- These constitute direct attempts to quantify fitness gradients (fig. 10.1) for rep- cies of Anolis on different diameter rods. In nature, the long-leggedA. gundlachi tilian locomotion. Jayne and Bennett (1990b) found that survivorsh.p of garter uses wide structures, whereasthe short-legged A. valencienni often moves on snakes (Thamnophissirtalis) was positively related to laboratory measures of narrow twigs; the other twospecies are intermediate in both respects. On wide both speed and dislance crawling capazity, although not during the first year of perches, sprint speed and leg length were directly related zmong the species; life. R. B. Huey ard colleagues (see also Tsuji et al., 1989; van Berkumet al., however, on narrow rods,all four specieshad similar sprint abilities (fig. 10.6). It 1989) conducteda similar study of hatchling fencelizards (Sceloporusocciden- is understandable why the long-leggedspecies do not use nirrow structures in talis), but the analyses are not yetcom~lete. In both cases,comparisons offami- nature: their locomotor capabilities wouldbe impaired. But why should short lies of presumed full-siblings suggest that speed and stamina may be heritable (Garland, 1988; Jayne and Bennett, 1490a; Tsuji et al., 1989; van Berkum and Tsuji, 1987). Miles(1989, pers.comm.) reportssignificant directionalselection on speed in Urosawuslizards. Finally, A. E. Dunham, R. B. Huey, K. L. Over- all, and colleaguesare continuinga study of selection on locomotor performance in Sceloporusmerriami, with preliminary resultssuggestingno significantselec- tion on locomotor performance (pers.comm.). As with almost all stddies of se- lection (Endler, 19,36;Wade and Kalisz, 1990), interpretat~onof these studies is problematicalbecause thecausal basisfor selection on sprint speed is not under- stood. In the abserce of data on whether lizards and snakzs actually use maxi- mum abilities in nature and, if they do, whether variation in maximum abilitiesis biologically significant,a story can bedevised for any result. This is not to sug- 1.I 2.1 2.6 3.3 4.6 Diameter gest that selection studiesare unimportant, but, rather, to urge that they be (cm) coupled with detailed analyses of natural history and possibly experimentalma- nipulations(Green?, 1986; Hews, 1990; Pough, 1989;Sinewo et al., 1992). FIGURE10.6 Lnteraction between loconotor performance ability and specie; identityfor four species of Anclis lizards running on rods of varyingdiameter (modified frorn Losos and Sinema, Some informat:on on fitness gradientscan be obtained through laboratory 1989). Species differences in maximalsprintspeedare apparent only on larger rods. gun = Anolis studies or controlled trials in seminatural field enclosures (e.g., Schwartzkopf gundlachi, lin = A. linearopus, gra = .4.grahami, val = A. valencienni. 266 Theodore Garland, Jr., and Jonalhan B. Losos Locomotor Performance in Squamatc Reptiles 267

legs evolve to utiliz- narrow structures7Anolis gxndlachi can run as fast as A. agers, which often captureprey bj a quick l~ngefrom an ambush site, often show valencienni on narrow structures without incurring the latter's 50% sacrifice in greater sprint~ngability (Huey et al., 1984). Further, in interspecific compari- speed on broad structures. The answer probably liesin the species' ability to sons, foraging mode appears tobe associated withdifferences in resource acqui- move without difficulty on narrow surfaces ("surefootedness" sensu SLnervoand sition and reproductive rates (Anderson and Karasov,198 1, 1988; Karasov and Losos, 1991). In o'Ter 75% of the trials on the narrowesr rod, A. gundlachi Anderson, 1484; Nagy et al., 1984). Three studies have revealed some mor- stumbled or fell off, whereas A. valencienni was much less affected. Conse- phological and physiological correlatesof d~fferencesin foragin,3 mode andloco- quently, A. valencienni seems to have trzded the ability to move rapidly onbroad motor perfornance(Bennett et al., 1984; Garland, 1993,1994b). surfaces for the ability to move without troubleonnarrow ones. Nonetheless, with the followingexceptions, few examples indicate tight rela- A similartrade-03' isapparent among fourpopulations of Sceloporus occiden- tionship between morphology, performance, and foragingmode. Active forag- ralis (Sineno and Losos, 1991) andbetween S. nccidentalis and S. graciosus ing lizards appear to experience higher predation, andtheir longer tails may (Adolphand Sinewc,in preparation).By contrast,relative sprint performancein represent an adaptation by increasing the likelihood that apredator will grab the (WO chameleon species is consistent across a rangeof surface dimensions (Losos detachableta.1, leaving intacttherest of the lizard (Huey andPianka, 198 1; Vitt, et al., 1993). In both the Anolis and Scel9porus cases, field studiesareneeded to 1983). Among snakes, active foragerstend to have longitudinalstripes and flee evaluate the relative ecological importance of maximum speed versus sure- when approashed; longitudinal stripes can give the impression that a moving footedness. Biomechanicalstudies should enlightzn relationshipsbetween limb snake is stationary, making it easy for a predator to lose sightof a fleeing snake. length, perch diameter, and sprinting (Alexander, 1968; Emerson and Koehl, By contrast, more sedentary speciesoften have broken patterns and rely on 1990; Hildebrandet al., 1985; Pounds, 1988). crypsis or active defenseto thwart predators(Jackson etal., 1976;Pough, 1976). The foregoing studies underline the importance of measuring performance Further, antlpredator behavior (fleeing versus crypsis) and color pattern over a variety of app:opriate conditions,of measuring severaldifferentaspects of (blotched versus striped) are geletically correlated in Tharnnophis ordinoides performance, andof considering a variety of behaviorsthat may relate to perfor- (Brodie, 1983b, 1993). mance abilities (cf. Bennett, 1989; Garland, 1993,1994a, b; Huey and Hertz, The relationshipsof clutch size, performance, andforagin; mode are better .984a; Sinervo and Losos, 1991). established.Gravidity leads to decreasedsprint speed andlorendurance in lizards (e.g., Cooperet al., 1990; Garland, 1985;Garland and Else, 1987; Sinervoet al., Foraging Mode and Relative Clutch Mass. Lizards habe traditionally been 1991; Van Damme, Bauwens, and Verhejen, 1989;but see Huey et al., 1990) classified either as "sit-and-wait" or as "active" foragers (Pianka, 1966; Regal, and snakes(Brodie, 1989a;Jayne and Bennett, 1990a;Seigel el al., 1987).Thus, 983; Schoener, 195I), although the diszinction represents extremesofa contin- active foragers, whichrely greatly on sustained locomotion, generally have uum rather than an actual dichotomy(ap?endix I o'Garland, 1993; McLaughlin, evolved smaller relative clutch masses (RCM), whichminimize these effects .989;O'Brien et al. 1990;Pietruszka, 1986). A variety of attributes distinguish (AnanjevaandShammakov, 1985; Dunhametal., 1988;Huey ~ndPianka, 1981; the two foraging modes among terrestrial lizards. Sit-and-wait (or ambush) for- Magnusson et al., 1985; Vitt anil Congdon, 1978; Vitt and Price, 1982; but see agers tend to be stocky, have short tails, and csny relatively large clutches, Henle, 1990;again, phylogeny is a confounding factor[Dunham et al., 19881). whereas active (or "widely foraging" or "cruising") foragers often are slender, Shine (1980), Seigel et al. (19E7), and \an Damme, Bauwens, and Verheyen with long tails and relatively small clut:hes (Huey and Pianka, 1981; Vitt and (1989) suggested that locomotorimpairment correlated with RCM, but Brodie Congdon, 1978;Vit: and Price, 1982; Peny et al.. 1990). Relatively little intra- (1989a) arg~edthat gravidity per se, rather than RCM, is the major cause of de- familial variation in foraging modeexists among lizards; hence, interspecific creased locamotor capacities (see also Sineno et al., 1991).In a similar vein, comparisonsof fora4ing types often are confoundedby phylogeny (Dunham et Shine (1988)argued, based on kiomechanical considerations, thata given RCM al., 1988). However, intrageneric (Huej, and Pianka, 198 1, Huey et al., 1984) would hinder snake locomotion more in aquatic than in terrestrial species. He and even intraspecific (Robinson and Cunninghan, 1978) variation in foraging thus interpreted the lesser RCMof aquatic species as adaptive. mode exists in lacertids (Peny et al., 1990). A linear relationship between gravidity, decreased sprin:ing abilities, and The two foraging modes tend to difer in sprint speed and endurance in an increased mortality cannot be assumed. For some species, gravid females may expected manner; active foragers have greater endurance, but sit-and-wait for- indeed be mxevulnerable to predation (Shine, 1980; referencesin Cooper etal., 268 Theodore Garland, Jr., andJonathan B. Lusos Locomotor Performancein SquamateReptiles 269

1990).but in other species behavioral shiftsmay compensatefor decreased loco- allometry occurs in a few species (Dodson, 1975; Poundset al., 1983). Inter- motor performance. Forexample, the lizards Lacerta vivipara (Bauwens and specifically, negative allometryof hindlimb length is common among lizards Thoen, 1981) and Eumeces laticeps (Cooper et a]., 1990), and the snake Tham- (e.g., figs. 1D.7c, 10.8~below; Losos, 1990b). A number of idaptive explana- nophis ordinoides (Brodie, 1989a), alter their behavior when gravid, becoming tions have been offered to exp1a:n these patterns. For example, Dodson(1975) less active and more reliant on crypsis and aggression for defense. Indeed, no proposed that the positive ontogeneticallsmetry in two specles of Sceloporus increase in mortality was observed for gravid Lacerta vivipara (Bauwens and represented an adaptation forincreased honerange size and movementin adults, Thoen, 1981 ; see also Schwartzkopfani Shine, 1992). although the underlying mechacism(e.g., increased mobility) for such a rela- tionship was neither specifiednor measured. Poundset al. (1983) hypothesized Conclusions.Relationships between performanceability and ecology or be- that positiveontogenetic allometry in Sceloporus woodi migh: relate eitherto a havior have been little explored, either intra- orinterspecifically. When studies shift to morearborealhabitats or to reliance on sprinting toavoid predation. Be- have been conducted, they often are correlational and do notdirectlyexamine the cause sprint speed usually increases ontogenetically(see above), Pounds et al. causal basisof any correlation.They are thus notable to dist~nguishseiection and (1983) inteqretedthe negative allometry observed in four other iguanid species sorting (sensu Vrbaand Gould, 1986). As well, phylogeny confounds most an- as a means of compensating forthe lesser sprinting abilityof smaller individuals alyses to date. Relationships of foraging behavior, reproductive state, and loco- by increasing the length of their hindlimbs:cf. Grand, 1991,on antelope). Sprint motor performance,however, do seem reasonably well established. speeds,however, were not measured, andGarland ( 1985)has argued that data on scaling of limb dimensions alone are inadequate to infer scalingof sprint speed. Morphology Behavior or FltnessIEcology -+ The importanceof explicitly considering allometryis appzrent in a study of Biologists comparing specieshave long noted correlations betweenform and fourteen species of diurnal Cter;otus skinks in Australia. Pia?ka (1969) found lifestyle or habitat (e.g., Bock and von 'vlrahlert, 1965;Gans, 1988;Luke, 1986; that relative lindleg length (length ofone hindlegisnout-ventlength) correlated

Rayner, 1981, 1987, Ricklefs and Miles, chap.2, lhis volume;Van Valkenburgh, positively w~thuse of open space(fig. 10.7~).Pianka (1986)inferred that long ihap. 7, this volume;references in Wainwright, 1391)and have taken such rela- legs must enlance sprint speedand thus are beneficial in open spaces, whereas, :ionships as evidence thatparticular morphologiesare adaptations(sensu Gould in densevegetation, long legsacrually imp-de efficient locomotion(see alsoJak- and Vrba, 1982)for particular lifestyles or habitats (Harvey and Pagel, 1991). sic' and NuAez, 1979). (In fact, some Crenorusdo fold their legs against the body Indeed, such comparisonsand interpretations are at the heart of traditional eco- and use serpentine locomotiontc move through clumps of spinifex grass [James, ogical morphology[e.g., Norberg, chap. 9, this wlume).Rarely, however, does 19891.) Unfortunately, therelati#mship between relative limb ength andhabitat evidence existdemonstrating that morphological differencesactually lead to dif- is confounded by bodysize. Larger speciesuseless open habitats (fig. 10.7b)and ferencesin perform~nceabilities thatare appropriatefor different habitats.Here, have relatively shorter legs (fig. 10.7~).When these correlaticnswith body size ,we review studies that have related reptilian locomotor morphologyto behavior are removedby regression analysis,a relationship between residual use of open or ecology, and evaluate the extent towhich locomotor performance represents space andresidual hindleg length is suggested, but nonsignificant(P < .12; fig. the mechanisticbasis of such relationships. 10.76). Amongspecies ofnocturnal Australian geckos,use of open spacesand relative LimbLength and Habitat Use.Several studieshave correlated interspecific hindleg length are uncorrelated(data from ?ianka, 1986;contrsry to analysesof a or interpopulationvariation inlimb length with diferencesin microhabitatuse or smaller dataset in Pianka and Pianka,1976; fig. 10.8a).In this case,however, use behavior. Usually, hawever, the effect of variationin limb length on performance of open spacz is not significantly relatedtosvl (r2 = ,025,P = ,6652;fig. 10.8b). and the relevanceof differencesin performanceto variation in habitat cr behavior Analysis of residuals from regressions on svl (a conservative procedure) also are not investigated.In addition, differencesin limb proportions (oftenexpressed indicates that open-space useis not significantly predictedby relative leglength as ratios) canbe con'ounded by differencesin size[see"Allometry and its impor- (figs. 10.8c, 4. Both of these examples (Crenotus, nocturnal geckos) deserve lance" above).We first offer a brief discussionof locomotor allometryin lizards. phylogenetic reanalyses whensuitable phylogeniesbecome available. Within most lizard species, hindlimh length shows nega:ive allometry (e.g., A number ofother studies have investizated whether a relationshipexists be- Garland, 1985; Kraner, 195I; Marsh, 1988; Pounds et al., 1983), but positive tween limb proportions and habitat. Longer-leggedtaxa use more open (includ- Locomotor Performance in SquamateReptiles 271

ing large bculders) and/or terrestrial habitatsamong populatons of Sceloporus woodi (Jackson, 1973b), amorg populations in a cline connectingLiolaemus platei andL. lemniscatus (Fuentes and Jsksic', 1980), and between species of Sceloporus(Jackson,1973a, b)and Lace:ta (Darevskii, 1967). By contrast, in a study of Ncrth American temperatelizard communities,Sclieibe (1987) found that large, ~ulky,and long-legged sit-and-waitforagers occupied extensively vegetated habitats, whereas small,slender, and short-leggedactive foragers used more openhabitats. However, this study is a prime exampleOF the importanceof ; conductingcomparative analysesin a phylogeneticcontext: of the three families 38 42 46 50 34 58 ; representedin thestudy, onlythe Iguanidae (twenty-oneof twenty-ninespecies in (1 Hindleg Length/Snout-Vent Length * 100 the study)exhibit substantial variation,aost of which is distributed among gen- era. This phylogeneticnon-independence leads, in effect, toa substantialinfla- tion of the inferred degrees of freedom, possibly leading to spurious significant results (cf. Garland et al., 1991).No relationshipbetween limb length and habitat use is evide~tamong Liolaemu~ (Jaksic' et al., 1980)or Brazilian cerrado lizards (Vitt, 1991). Several other studieshave laoked for correlates of limb length in lizards. An- anjeva (1977) found that among five species of Russian Erenias, limb propor- tions were related to locomotor behavior (e.g., climbing, burrowing). In addition, insular populationsof lacertid lizards in the Adriaticseagenerally have oJ.:.:.:.:~ 35 45 55 65 75 shorter legs than do mainland populations, except on islands with steep cliffs. (b) Snout-Vent Length (mm) Kramer (1951) suggested thatthe lack of predators on islands and the need for clinging and jumping ability or cliffs is rzsponsiblefor thesepatterns. Carlquist (1974) disc~ssedother examplesof varia:ion in limb proportions. E3515 Interpre~ingthe foregoingresults is difficult, because the functional conse- - 25 : quences of morphologicalvariat.on are unknown. Further, the ecological relevance rn ; of functions1differences (assumingthey exist) is usually speculative. Nonethe- a k u- less, several studies have related limb m,xphology,functional capabilities, and .C_ : I15 7 habitat use. Laerm (1974) compared two species of basilisks which differed in 35 45 55 65 75 ,

(51 Snout-Vent Length (mm) their use of aquatic habitats. The more aquatic Basiliscusplmifrons, which has longer legsand wider toe fringes(see below), can run more quicklyon water than can B. vittarus, which is of similar size.

4 FIGURE10.7 :a) Positive relationshipbetween use ofopen microhabitatsanj relative hindleg length for 14 species of diurnal Cfenot~sskinks in 4ustralia (Pianka, 1969; revised data from Pianka, 1986, appendicesC.3 and G.3). (b) Negative relationshipbetween percentage firstseen in open and snout-ventlength, a measureof body size. (c) Deviation fromgeometric similarity (dashed line)or relationship betweenhindleg length and snout-vent length. Solidline is least squares linearregression. (d)Nonsign.ficant relationshipbetween residual percentagefirst seen in

(dl Residuol Hindleg Length (rnm) Locomotor Performancein SquamateReptiles 273 L i Williams (1972) coined the term "ecomorph" to refer to the radiation of An- olis lizards in the Greater Antilles. A set ~f morphologically distinctive species (termed ecmorphs and named for the microhabitat they most commonly use; e.g., "trunk-crown") occurs oneach of the Greater Antilles (i.e., Cuba, Hispa- niola, Jamaica, and Puerto Rico[Mayer, 1989;Williams, 1972, 19831). Compar- ison of island faunas indicates that not only are the same morphological types present on each island, but that morphologically similar specles also are similar in ecology and behavior (Losos, 1990a, b; Moermond, 1979a, b; Rand and Wil- liams, 1969; Williams, 1972, 1883). Although Anolis phylogeny is controversial (Bumell and Hedges, 1990; Cannatella and de Queiroz, 1989; Guyer and Sav- J Hlndleg Length/Sno~t-Vent Length * 103 age, 1986, ;992; Williams, 19E9), at least three independent radiations have oc- curred on Jamaica, Puerto Rico, and Cuba-Hispaniola (Williams, 1983). The ecomorph types differ morphologically in a number of characters, and figure 10.9 confirms that members of each ecomorph type are more similar mor- phologicall:/ to other members of that ecornorph on other islands than they are to more closely related species on the same island (Loso, 19921.Thus, parallel or convergent evolution has occurred. Ths ecomorphs also differ ecologically (perch heignt, perch diameter, and distance to the nearest available perch) and

L behaviorally (frequency of mohements, display rate, distance jumped, and rela- 0 a a a tive proportion of runs, jumps, and walks; Losos, 1990a, b; Moermond, 1979a, 0 a $5 45 55 65 75 b; Rand, 1964, 1967; Schoener and Schoener, 197 la, b). (b) Snout-Vent Length (mm) The "habitat matrix" model (Moermond, 1979a, b, 1986; Pounds, 1988) sug- gests that ecomorphological radiation is driven by adaptation in locomotor mor- V. phology anj behavior: Anolis alter their behavior in different microhabitats; as 50 species evolve habitat specializations they also evolve morphologies appropriate -5 25 for the behaviors they use. More specifically, the habitat matrix model predicts 0, that as the distance to the nearest perch mcreases, lizards should jump less fre- a T) 0 0 quently but over longer distances; as tne surface becomes narrower, lizards

35 45 55 65 75 should be forced to move more slowly and carefully. Consequently, limb length

IC) Snout-Vent Length (mm) should comlate with perch diameter and with distance to the nearest perch. Data from twenty-eight species of Costa Ricsn, Hispaniolan, Jamaican, and Puerto

FIGURE10.8 (a)Nonsignificant relaticnship betwecn percentage first seen in open and relative hindleg length for 12 species of nocturnal geckos ir Australia (Pianka and Panka, 1976;revised data from Piaeka, 1986,appendices C.3and G.3). Following Pianka and Pianka (1976, p. 131). two species(cpen circles)are excluded from subsequent regressionanalyses. (b) Nonsign~ficant relationship between percentage first seen in open and snout-vent length (c) Deviationfrom geometric similarity (dashed line)for relationship betweenhindleg length and snout-vent length. Solid line is leist squares linear regreszion. (d) Norsignificantof relationshi3 between residual percentages first seen in open and residual hindleg length.

(dl Residuol Hindleg Length (mrn) 274 Theodore Garland, Jr., and Jonathan B. Losos Locomotor Performance in Squamate Reptiles 275

H WW? WH W *00000000VV1VVVAAA0 0 0 correlated with limblength but not necessarily causally involved inthe morphol- PJJHPHHHPJHHP.HHPHPPHHP JHPHJ ogy + ecologyrelationship. A phylogenetically based pathanslysis (cf. Arnold, 1983) might help to tease apartthese relationships. More generally, the relationships betweenmorphology, performance,and ecology ma) not be constant across microhabitats(see "Context-Specificity of Performance" above). Rather,species mightbe adapted to perform best in their own microhabitat, and different microhab~tatsmight select fothe optimization of different performance capabilities. Performancetests made under homoge- neous conditionsmight thus obs~urewhy particular morphologiesare appropri- ate for particular "niches." A final caveat concerning the functional and adaptive significance of limb length is in order. Muth (1977, ?. 718), in a study of Callisaurus draconoides, which occupiesopen areas in ofien extremely hot North American deserts, con- cludedthat: "Long legs alsomay functionto increasethe heighi of the body in the FIGURE10.9 UPGMAphenogram of the position of Anolis lizard speciesin a multidimensional elevated posture, and to exploit the convectiveheat loss regine" (see also Ar- morphospace (fromLoss, 1992). Variables analyzedwere forelimblenglh, hindlimblength,tail length, mass, and lamellae number (all with the effectof snout-vent lengthremoved v.a nold, 1984b;Greer,1989, p. 33).Thus, 1or.g limbs may be advantageous bothfor computation of residuals fromleast squareslinear regressions), and snout.vent length ~tself. reducing thethreat from predators andforreducing heat load, both of which are Members of each ecomorph type (indicatedby the different symbols) aremore similar likely to be higher in open as compared with closed microhabitats. Giventhat morphologicallyto other members of that ecomcrph on otherislandsthanthey are to more closely- related specles on the same island. Thus, parallelorconvergent evolution has occurred. limb length nay affect severalabilities (e.g.,sprinting, climbirg, jumping,mov- ing through grass, thermoregula:ion, push-up displays), that it varies among in- dividuals and among populations (e.g., Bulova, in press), and that it correlates Rican Anolis suppcrt these predictions (Losos, 1990b, c, unpubl.; Moermond, stronglywith both body sizeandphylogeny, integrated analysesof the evolution 1979a,b; Pounds, 1988). of limb length are warranted. The predictionsof the habitat matrix are predicated on the assumption that variation in morphology affects performance,which is related to differences in Limblessness. Elongation of the body and loss of the fore-and/or hindlimbs ecology andbehavior. Studies summarizedabove (see "Morphology + Perfor- has evolved at least twelve times among squamate reptiles(Edwards, 1985). mance") support th.s assumption.Relative sprinting and jumping abilities (with With the exception of snakes, most legless squamates areeither fossorial, use the effect of size removed) are related to relative limb length. In turn, variation in burrows, or shelter under objects on the ground (Gans, 1975):Walls (1942) has performancecapability correlateswith differencesin locomotorbehavior and mi- argued that snakes evolvedfromburrowing forms. Severalforms of limbless lo- crohabitat use (Losos, 1990a,b). comotion ex~st;lateral undulation,however, is common to most limbless verte- Nonetheless, it is surprising thatonly a weak ~latjonshipwas found between brates (Gans, 1975).Undulatory locomotion is also used by some limbed absolute performance ability and ecology or behavior. One might expect that squamates, which fold their legs against :he body while moving through fluid an organism'sabsolute running andjumping abilitiesshould be important in de- (e.g., water,sand) or tangled environments.The evolutionary origin oflimbless- termining its ecology and behavior, rather than whether it can run orjump well ness appearsusuallyto be associated with:he utilization ofnarrow openingsand for its size (cf. Huey and Bennett, 1987, p. 1106; "Discussion" in Garland, crevices(Gans, 1975;Gans et a1 , 1978; Shine, 1986). although insome circum- 1994a, b). Perhaps relativelimb length affectsecology and behavior via a rela- stances nonfi~ssoriallocomotor performance maybe enhanced by using undula- tionship with someother aspect ofperf~rmance, such as endurancecr energetic tory locomotion (asin some larze Austra.ian skinks; John-Alder et al., 1986a; costs of locomotion(Autumn et al., 1994;Full etal., 1990: Full, 1991;Garland Garland, pers. obs.). An analys~sof the performance capabilities of a series of and Janis, 1993;John-Alder et al., 198ia;Strang and Steudel, 1990; references related species varying in limb dimension5 might shed valuablz light on theevo- therein). In this scenario, relativejumping and sprintingabilities would also be lution of lim~lessness. 276 Theodore Garland,Jr., and Jonathan B. Losos LocomotorPerformance in SquamateReptiles 277

In snakes, the energetic costof loccmotiond~ring lateral undulationis similar havior and ecology. Other stud,es have argued, sometimesthrough the use of to that predicted for a quadrupedallizard (or mammal)of similar size(Autumn et biomechan~calor physiological models(e.g., Emerson et al. chap. 6, this vol- al., 1994; John-Alderet al., 1986a),whereas thecostof concertinalocomotion is ume; Norberg, chap. 9, this volume; Wainwright.chap. 3, this volume),that mor- significantly higher (Walton et a]., 1950;but seeDialet al., 1987) and the cost of phology must relate to ecologj through its effect on organismal performance sidewinding signihcantly lower in at least one species (Secor et a1 , 1992). As abilities, buf have not actuallymeasured performance.The idea that morphology determined on a motorized treadmill. maximalaerobic speeds, and hence en- affects fitness and ecology only through its effects on performance hasbeen for- durance capacitiesatcertain speeds, may be rathzr low in snakes (Garland, 1988; malized in the paradigms discussed above (Arnold, 1983;Emerson and Arnold, Jayne and Bennett,1990a, b; Walton et al., 1990; but see Secor et a]., 1992) as 1989; "Introduction" above; fig. 10.1). compared with some lizardsof similarsize(e.g., Garland, 1984, 1944b;Garland The Importance of Behavior and Else, 1987;Jam-Alder and Bennett, 1981;John-Alder etal., 1936a).Part of this differencema;/ be related to temperature(cf. Garland, 1994b):existing data Studies integrating measurements of morphology, performance,behavior, for snakes have been taken at temperatures (30°C) somewhat lower than those at and ecology are rare but increasing in frequency. Those now available indicate which lizards ha~ebeen measured (35-40°Cl; however, species from both that the mo~phology+ performance+ fitness paradigm is indeed a useful one groups have been neasured at or neartheir mea2 field-active body temperature. for examining natural selectionand adaptation in the ecological morphology of reptilian locxnotorperformance. The simplicityof the paradigm makes it exper- Toe Fringes. T3e fringes, composed of laterally projecting elongatedscales, imentally tractable, but also incomplete.In particular, therole of behavior and have evolved atleast twenty-six times within seben lizard families (Luke, 1986). habitat must be considered (see "Introduc:ionn above; figs. 1C. 2, 10.3). The evolution of iringes has been associated primarilywith the occupation of By way of example, consider the role of behavior relativeto morphology in windblown sandor water habitats (Luke,1986). Presumably, fringes work by gliding reptiles. Numerous arboreal specieshave evolved structures thatincrease providing increased surface area and hence less slippage on fluid substrates surface area and hence increase gliding capabilities.However, the most wide- (Laerm, 1973), and may be more important duringacceleration than at maximal spread adaptation for increasing gliding ability is a behavioral one: when fal- speed, when slippage may be minimal (Carothers, 1986,p. 872). Carothers ling, arboreal species of squamatereptiles, amphibians,and mammalsadopt an (1986) demonstraledthat when the fringes of Uma scoparia were removed, the outstretched posture that maximizes surface area and stability (Oliver, 1951; lizards ran more slowly and with lower accelera:ion on sandy, but not on rubber, Russell, 1979). In an early study, Oliver (195 1) compared the fallingbehavior of surfaces (also seediscussion of Laem's [I9741study of basilisks under "Limb the arborealAnolis carolinensisto that of the more terrestrialSceloporus undu- Length and Habitzt Use" above). latus. The anole immediately adopted the outstretchedposition and landed rela- tively unharmed; the fencelizard, by contrast, cycledits limbs in an attempt to Conclusions. Although a wealthof data indicate that locomotor morphology run and landed forcefully. In a considerably more elegant study, Emerson and and ecology are related among reptiles, we have little hard evidence aboutthe Koehl (1990) compared the role of posture and morphologicalmodifications, causal basis of this relationship. Information on the ecological consequencesof such as flaps of skin between the legs and toes, in model treef-ogs in a wind tun- variation in performance abilitiesand whether the morphology-performance- nel. They found that the effect of behaviaral and morphologi:al features exhib- ecology relationshipis constant among habitats is necessaryto help elucidate ited by flying frog species,when tested independently,often had quite different these correlations. Such integrativestudies conductedwithin populationsare par- effects on the performance of the models Further, the effect ~f posture was de- ticularly notablein their absence. pendent on morphology. We have argued that natural selection does not act direct y on performance ability, but rather on what an organismd,>es (see "Introduction" above). Selec- Biologists have for many years gathered data documenting relationships be- tion can acton performance only when individuals are behaving in the sameway tween morphology andecology, as several chapters in this volume attest. Some (e.g., trying to escape from a predator by running away as quickly as possible) studies merely describe correlationsuithout consideringdirectly the mechanism and some individuals are better than others, due to their higherperformance abili- by which morphology, physiology, and biochemistry are transduced into be- ties; otherw.se,selection will adon the differencesin behavior.Thus, behavior is 278 TheodoreGarland, Jr., and Jonathan B. Losos Locomotor Perfarmancein SquamateReptiles 279 a filter through which performance is related to fitness (Garland et al., 1990b), Christian and Tracy, 1981 ; Grant, 1990; Grant and Dunham, 1988; Hertz et al., and performanceis itself a filter through which morphology is transduced(cf. 1988).As the jay proceeds, thethzrmal regimen of microenvironmentschanges, Ricklefs andMiles, chap. 2, this volume) to determinebehavioral options(Gar- and the lizards tend to alter theirposition tomaintaintheir temperature. The role land, 1994a). Behallior can affect the performance+ fitness link intwo general of the structural environmentis apparent in Anolis communities, where species ways: by negating advantages inperformance ability, and by compensatingfor tend not (butsee Huey, 1983)to use habitatsinwhich their locomotor abilitiesare decrements in abilily. compromised(see above, "Limb Length and Habitat Use"). An example of behavior makingperformanc: differences irrelevant ispre- Evolutionary adaptationis also mediated via habitat use(Dunson and Travis, sented in a study of crypsis in the Pacific treefrog, Pseudacris regilla which oc- 1991;Huey, 1991). In Anolis lizards, for example, the optimal temperature for curs in two color morphs, green and brown. Morzy (1990) investigakdwhether locomotorperformance has apparently evolvedto match the thermalregimen of frogs would choose tosit on substrates matching their color, and whether sub- their environment (van Berkum, 1986), although some agarnid, scincid, and strate matchingaffects susceptibility'to predation by garter snakes,Thamnophis Sceloporus lizards are more conservative(Crowley, 1985a;Gar and et a]., 199 I; elegans, in laboratory trials. Individua frogstended to selzct substrates match- Hertz et al., 1983; van Berkum, i988). Similarly, the habitat matrix model (see ing their own color.Laboratory trials wsre conductedin which one frog matched above) predicts that species utilizing diffe~ntmicrohabitats will alter their be- the substrateand a seconddid not. Indeed,in the ten trials in which frogs did not havior accordinglyand that apprcpriate morphologies willevolve subsequently. move, the snake ctose the nonmatching frognire times. However, in eighteen Caribbeananoles exhibit all three componentsof the model: they shift habitat use trials, one of the Frogs moved and was immediately attacked regardless of in responsetoa number of factors,including climate and the presence of compet- whether its color matched the background. In this example color gives a perfor- itors (e.g., Moermond, 1986; Schoener and Schoener,197 1 a, b; and see above); mance advantage,crypsis, which leads to increased prey survival only when alter their locomotor behavior in different environments (Losos,1990a; Moer- coupled with the appropriatebehavior (nonrnovement). mond, 1979a,b; Pounds, 1988);and have evolved appropriatemorphologies for That alterations in behavior can compensare for decreased performance their locomotor behavior (see above).Behavioral changes do nct always precede ability has been demonstrated in several contxts. Lizards compensate for changes in morphology and perf~rmanceabilities, however (cf. Burggren and diminished locomotor abilities at lower body temperatures either by increasing Bemis, 1990,p. 221). For example,Russell (1979) has shown that the enlarged their approach distance(i.e., the distance at which they will flee from a potential lateral body folds usedby some geckos in parachuting prcbably originally predator) (Rand, 1964; Shallenberger, 1970;but see Bulova, in press) or by evolved to ennance crypsis (i.e., they are an exaptation,sensu Gould and Vrba, switching from flight to aggressive defense(Crowley and Pietruszka, 1983; 1982). Similarly, the ability to flatten dorsoventrallyin Leiolcpis belliani may Hertz et al., 1982: see also Arnold and Bennett, 1984; Schieffelin and de Quei- have evolvedeither as a means of thermoregulation or for social displays; the roz, 1991). Lizardsand snakeswith decreasedlocomotor abilities dueto tail loss gliding ability that it entails seemsof little significance to this beach-dwelling (Ballinger, 1973; Dial and Fitzpatrick, 1984;Formanowicz et al., 1990), grav- lizard (Lososet al., 1989).Similarly, the evolutionof long legsfor thermoregula- idity (Bauwens and Thoen, 1981; Formanowicz et al., 1990), a full stomach tory purposes (cf. Muth, 1977; see above, "Limb Length and Habitat Use") (Herzog and Bailey, 1987), or exhaustion (Arnoldand Bennett, 1984; Garland, might preadapt a lizard for the evolution of nigh sprint speed (cf. Gans, 1979, on 1988) similarlyalter their behavior. In some casss, thesebehavioral shiftsmay "momentarilg excessive construction"). Finally, the agamid Calotes versicolor suffice to eliminate completely theeffect of decreased periormance on survival has the ability to swim effectively, but when dropped in water, it swims effec- (references in Brodie, 1989a; but sze references in Cooper et al., 1990; tively for a few moments and then becomes disoriented, cyclesits limbs ineffec- Schwartzkopf and Shine,1992). tively, attempts to breathe while underwater, and eventually sinks and walks Behavior also asts as an intermediate filter inthe performance+ fitness link around aimlessly on the bottom (Gans, 1977)! Apparently, this lizard has the in the context of hebitat selection. For example,performance is clearly context- functional ability to swim, but not the appropriate behaviorto use this ability. dependent-maximal capabilitiesare only valuable in habitats in wh~chthey can Trade-offs and Correlationsof Locomotor Abilities be used. Consideringthe thermal environment,Waldschrnidt andTracy (1983) demonstrated that Uta stansburiuna lltilize microhabitats that allow them to Potential trade-offs and constraintsare of major concern in evolutionarybiol- maintain body temperaturesat which tley can sprint fastest(cf. Adolph, 1990a; ogy, behavio~alecology, and comparativemorphology and physiology(e.g., Ar- Locomotor Performancein SquamateReptiles 280 TheodoreGarland, Jr., and Jonathan B. Losos 281

most heritable traits within populationsofmany species (Falconer, 1989). In the nold et al., 1989; Barbault, 1988; Carrier, 1987, 1991; Congdon and Gibbons, case of arboreal or cliff-dwe1lir.g (cf. Kramer, 1951)species, however, an in- 1987; Derricksonand Ricklefs, 1988; Feder and Londos, 1984;Garland and crease in body size might be selected against,resulting insteadin an evolutionary Huey, 1987; Grant and Dunham, 19E8; Halliday, 1987; Maynard Smithet a]., increase in limb length. 1985; Miles and Dunham, 1992; Moermond, 1979b; Rose et al., 1987; Shine, rtlative 1988; Sinervo andLicht, 1991; Townsendand Calow, 1951). With respect to lo- comotion, performance of several functions may be correlated if the functions Our understandingof the ecological morphologyof reptilian locomotor per- share a common mechanistic basis(cf EmersonandKoehl, 1990).Such correla- formancehas increased greatlyin the last decade. Many data have been gathered tions may limit pctential evolutionarypathways and prevznt taxa from optimiz- and a unified and general theoretical frameworkis coming into existence. This ing several performance abilitiessimultaneonsly (cf. Arnold, 1987, 1988; framework envisions measures of whole-animalperformance ascentral for at- Brodie and Garland, 1993; Emersonand Arnold, 1989). However, predictingthe tempting tolink morphological,physiological, or biochemicalvariationwith be- existence of trade-offs basedon first ~rinciplesis not always easy.For example, havior, fitness, or ecology. Nevertheless, many relatively simpleideas and contrary tosimple models suggestingi necessary trade-offbased on a dichotomy hypotheses remain untested or understudied, forexample, whether a trade-off of fast versus slow muscle fiber types (cf. Gans:t al., 1978; Pennycuick, 1991), speed and stamina are not negativelycorrelated at the lewd of individual varia- between spezd and stamina is ineluctable whetherand why limb length corre- tion (Garland, 1984, 1988; Garlandand Else, 1987; Jayne and Bennett, 1990a; lates with h~bitatcharacteristics; the selective importanceof ability to recover Secor et al., 1992), nor are they negatively genetically correlated in either from exhaustive exercise(cf. Gatten and Clark, 1989; Galten et al., 1992; Thamnophissirtalis (Garland, 1988;see also Br~die,1989b, 1992, on speed and Gleeson, 1991 ; Pough et al., 1942); and possiblerelationships between locomo- tor abilities,vagility, and genetic variation(Gorman et al., 1977). Entire groups distance crawledin T. ordinoides)or Sceloporusoccidentalis (Tsuji et al., 1989). of reptiles are virtually unstudied (e.g., turtles; but see Dial, 1987;Janzen, 1993; Among species of Anolis, sprinting, jumping,and cl~ngingability are pos- Miller et al. 1987; Wyneken and Salmon, 1992; Zani and Clausen, in press). itively correlated, in part because all increase with body size (Losos, 1990b, c). Studiesof performance gradients, relating individualvariation in morphologyto With the effect af size removed by computing residuals, however, relative performance, have been quite s~ccessful,but can become much more sophisti- sprinting and jumping abilityare still positively correlated, presumably due to cated (cf. work in mammalian exercise pl-ysiology). Fitness gradients,relating the positive relationshipof both to relative h.ndlimb length (Losos, 1990~). performance to fitness within populations, are starting to be quantified.How- These correlations suggest that theevolution of sprintingand jumping ability is ever, quantitative dataon field behavior, as derived from focal animal observa- likely to be tightly linked. Consequently, the ability of Anolis to adapt in some tions, are uncommon, makingit difficult to identify possible selective agents ways to particular microhabitats may be constrained. Similarly, anole species responsible for correlationsbetween laboratory locomotor performance andfit- adapt to utilize narrow surfaces such as twigs by evohing short limb length ness/behavior/ecology.The lackofquantitative dataon field behaviorlimits both (Losos, 1990a; Williams, 1983), thus trading the ability to move quickly on comparisons amongspecies and studies of natural selection (Eennettand Huey, broad surfacesforenhanced ability to move witkout difficulty on narrow surfaces 1990; Garland, 1993; Pough, 1989). For example, it has never even been docu- (Lososand Sinervo, 1989). As a result, anolescannot adaptto utilize narrow sur- mented thatlizards with greatercapabilities for sprinting (as measured in thelab) faces andstill be zble to make long jumps between perches. actually run fasterin nature (cf. Garland, 1993; Hertz et a]., 1988). Trade-offs may also occur between differen:types of performance. Chame- We predict that the next dechde will continue to see exciting empirical and leons, for example,have specialized for one locomotor task, graspingand mov- conceptual advances, aimedprimarily at understanding the evolution oforganis- ing upon extremely narrow surfaces,at the expense of another, sprint speed. ma1 performance (cf. Garland a3d Carter, 1994).Techniques for sophisticated Presumably, changesin the muscle architecturehave played an important role in measurements of locomotor peformanceand for quantitative genetic (Boake, mediating this trade-off (see also Abu-Ghalyunet al., 1988). 1994;Brodieand Garland, I993)andphylogenetic analysesare now in place and Ecological circumstances mayalso dictate when correlationsarise and when awaiting integrated application. At present, these techniques are still novel they are broken. For example, changein body slze may be the path of least resis- enough to merit study in their own right. Soon, however, state-of-the-art studies tance when selection is for increasedspeed, generating among-population cor- will involve experimental, quantitative genetic,and phylogenetic analyses of relations of all traits that scale with :ize. Indeed, body size is often one of the 282 Theodore Garland, Jr., and Jonathan B. Losos Locomotor Performance in Squamrte Reptiles 283 measurements of morphology, performance,behavior, and fitness (or "adapted- or rare, strong or weak, directional or stabilizing. (Unfortunately, quite large ness," when comparing populationsor species). samples may be required to detect weak selection, although power canbe en- In several cases, certain data setsalready exist in partial form; these matrices hanced by experimental manipulations [Sinervoet al., 19421.) Of particular can be filled in relatively easily. Forexample, relatively standardizedtechniques interest would be studiesin which traits atdifferent levels of b.ologicalorganiza- for measuring sprint speed have now been de~eloped,and data on maximal tion are measured simultaneously, suchas antipredatordisplay, speed, and scale speeds are now availablefor more thanonehundred speciesof lizards;it is time to counts in garter snakes or body mass, relative limb lengths,and endurance In relate such data to morphology andto behavior and ecology (cf. Garland et a]., lizards (cf. Lauder, 1990).Only these kinds of studies cantell us whether selec- 1988; GarlandandJanis, 1993;Janis, in press; Losos, 1990b,c). In many cases, tion really isstronger for behavior and performance than forlower-level traits(cf. the most outstandingneed is for quanti~ativedataon field bzhavior.Comparisons Garland et al., 1990b).Interestingly, Jayne and Bennett(l99Clb) report selection would be greatly fzcilitatedby standardizationof methods for taking quantitative intensitieson locomotor performancein snakes similar tothosz reported formor- measurements of ccology and behavior (e.g., home ranges, movement rates, phometric traits in birds. Such studiescan also tell us whether selection is distances, speedsi? nature;cf. Case, 1979;Coop and Gulllette, 1991 ; Garland, correlational, favoring, forexample, particular combinations of behavior and 1993; Huey and P~anka,198 1; Magnusson et al., 1985; Moermond, 1979a, b; morphologylphysiology(cf. Br,sdie, 1989b;Garland, 1988,1994a, b; Huey and Pietruszka, 1986). Anotherunresolved issue isthe extent of behavioral compen- Bennett, 1937), and informing 1s about the form of the fitness function (cf. fig. sation for changes in performance due to a full stomach,gravidity, or lowered 3.4 in Feder, 1987;Schluter, 1958). Finally,we might test whether selection ever body temperature. Behavioraladjustmznts related to changesin performancedue acts directly on morphology (cf. fig. 10.4), although unmeasured characters to size and/or age also warrant study(cf. Grand, 1991;Pough and Kamel, 1984; could confc~undsuch analyses (Lande and Arnold, 1983; Mitchell-Olds and Pounds et a]., 1983; Taigen and Pough, 1981).How often does behavior shield Shaw, 1987,Wade and Kalisz, :990). performancefrom the direct effectsof selection (fig. 10.2;Garland,1994a; Gar- Although not aneasy task, especially with the current difficulties in obtaining land et al., 1990b)? long-term funding, somestudies of natural selection shouldbe carried out for Future comparative studies mustdeal directly with phylogenetic effects multiple years (cf. Grant, 1986;Grant and Grant, 1990;Hueg et al., 1990). De- (Brooks and McLznnan, 1991; Garland et al., 1991, 1992, 1993; Harvey and tection of rare events may be difficult (Buffetaut, 1989; Weatherhead,1986), but Pagel, 1991 ; Laud-r, 1991; Losos and Miles, chap. 4, this volume; Lynch, 1991; their potential selectiveand hence evolutionaryImportance (Grant, 1986; Wiens, Miles and Dunharn, 1992; Pagel, 1995).As well, many existing studieswarrant 1977;Wiens and Rotenbeny, 1980) dictates thatsubstantial effort be expended to reanalysis with phylogenetically based methods. Computer programs are now study them. availableto do so (e.g.,Garland et al., 1993; Lynch, 1991;Martins and Garland, Anotherimportant direction forstudies of natural selectionis toward experi- 1991;A. Purvis, pers. comm.), and there is no excuse for not attempting to uti- mental man!pulation to extend the range of natural variation andlor to diminish lize whatever (even incomplete) phylogenetic information is available(Harvey correlations between independentvariables (e.g., performan:e and body size). and Pagel, 1991 ; Punis and Garland, 1993).This historicalcontext may be par- Such manipulationscan improve statisticalpower to detectselection acting on ticularly important for investigationsconcerning the ecomorphologyof reptilian individual traits as well as allowing hypothesessuggested by comparative an- locomotion,because many aspectsof morphology, performance, and foraging alyses to beexperimentallyprobed (Baum andLarson, 1991; Mitchell-Oldsand mode seem strongly associated with phylogeny inboth l~zardsand snakes (cf. Shaw, 1987;Sineno, 1990; Sinervoand Huey, 1990, pers.cornm.). Hormonalor Miles and Dunham, 1992). As well, many morphologicalbases-such as limb- pharmacological manipulation,for example, could be used to change perfor- lessness and toe fringes, and behavioral1ecologicaIcorrelates such as active mance capacities of individuals, after which one could test for correlations foraging-of locomotor performancehave evolved many limes independently in between pe~formanceand survivorship in the field (Joos and John-Alder, 1990; reptiles. John-Alder, 1990, pers. comm.;John-Alder etal., 1986b).Though probably im- More studiesof natural selectionacting on individual differences withinpop- practical wirh reptiles, geneticperturbaticn experiments todetect selection have ulations shouldbe done. The available data base for reptilian locomotor perfor- been succes~fullyperformed with invertebrates and with mice (Anderson et al., mance is exceedinglysmall (see Bennett and H~ey,1990; Brodie, 1992; Sorci et 1964; Hedrick, 1986). al., in press). We need to know whether selection on performanceis pervasive Studiesof natural selectionshould be integrated with estimates ofheritabilities 284 TheodoreGarland, Jr., and Jonathan B. Losos LocomotorPerformance in SquamateReptiles 285

in nature (cf. Riska et al., 1989), to allow both prediction andrecor.struction of Bennett, S. J. Bulova, M. R. Dohm, D. L Gregor, K. L. Steudel, D. B. Miles, microevolutionaryphenomena(cf. S. J. Arnold, 1981, 1988). Estimation of field and the editors of this volumekindly reviewedthe manuscriptor provided help- heritabilities (fromfree-living animals) is difficult but important, as field heri- ful discussions. Supportedin part by N.S.F. grants BSR-9C06083 and BSR- tabilities may be considerablylower than those obtainedin the laboratory(but see 9157268to TG and BSR-89012Cl5to JBL and H. W. Greene. Hedrick, 1986,pp 552-3). Correlationsbetween morphologysnd ecology, and trade-offs anc constraints

in performance,can be studied at mulliple levels, yet integrativestudies are un- Abu-Ghalyun. Y.,L. Greenwald, T. E. Herheringtcn, and A.S. Gaunt. 1988. The physiological common (Emerson andArnold, 1989;Sinervo, 990; Sinervo and Licht, 1991). basis of slow locomotion in chamaeleons.J. Exp. Zool. 245:225-231 Adolph, S. C. 1990a. Influence of bshavioral tkrmoregulation on miclohabitat use by two Given the growing information on interspecific variation, quantitative genet- Sceloporus izards. Ecology 7 1:3 15-327. ics, and physiological basesof locomotor performance, we anticipate studies Adolph, S. C. IY90b. Perch height seleclion by ~uvenileSceloporus Ilzards: intcrspecihc d~fferenceb in which physiologicaland biomechar-icalmodels are used to predict trade-offs and relationship to habitat use. Journal of Herpetology24:69-65. in locomotor capacities, whichare then tested, at complementar). levels, by Alexander, R. McN. 1968. Animal MecLanics. Seatt.e:University of WashingtonPress Ananjeva, N. B. 1977. Morphometrical analysisof limb proportionsof five sympatrlc species of quantification of (1) genetic correlations with,n popularions (e.g., Garland, desert lizarcs(Sauria, Eremias) in the southern Balkhash Lake region. Pioc. 2001. Inst. Acad. 1988) and (2) "evolutionary correlations" through interspecificcomparative Sci. USSR 74:3-13. studies (Garlandet al., 1991, 1992;Garland and Janis, 1993; Harvey and Pagel, Ananjeva,N. B , and S. M. Shammakov. 1985. Ecol~gicstrategies and relati\e clutch mass in some species of lirard fauna in the USSR. Jov J. Ecol. 16:241-247. (Englishtrinslation of Ekologiya 1991; Lynch, 1991; Martins and Garland,1991; Pagel, 1993). Such studies may 4:58-65) also allow inferences concerningpast patterns of (correlational)selection within Anderson. P. K., L. C. Dunn, and A. E.Beasley. 1964. Introductionof a lethal allele into a feral populations (S. J. 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Cambridge:CarnbridgeUniversity Press. Arnold, S J. 1988. Quantitative genetl:s and aelection in natural populatiols. Microevolutionof vertebral numbers ~nthe garter snakeTharnnophi: elegans In Proceedrngsof the Secondlnrerna- tional Confrrence on Quantitative Generics,ed. B. S. Weir, E. J. Eisen, M.J. Goodman, and We thank Craig James for providing an unpublished portion of his thesis, G. Narnkoolg,619-636. Sunderland, MA:Sina~er Associates. Arnold, S. I., and A. F. Bennett. 1984.Behavioural 'lariation in natural popul~tions.111. Antipreda- A. F. Bennett and R. B. Huey forproviding copiesof unpublished manuscripts, tor displaysin the garter snakeThamophis radi~.Anim. Behav. 32: 1 10811 18. and Eric Pianka forprovidinginformation. S. C. Adolph, R.A. Anderson,A. F. Arnold, S. J., and A. F. Bennett. 1988.Behavioral variation in natural populations.V. Morphologi-

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