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Female mate attraction in ornate tree lizards, Urosaurus ornatus: a multivariate analysis
ANIMAL BEHAVIOUR, 2005, 69, 219–224 doi:10.1016/j.anbehav.2004.03.011
Female mate attraction in ornate tree lizards, Urosaurus ornatus: a multivariate analysis P AU L S. H AM ILTON * & B RIAN K. SULLIVAN†
*Department of Biology, Arizona State University, Tempe yDepartment of Life Sciences, Arizona State University West, Phoenix (Received 19 February 2003; initial acceptance 9 May 2003; final acceptance 12 March 2004; published online 26 November 2004; MS. number: A9561R2)
Recent reviews of mate choice have concluded that this phenomenon is rare or nonexistent in lizards. However, direct tests of lizard mate choice are few and generally limited in scope. We present results of a mate choice experiment with Urosaurus ornatus in which two male lizards differing in morphology, colour and behaviour were given the opportunity to attract a female lizard. Pairwise comparisons of selected and unselected males revealed that variation in individual traits failed to account for much of the variation in mate attraction success. However, a multivariate analysis revealed that mate attraction was related to multiple cues from a male’s phenotype: body mass and head size as well as body and tail coloration all contributed to mate attraction. We argue that the additive and interactive effects of several traits combined may be more important than single traits in mate choice. We suggest that mate choice studies should account for multivariate effects of male traits, and also allow mate attraction to occur over variable spatial and temporal scales, paralleling mate choice under natural conditions. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Although mate attraction and mate choice have been demonstrated in a wide variety of animals, ranging from Drosophila to Homo (reviewed in Andersson 1994), some groups have received little attention. For instance, relatively few studies have been conducted with lizards (e.g. Olsson 1993; Baird et al. 1997; LeBas 2001; LeBas & Marshall 2001), and many of these have focused on one particular trait (e.g. dewlap, Tokarz 2002) or tested only one model of sexual selection (e.g. sensory exploitation, Olsson 2001). Despite the limited scope of most studies, some authors have argued that negative results indicate that female lizards rarely, if ever, choose their mates (Olsson & Madsen 1995; Tokarz 1995). However, in the absence of an examination of several of the potential factors involved in mate choice, and without restriction to a particular model of sexual selection, such a conclusion is premature. Also, without examining many of the phenotypic traits potentially involved in mate attraction, mate choice cannot be excluded in any given species. Recent studies have highlighted the importance of multiple traits in mate choice (e.g. Marchetti 1998; Calkins & Burley 2003; reviewed in Candolin 2003). This
Correspondence: P. S. Hamilton, Department of Biology, Tempe, AZ 85287-1501, U.S.A. (email: [email protected]). B. K. Sullivan is at the Department of Life Sciences, Arizona State University West, PO Box 37100, Phoenix, AZ 85069, U.S.A. 0003–3472/04/$30.00/0
approach represents a departure from classic mate choice studies that focused on single traits with presumed a priori significance in mate attraction (Andersson 1994). Negative findings in such studies have often been interpreted to mean that mate choice is absent in a given taxon. Indeed, recent theoretical work has focused on explanations for secondary sexual traits that appear not to be favoured by females (Holland & Rice 1998). Signal redundancy has also been proposed to explain such patterns (Møller & Pomiankowsi 1993; Partan & Marler 1999). Alternatively, an examination of multiple traits simultaneously may find that each trait in a suite of characters conveys novel information, or that the interactive effects of multiple traits may be more important than their individual contributions (Møller & Pomiankowsi 1993; Jennions & Petrie 1997). Clearly, a ‘one trait at a time’ paradigm in mate choice studies does not allow for examination of such ideas. Furthermore, this paradigm may lead to a premature conclusion that mate choice is completely lacking in a taxon, rather than simply not acting on a single isolated trait. Lizard display behaviour, including species-specific ‘pushup’ displays, is generally assumed to have a role in mate recognition, but few studies have directly tested this assertion (Jenssen 1970; Tokarz 1995). A field study of sexual selection (Hews 1990) demonstrated that head and body size are important in lizard sexual selection, but laboratory experimental studies have not yet found a link
219 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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between these morphological traits and mate attraction or mating success. Phrynosomatid lizards, including U. ornatus, have been the subject of numerous studies on male– male signalling. Several of these studies have implicated dorsal (Zucker 1994) as well as throat (Hover 1985; Thompson & Moore 1991) ornamentation as important indicators of male dominance. However, the role of these ornaments in mate choice remains largely unknown (but see Cooper & Burns 1987, regarding ventral ornaments in Sceloporus undulatus). Extreme phenotypic variation in ornate tree lizards, Urosaurus ornatus (see below), offers an ideal opportunity to examine the multivariate influences of colour, morphology and behaviour on the ability of males to attract potential mates. Herein, we examine the influence of multiple male traits on female mate attraction in U. ornatus.
MATERIALS AND METHODS Beginning in 1999, we monitored ornate tree lizards, Urosaurus ornatus, in the western foothills of Sierra Estrella, Maricopa County, Arizona, U.S.A. (33 210 340 N; 0 0 112 22 25 W), as part of a longitudinal study of sexual selection in a natural population. This area consists of lower Colorado Sonoran Desert dominated by saguaro, palo verde, creosote and bursage; U. ornatus generally occupy boulder outcrops in this region. For each mate choice trial, two males and one female were chosen randomly from recently collected field animals from areas near the primary study site. Prior to trials, animals were housed individually in 38-litre aquaria under full-spectrum lighting and a thermal gradient provided by a heat lamp on one side of each tank. Crickets, Acheta domestica, dusted with vitamin supplements and water sprayed in each tank were provided ad libitum. To avoid pseudoreplication, lizards were used only once in trials. A total of 48 trials were completed in 1999 and 2000. Trial arenas (Fig. 1) consisted of approximately 20-cmhigh aluminium sheeting that formed two 4 ! 4 m outdoor arenas on soil. Three rock piles were placed in each arena to serve as starting positions for each of the three lizards. These rocks were taken from boulder habitats where lizards were collected and represented the colour and thermal microhabitats in which lizards were found. Rock piles of the two males were visually separated from each other by a sheeting barrier. The two males were tethered with clear monofilament around the waist. These 1-m-long tethers were attached to a pole directly over each male. Each male could move freely on his rock pile perch, but could not approach the female or the other male. Trials were completed during peak mating times for U. ornatus in the source population, late April through June, and in peak times of day for activity, immediately after dawn or immediately before dusk. The two males were given at least 20 min to acclimate to the arena before starting a trial. A trial began when the female was placed in the arena. An observer remained relatively motionless outside the arena and recorded male and female behaviours until the female directly approached one male or the other. We used a female’s
4m
Female
4m
Male 1
Male 2
Figure 1. Schematic of mate choice enclosure. Lines represent aluminium flashing and circles represent areas in which each male could freely move.
approach to one male or another as a proxy for mate choice by females (see ‘Results’ for descriptions of female approach behaviours).
Phenotypic Measurements At least 48 h prior to conducting mate choice trials, males were restrained against a neutral grey surface and photographed ventrally and laterally. Film transparencies were digitally scanned and calibrated for hue and spatial scale using a colour standard (GretagMacbeth 1998) and a millimetre ruler, respectively. Hue was calibrated with the ‘Calibrate’ option of Scion Image software (ScionCorp 2000), using a digital layer representing wavelength as optical density. This function produced a calibration regression between the colours of known hue from the standard and the hues in a digital image of the standard. This calibration regression was then applied to lizard photographs to obtain a corrected hue for throat colours. Optical density of the hue layer of lizard photographs was converted to a 1–360-degree Munsell hue score, with ‘1’ representing far blue wavelengths and ‘360’ representing far red. For morphological measurements, spatial scale of photographs was calibrated using the ‘Calibrate Spatial Measurements’ option in ImageTool software (UTHSCSA 2002). These colour and morphology methods are treated in more detail elsewhere (unpublished data). Morphological measurements obtained from standardized images included snout–vent length (SVL), head width (HW, the linear distance between the anterior edges of each tympanum), head length (HL, the linear distance between the tip of the snout and the midpoint between the anterior edges of the two tympanum), and head depth (HD, the vertical distance between the lower edge of the tympanum and the dorsal border of the head). The three head measurements were taken at Cartesian angles to one another, and thus represent mathematically independent
HAMILTON & SULLIVAN: MULTIVARIATE MATE CHOICE IN LIZARDS
measures of head size, without angular dependencies of one measurement on another. The areas of three ventral display patches were measured from standardized ventral photographs: the blue ventral trunk display patches, and two throat patches (see below). Also, the hue of each of the two throat patches was measured as above. Ornate tree lizards from some populations have at least two distinct colour badges on their throats, which have been implicated in social signalling among males (Thompson & Moore 1991). Some individuals have only a single throat colour (usually orange), whereas others also have a distinct central patch of blue or green. However, the U. ornatus at our study site often did not fall easily into either of these categories and sometimes had indistinct central colours. So, rather than typing these lizards into dichotomous colour morphs, we analysed throat colour with two continuous variables: the proportion of surface area of the central throat patch relative to that of the total throat patch, and the difference in hue between the central and outer portions of the throat patch (in colour degrees). The extremes in these continuous variables roughly correspond with the dichotomous types described previously (unpublished data). Males of U. ornatus used in this study also varied in the number of blue scales on the lateral surface of the tail. We counted 50 of the most proximal tail scales on the left side, and recorded the percentage of blue scales. Whether or not the tail had been broken and regrown was also recorded. All male lizards used had intact or completely regrown tails. During trials, we recorded the number of pushup displays performed by the males before a female approached either male. Display rate greatly increased after a female approached, so these postapproach displays were not counted. Males also occasionally performed two variations on the pushup display, the ‘shudder’ (a rapid dorsoventral vibration of the head) and the ‘fullshow’ (a pushup with lateral compression). Shudder displays are used primarily in courtship, but were only performed in two trials before a female approached a male, and thus were not analysed. Fullshow displays are, like pushups, performed in multiple social contexts, and thus were lumped in with pushups to calculate an overall display rate. Last, we recorded the proportion of time a male stayed in front of his perch in view of the focal female.
Statistical Analysis Several traits (head dimensions, belly patch size and mass) were significantly correlated with SVL (results not presented). For these traits, residual values from regressions on SVL were used in pairwise analysis. We analysed phenotypic differences between pairs of lizards (winners and losers in attracting females) with paired t tests when meeting parametric assumptions. Otherwise, we used Wilcoxon matched-pairs signed-ranks tests or a sign test. To address the multivariate relationship among male phenotypic variables and male attraction to females, we used multiple logistic regression. In this analysis, for each variable, we calculated the difference between the value of
the male on the left side of the area and the one on the right. Thus, each pair of lizards had a single variable to enter into the equation. We then performed multiple logistic regression with the trial outcome (win or loss) of the left lizard as the dichotomous dependent variable, with the 12 difference scores as independent variables. Raw values (i.e. not residuals) were used for all traits in this analysis. Although prior work suggested that larger and more colourful males should be preferred by females (reviewed by Kodric-Brown & Brown 1984; Andersson 1994), we used two-tailed tests in assessing female mate choice of male size, behaviour and colour variation.
RESULTS Trials averaged 49 min (range 4–192 min) and lasted until a female ran to a male’s rock pile or lizards became inactive. In 12 of 48 trials, females did not move directly towards either male, but rather ran towards an arena wall away from the males. These trials were excluded from further analysis. In one trial, the female attacked the smaller of the two males presented to her, and this trial also was excluded. In the remaining 35 trials, females ran directly to the perch of a male, usually in a straight line from her starting perch. However, in some trials (N Z 11), females ran to one side of the arena or another (i.e. not directly to a rock pile), and then subsequently moved to the perch of a male. To address the possibility that these females were simply running in a random direction and happened to end up on one side or the other, each of these 11 trials was rerun. In each of these cases, the female ran towards the same side of the arena, suggesting that the movement was not random (binomial test: P Z 0.0005). To further address repeatability, the eight trials run in 2000 were redone with the same animals on different days. In this second set of trials, we used a different arena and switched the relative positions of the males (right or left). In six of these trials, the female moved towards the same male in both trials, despite the new arena and side. In one case she moved towards the other male, and in another, she failed to move towards either male on the second trial. Excluding this last case, the binomial probability of six of seven trials repeating the same outcome is 0.055. Hence, females were generally consistent in their selections, and a bias towards one side of the arena or the other was not apparent. We included only the first selection of these trials in subsequent analysis. Selected males tended to have larger bodies, greater head depth, and more blue scales on their tails (Table 1, Fig. 2). However, when controlling for an experimentwide error rate, none of the univariate comparisons remained significant (Bonferroni, P O 0.05 in all comparisons). Overall, nine of 12 comparisons were in the predicted directions: selected males usually had the larger or more conspicuous trait, or an intact tail. Logistic regression revealed that the outcome of a trial could be predicted well with the combined effects of multiple phenotypic variables (Model Nagelkerke R2 Z 0.691, P Z 0.016; Table 1). The logistic regression model correctly predicted the outcome in 30 of 34 trials (88%).
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Table 1. Male traits evaluated in mate choice trials with female Urosaurus ornatus and the statistical comparisons used to assess selected males in relation to unselected males in paired trials Male trait SVL Mass* HW* HL* HD* Belly patch size* Throat hue contrast Throat size Tail blue Tail break Display rate Time in view
Test
P
P (logistic)
Paired t Paired t Paired t Paired t Paired t Paried t Wilcoxon Wilcoxon Paired t Sign Wilcoxon Wilcoxon
0.053 0.594 0.396 0.463 0.097 0.337 0.304 0.144 0.068 0.454 0.238 0.750
0.133 0.057 0.362 0.742 0.089 0.060 0.918 0.338 0.053 0.226 0.367 0.666
SVL: snout–vent length; HW: head width; HL: head length; HD: head depth. Residuals on body mass were used in pairwise tests for those variables marked with a ‘*’. Raw values (i.e. not residuals) were used for all variables in the logistic regression analysis.
Some of the same variables (e.g. head depth and blue on tail) implicated in univariate analysis were also implicated with this method. In addition, body mass and belly patch size were identified as indicators of male success in the logistic analysis. Interestingly, the trend with body mass was opposite to that expected; females tended to choose thinner males (Fig. 2). However, as in the univariate tests, of the individual variables in the logistic regression were not statistically significant in this second analysis.
DISCUSSION We found that selected males had deeper heads (HD), were thinner (mass), and more brightly coloured (blue on tail, belly patch size) than males that were not selected. However, the contribution of each of these variables independently was negligible, and a pattern was only evident with a multivariate examination of all traits simultaneously. Indeed, when we examined each trait individually, no single trait attained statistical significance. Thus, as in previous univariate studies, an examination of individual traits yielded negative results. However, when considered together in a multivariate analysis, the combination of characters contributed to mate attraction success. Male lizards with large heads and bodies have been repeatedly shown to benefit in male–male contests (e.g. Hews 1990; Baird et al. 1997). A number of studies of lizards also have documented a mate association benefit for large males (e.g. Cooper & Vitt 1993; Salvador & Veiga 2001), and in some of these, a role for female mate choice has been directly supported (Censky 1997). Hews (1990) documented selection acting on male head depth in Uta palmeri, an insular phrynosomatid, but sexual selection in this trait was shown to occur through male–male competition rather than female mating preferences. Our results provide one of the first suggestions of sexual selection acting on both head and body size through female choice. Although body mass was not significant by itself, females
tended to choose thinner males, which is a departure from theoretical expectations and empirical precedents. Head and body size in many Carribean anole lizards have been thought to be shaped by ecological selection (Schoener 1967), and sexual selection has sometimes been considered a less likely explanation for sexual dimorphism in these traits (Shine 1989). By contrast, the current findings suggest that sexual selection may in fact be an important cause for such dimorphism. Numerous studies have addressed the role of lizard colour in sexual selection. Most of these studies have focused on single characters such as throat colour (Thompson & Moore 1991; Sinervo & Lively 1996; Smith & Zucker 1997), dewlap colour (Sigmund 1983), body colour (Olsson 1994; Zucker 1994; Baird et al. 1997), or tail colour (Kwiatkowski & Sullivan 2002). Although some colour traits, particularly throat or dewlap colours (Thompson & Moore 1991; Sinervo & Lively 1996) have been implicated in male–male competition, relatively few investigators have directly addressed the role of these colours in mate choice (but see Smith & Zucker 1997). In addition to morphology, we found that male coloration played a role in attraction of females. Of the colour variables measured, blue scales on the tail and the size of belly patches were most conspicuous to human observers, and these were also traits implicated in mate attraction. This is one of the first studies documenting a female preference for more conspicuously coloured males (see also Kwiatkowski & Sullivan 2002). This is somewhat surprising given the number and diversity of colour badges in many lizards and hypotheses concerning their evolution (e.g. Wiens 1999). Unlike belly and tail colours, throat colours were not found to influence mate attraction. However, these subtle throat colours were probably not discernable to females from their starting positions in our arena (ca. 2.5 m). Future studies may address these potentially important colours by the use of close-range discrimination trials and longer time periods for selection. These conditions would mirror those found in the field with this species, in which courtship can sometimes involve numerous close-range interactions with a male courting a female for extended periods (P. Hamilton, personal observations). Our study design was limited in that we did not assess the contribution of particular traits to female mate choice while holding other characters constant, as is a standard approach in investigations of female mate choice using discrimination experiments (Andersson 1994). However, the ‘one trait at a time’ discrimination trial paradigm may fail with some taxa if the females of these forms require stimulation by a variety of male characters. In nature, females no doubt make use of multiple aspects of a male’s phenotype when selecting a mate (e.g. Calkins & Burley 2003). In this study, no single trait explained a significant proportion of the variance of mate attraction by itself. This implies that while each of these traits might convey unique information to the female above the contribution of all others, selection is acting simultaneously on many traits combined. Univariate tests clearly do not allow such examinations. Multivariate approaches, in contrast, require no a priori assumptions about the salience of any
HAMILTON & SULLIVAN: MULTIVARIATE MATE CHOICE IN LIZARDS
0.2 1
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Figure 2. Phenotypic correlates of mate attraction in U. ornatus.
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single character, and allow identification of traits that may be assessed in a univariate fashion in subsequent manipulated discrimination tests. Such multivariate approaches have been used successfully in studies of the roles of colour and morphology in male–male dominance in U. ornatus (Carpenter 1995; Zucker & Murray 1996), and we encourage additional applications of these methods in investigations of female choice. Acknowledgments J. Alcock, J. Sabo, J. Macedonia, D. Hews and two anonymous referees each provided insightful comments on the manuscript. M. Moore, K. Hughes, M. Douglass and M. Kwiatkowski provided comments on initial analyses. N. DeBellis and S. Hoss assisted with catching and observing lizards in the Phoenix sun. S. Laage assisted with image digitization. We are grateful to Estrella Mountain Regional Park for granting permission to work and collect in the park. All animals were captured under a Arizona Game and Fish Scientific Collecting Permit. All procedures described herein were carried out under supervision of the Arizona State University Institutional Animal Care and Use Committee. References Andersson, M. 1994. Sexual Selection. Princeton, New Jersey: Princeton University Press. Baird, T. A., Fox, S. E. & McCoy, J. K. 1997. Population differences in the roles of size and coloration in intra- and intersexual selection in the collared lizard, Crotaphytus collaris: influence of habitat and social organization. Behavioral Ecology, 8, 506–517. Calkins, J. D. & Burley, N. T. 2003. Mate choice for multiple ornaments in the California quail, Callipepla californica. Animal Behaviour, 65, 69–81. Candolin, U. 2003. The use of multiple cues in mate choice. Biological Review, 78, 575–595. Carpenter, G. C. 1995. Modeling dominance: the influence of size, coloration, and experience on dominance relations in tree lizards (Urosaurus ornatus). Herpetological Monographs, 9, 88–101. Censky, E. J. 1997. Female mate choice in the non-territorial lizard, Ameiva plei. Behavioral Ecology and Sociobiology, 40, 221–225. Cooper, W. E., Jr & Burns, N. 1987. Social significance of ventrolateral coloration in the fence lizard, Sceloporus undulatus. Animal Behaviour, 35, 526–532. Cooper, W. E., Jr & Vitt, L. J. 1993. Female mate choice of large male broad-headed skinks. Animal Behaviour, 45, 683–693. GretagMacbeth. 1998. Color Checker Color Rendition Chart. New Windsor, New York: GretagMacbeth. Hews, D. K. 1990. Examining hypotheses generated by field measures of sexual selection on male lizards, Uta palmeri. Evolution, 44, 1956–1966. Holland, B. & Rice, W. R. 1998. Perspective: chase-away sexual selection: antagonistic seduction versus resistance. Evolution, 521, 1–7. Hover, E. L. 1985. Differences in aggressive behavior between two throat color morphs in a lizard, Urosaurus ornatus. Copeia, 1985, 933–940. Jennions, M. D. & Petrie, M. 1997. Variation in mate choice and mating preferences: a review of causes and consequences. Cambridge Biological Review, 72, 283–327.
Jenssen, T. A. 1970. Female response to filmed displays of Anolis nebulosus (Sauria, Iguanidae). Animal Behaviour, 18, 640–647. Kodric-Brown, A. & Brown, J. H. 1984. Truth in advertisingdthe kind of traits favored by sexual selection. American Naturalist, 124, 309–323. Kwiatkowski, M. A. & Sullivan, B. K. 2002. Geographic variation in sexual selection variation among populations of an iguanid lizard, Sauromalus obesus (Zater). Evolution, 56, 2039–2051. Lebas, N. R. 2001. Microsatellite determination of male reproductive success in a natural population of the territorial ornate dragon lizard, Ctenophorus ornatus. Molecular Ecology, 10, 193–203. Lebas, N. R. & Marshall, N. J. 2000. The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus. Proceedings of the Royal Society of London, Series B, 267, 445–452. Marchetti, K. 1998. The evolution of multiple male traits in the yellow-browed leafwarbler. Animal Behaviour, 55, 361–376. Møller, A. P. & Pomiankowski, A. 1993. Why have birds got multiple sexual ornaments? Behavioral Ecology and Sociobiology, 32, 167–176. Olsson, M. 1993. Male preference for large females and assortative mating for body size in the sand lizard (Lacerta agilis). Behavioral Ecology and Sociobiology, 32, 337–341. Olsson, M. 1994. Why are sand lizard males (Lacerta agilis) not equally green? Behavioral Ecology and Sociobiology, 35, 169–173. Olsson, M. 2001. No female mate choice in Mallee dragon lizards, Ctenophorus fordi. Evolutionary Ecology, 15, 129–141. Olsson, M. & Madsen, T. 1995. Female choice on male quantitative traits in lizards: why is it so rare? Behavioral Ecology and Sociobiology, 36, 179–184. Partan, S. & Marler, P. 1999. Communication goes multimodal. Science, 283, 1272–1273. Salvador, A. & Veiga, J. P. 2001. Male traits and pairing success in the lizard Psammodromus algirus. Herpetologica, 57, 77–86. Schoener, T. W. 1967. The ecological significance of sexual size dimorphism in the lizard Anolis conspersus. Science, 155, 474–477. ScionCorp. 2000. Scion Image 4.0.2. http://www.scioncorp.com. Shine, R. 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology, 64, 419–461. Sigmund, W. R. 1983. Female preference for Anolis carolinensis males as a function of dewlap color and background coloration. Journal of Herpetology, 17, 137–143. Sinervo, B. & Lively, C. M. 1996. The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240–243. Smith, J. M. & Zucker, N. 1997. Do female tree lizards, Urosaurus ornatus, exhibit mate choice? Journal of Herpetology, 31, 179–186. Thompson, C. W. & Moore, M. C. 1991. Throat colour reliably signals status in male tree lizards, Urosaurus ornatus. Animal Behaviour, 42, 745–753. Tokarz, R. R. 1995. Mate choice in lizards: a review. Herpetological Monographs, 9, 17–40. Tokarz, R. R. 2002. An experimental test of the importance of the dewlap in male mating success in the lizard Anolis sagrei. Herpetologica, 58, 87–94. UTHSCSA. 2002. ImageTool 3.0. http://ddsdx.uthscsa.edu/dig/ itdesc.html. Wiens, J. J. 1999. Phylogenetic evidence for multiple losses of a sexually selected character in phrynosomatid lizards. Proceedings of the Royal Society of London, Series B, 266, 1529–1535. Zucker, N. 1994. Social influence on the use of a modifiable status signal. Animal Behaviour, 48, 1317–1324. Zucker, N. & Murray, L. 1996. Determinants of dominance in the tree lizard Urosaurus ornatus: the relative importance of mass, previous experience and coloration. Ethology, 102, 812–824.
Female mate attraction in ornate tree lizards, Urosaurus ornatus: a multivariate analysis P AU L S. H AM ILTON * & B RIAN K. SULLIVAN†
*Department of Biology, Arizona State University, Tempe yDepartment of Life Sciences, Arizona State University West, Phoenix (Received 19 February 2003; initial acceptance 9 May 2003; final acceptance 12 March 2004; published online 26 November 2004; MS. number: A9561R2)
Recent reviews of mate choice have concluded that this phenomenon is rare or nonexistent in lizards. However, direct tests of lizard mate choice are few and generally limited in scope. We present results of a mate choice experiment with Urosaurus ornatus in which two male lizards differing in morphology, colour and behaviour were given the opportunity to attract a female lizard. Pairwise comparisons of selected and unselected males revealed that variation in individual traits failed to account for much of the variation in mate attraction success. However, a multivariate analysis revealed that mate attraction was related to multiple cues from a male’s phenotype: body mass and head size as well as body and tail coloration all contributed to mate attraction. We argue that the additive and interactive effects of several traits combined may be more important than single traits in mate choice. We suggest that mate choice studies should account for multivariate effects of male traits, and also allow mate attraction to occur over variable spatial and temporal scales, paralleling mate choice under natural conditions. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Although mate attraction and mate choice have been demonstrated in a wide variety of animals, ranging from Drosophila to Homo (reviewed in Andersson 1994), some groups have received little attention. For instance, relatively few studies have been conducted with lizards (e.g. Olsson 1993; Baird et al. 1997; LeBas 2001; LeBas & Marshall 2001), and many of these have focused on one particular trait (e.g. dewlap, Tokarz 2002) or tested only one model of sexual selection (e.g. sensory exploitation, Olsson 2001). Despite the limited scope of most studies, some authors have argued that negative results indicate that female lizards rarely, if ever, choose their mates (Olsson & Madsen 1995; Tokarz 1995). However, in the absence of an examination of several of the potential factors involved in mate choice, and without restriction to a particular model of sexual selection, such a conclusion is premature. Also, without examining many of the phenotypic traits potentially involved in mate attraction, mate choice cannot be excluded in any given species. Recent studies have highlighted the importance of multiple traits in mate choice (e.g. Marchetti 1998; Calkins & Burley 2003; reviewed in Candolin 2003). This
Correspondence: P. S. Hamilton, Department of Biology, Tempe, AZ 85287-1501, U.S.A. (email: [email protected]). B. K. Sullivan is at the Department of Life Sciences, Arizona State University West, PO Box 37100, Phoenix, AZ 85069, U.S.A. 0003–3472/04/$30.00/0
approach represents a departure from classic mate choice studies that focused on single traits with presumed a priori significance in mate attraction (Andersson 1994). Negative findings in such studies have often been interpreted to mean that mate choice is absent in a given taxon. Indeed, recent theoretical work has focused on explanations for secondary sexual traits that appear not to be favoured by females (Holland & Rice 1998). Signal redundancy has also been proposed to explain such patterns (Møller & Pomiankowsi 1993; Partan & Marler 1999). Alternatively, an examination of multiple traits simultaneously may find that each trait in a suite of characters conveys novel information, or that the interactive effects of multiple traits may be more important than their individual contributions (Møller & Pomiankowsi 1993; Jennions & Petrie 1997). Clearly, a ‘one trait at a time’ paradigm in mate choice studies does not allow for examination of such ideas. Furthermore, this paradigm may lead to a premature conclusion that mate choice is completely lacking in a taxon, rather than simply not acting on a single isolated trait. Lizard display behaviour, including species-specific ‘pushup’ displays, is generally assumed to have a role in mate recognition, but few studies have directly tested this assertion (Jenssen 1970; Tokarz 1995). A field study of sexual selection (Hews 1990) demonstrated that head and body size are important in lizard sexual selection, but laboratory experimental studies have not yet found a link
219 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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between these morphological traits and mate attraction or mating success. Phrynosomatid lizards, including U. ornatus, have been the subject of numerous studies on male– male signalling. Several of these studies have implicated dorsal (Zucker 1994) as well as throat (Hover 1985; Thompson & Moore 1991) ornamentation as important indicators of male dominance. However, the role of these ornaments in mate choice remains largely unknown (but see Cooper & Burns 1987, regarding ventral ornaments in Sceloporus undulatus). Extreme phenotypic variation in ornate tree lizards, Urosaurus ornatus (see below), offers an ideal opportunity to examine the multivariate influences of colour, morphology and behaviour on the ability of males to attract potential mates. Herein, we examine the influence of multiple male traits on female mate attraction in U. ornatus.
MATERIALS AND METHODS Beginning in 1999, we monitored ornate tree lizards, Urosaurus ornatus, in the western foothills of Sierra Estrella, Maricopa County, Arizona, U.S.A. (33 210 340 N; 0 0 112 22 25 W), as part of a longitudinal study of sexual selection in a natural population. This area consists of lower Colorado Sonoran Desert dominated by saguaro, palo verde, creosote and bursage; U. ornatus generally occupy boulder outcrops in this region. For each mate choice trial, two males and one female were chosen randomly from recently collected field animals from areas near the primary study site. Prior to trials, animals were housed individually in 38-litre aquaria under full-spectrum lighting and a thermal gradient provided by a heat lamp on one side of each tank. Crickets, Acheta domestica, dusted with vitamin supplements and water sprayed in each tank were provided ad libitum. To avoid pseudoreplication, lizards were used only once in trials. A total of 48 trials were completed in 1999 and 2000. Trial arenas (Fig. 1) consisted of approximately 20-cmhigh aluminium sheeting that formed two 4 ! 4 m outdoor arenas on soil. Three rock piles were placed in each arena to serve as starting positions for each of the three lizards. These rocks were taken from boulder habitats where lizards were collected and represented the colour and thermal microhabitats in which lizards were found. Rock piles of the two males were visually separated from each other by a sheeting barrier. The two males were tethered with clear monofilament around the waist. These 1-m-long tethers were attached to a pole directly over each male. Each male could move freely on his rock pile perch, but could not approach the female or the other male. Trials were completed during peak mating times for U. ornatus in the source population, late April through June, and in peak times of day for activity, immediately after dawn or immediately before dusk. The two males were given at least 20 min to acclimate to the arena before starting a trial. A trial began when the female was placed in the arena. An observer remained relatively motionless outside the arena and recorded male and female behaviours until the female directly approached one male or the other. We used a female’s
4m
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Figure 1. Schematic of mate choice enclosure. Lines represent aluminium flashing and circles represent areas in which each male could freely move.
approach to one male or another as a proxy for mate choice by females (see ‘Results’ for descriptions of female approach behaviours).
Phenotypic Measurements At least 48 h prior to conducting mate choice trials, males were restrained against a neutral grey surface and photographed ventrally and laterally. Film transparencies were digitally scanned and calibrated for hue and spatial scale using a colour standard (GretagMacbeth 1998) and a millimetre ruler, respectively. Hue was calibrated with the ‘Calibrate’ option of Scion Image software (ScionCorp 2000), using a digital layer representing wavelength as optical density. This function produced a calibration regression between the colours of known hue from the standard and the hues in a digital image of the standard. This calibration regression was then applied to lizard photographs to obtain a corrected hue for throat colours. Optical density of the hue layer of lizard photographs was converted to a 1–360-degree Munsell hue score, with ‘1’ representing far blue wavelengths and ‘360’ representing far red. For morphological measurements, spatial scale of photographs was calibrated using the ‘Calibrate Spatial Measurements’ option in ImageTool software (UTHSCSA 2002). These colour and morphology methods are treated in more detail elsewhere (unpublished data). Morphological measurements obtained from standardized images included snout–vent length (SVL), head width (HW, the linear distance between the anterior edges of each tympanum), head length (HL, the linear distance between the tip of the snout and the midpoint between the anterior edges of the two tympanum), and head depth (HD, the vertical distance between the lower edge of the tympanum and the dorsal border of the head). The three head measurements were taken at Cartesian angles to one another, and thus represent mathematically independent
HAMILTON & SULLIVAN: MULTIVARIATE MATE CHOICE IN LIZARDS
measures of head size, without angular dependencies of one measurement on another. The areas of three ventral display patches were measured from standardized ventral photographs: the blue ventral trunk display patches, and two throat patches (see below). Also, the hue of each of the two throat patches was measured as above. Ornate tree lizards from some populations have at least two distinct colour badges on their throats, which have been implicated in social signalling among males (Thompson & Moore 1991). Some individuals have only a single throat colour (usually orange), whereas others also have a distinct central patch of blue or green. However, the U. ornatus at our study site often did not fall easily into either of these categories and sometimes had indistinct central colours. So, rather than typing these lizards into dichotomous colour morphs, we analysed throat colour with two continuous variables: the proportion of surface area of the central throat patch relative to that of the total throat patch, and the difference in hue between the central and outer portions of the throat patch (in colour degrees). The extremes in these continuous variables roughly correspond with the dichotomous types described previously (unpublished data). Males of U. ornatus used in this study also varied in the number of blue scales on the lateral surface of the tail. We counted 50 of the most proximal tail scales on the left side, and recorded the percentage of blue scales. Whether or not the tail had been broken and regrown was also recorded. All male lizards used had intact or completely regrown tails. During trials, we recorded the number of pushup displays performed by the males before a female approached either male. Display rate greatly increased after a female approached, so these postapproach displays were not counted. Males also occasionally performed two variations on the pushup display, the ‘shudder’ (a rapid dorsoventral vibration of the head) and the ‘fullshow’ (a pushup with lateral compression). Shudder displays are used primarily in courtship, but were only performed in two trials before a female approached a male, and thus were not analysed. Fullshow displays are, like pushups, performed in multiple social contexts, and thus were lumped in with pushups to calculate an overall display rate. Last, we recorded the proportion of time a male stayed in front of his perch in view of the focal female.
Statistical Analysis Several traits (head dimensions, belly patch size and mass) were significantly correlated with SVL (results not presented). For these traits, residual values from regressions on SVL were used in pairwise analysis. We analysed phenotypic differences between pairs of lizards (winners and losers in attracting females) with paired t tests when meeting parametric assumptions. Otherwise, we used Wilcoxon matched-pairs signed-ranks tests or a sign test. To address the multivariate relationship among male phenotypic variables and male attraction to females, we used multiple logistic regression. In this analysis, for each variable, we calculated the difference between the value of
the male on the left side of the area and the one on the right. Thus, each pair of lizards had a single variable to enter into the equation. We then performed multiple logistic regression with the trial outcome (win or loss) of the left lizard as the dichotomous dependent variable, with the 12 difference scores as independent variables. Raw values (i.e. not residuals) were used for all traits in this analysis. Although prior work suggested that larger and more colourful males should be preferred by females (reviewed by Kodric-Brown & Brown 1984; Andersson 1994), we used two-tailed tests in assessing female mate choice of male size, behaviour and colour variation.
RESULTS Trials averaged 49 min (range 4–192 min) and lasted until a female ran to a male’s rock pile or lizards became inactive. In 12 of 48 trials, females did not move directly towards either male, but rather ran towards an arena wall away from the males. These trials were excluded from further analysis. In one trial, the female attacked the smaller of the two males presented to her, and this trial also was excluded. In the remaining 35 trials, females ran directly to the perch of a male, usually in a straight line from her starting perch. However, in some trials (N Z 11), females ran to one side of the arena or another (i.e. not directly to a rock pile), and then subsequently moved to the perch of a male. To address the possibility that these females were simply running in a random direction and happened to end up on one side or the other, each of these 11 trials was rerun. In each of these cases, the female ran towards the same side of the arena, suggesting that the movement was not random (binomial test: P Z 0.0005). To further address repeatability, the eight trials run in 2000 were redone with the same animals on different days. In this second set of trials, we used a different arena and switched the relative positions of the males (right or left). In six of these trials, the female moved towards the same male in both trials, despite the new arena and side. In one case she moved towards the other male, and in another, she failed to move towards either male on the second trial. Excluding this last case, the binomial probability of six of seven trials repeating the same outcome is 0.055. Hence, females were generally consistent in their selections, and a bias towards one side of the arena or the other was not apparent. We included only the first selection of these trials in subsequent analysis. Selected males tended to have larger bodies, greater head depth, and more blue scales on their tails (Table 1, Fig. 2). However, when controlling for an experimentwide error rate, none of the univariate comparisons remained significant (Bonferroni, P O 0.05 in all comparisons). Overall, nine of 12 comparisons were in the predicted directions: selected males usually had the larger or more conspicuous trait, or an intact tail. Logistic regression revealed that the outcome of a trial could be predicted well with the combined effects of multiple phenotypic variables (Model Nagelkerke R2 Z 0.691, P Z 0.016; Table 1). The logistic regression model correctly predicted the outcome in 30 of 34 trials (88%).
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Table 1. Male traits evaluated in mate choice trials with female Urosaurus ornatus and the statistical comparisons used to assess selected males in relation to unselected males in paired trials Male trait SVL Mass* HW* HL* HD* Belly patch size* Throat hue contrast Throat size Tail blue Tail break Display rate Time in view
Test
P
P (logistic)
Paired t Paired t Paired t Paired t Paired t Paried t Wilcoxon Wilcoxon Paired t Sign Wilcoxon Wilcoxon
0.053 0.594 0.396 0.463 0.097 0.337 0.304 0.144 0.068 0.454 0.238 0.750
0.133 0.057 0.362 0.742 0.089 0.060 0.918 0.338 0.053 0.226 0.367 0.666
SVL: snout–vent length; HW: head width; HL: head length; HD: head depth. Residuals on body mass were used in pairwise tests for those variables marked with a ‘*’. Raw values (i.e. not residuals) were used for all variables in the logistic regression analysis.
Some of the same variables (e.g. head depth and blue on tail) implicated in univariate analysis were also implicated with this method. In addition, body mass and belly patch size were identified as indicators of male success in the logistic analysis. Interestingly, the trend with body mass was opposite to that expected; females tended to choose thinner males (Fig. 2). However, as in the univariate tests, of the individual variables in the logistic regression were not statistically significant in this second analysis.
DISCUSSION We found that selected males had deeper heads (HD), were thinner (mass), and more brightly coloured (blue on tail, belly patch size) than males that were not selected. However, the contribution of each of these variables independently was negligible, and a pattern was only evident with a multivariate examination of all traits simultaneously. Indeed, when we examined each trait individually, no single trait attained statistical significance. Thus, as in previous univariate studies, an examination of individual traits yielded negative results. However, when considered together in a multivariate analysis, the combination of characters contributed to mate attraction success. Male lizards with large heads and bodies have been repeatedly shown to benefit in male–male contests (e.g. Hews 1990; Baird et al. 1997). A number of studies of lizards also have documented a mate association benefit for large males (e.g. Cooper & Vitt 1993; Salvador & Veiga 2001), and in some of these, a role for female mate choice has been directly supported (Censky 1997). Hews (1990) documented selection acting on male head depth in Uta palmeri, an insular phrynosomatid, but sexual selection in this trait was shown to occur through male–male competition rather than female mating preferences. Our results provide one of the first suggestions of sexual selection acting on both head and body size through female choice. Although body mass was not significant by itself, females
tended to choose thinner males, which is a departure from theoretical expectations and empirical precedents. Head and body size in many Carribean anole lizards have been thought to be shaped by ecological selection (Schoener 1967), and sexual selection has sometimes been considered a less likely explanation for sexual dimorphism in these traits (Shine 1989). By contrast, the current findings suggest that sexual selection may in fact be an important cause for such dimorphism. Numerous studies have addressed the role of lizard colour in sexual selection. Most of these studies have focused on single characters such as throat colour (Thompson & Moore 1991; Sinervo & Lively 1996; Smith & Zucker 1997), dewlap colour (Sigmund 1983), body colour (Olsson 1994; Zucker 1994; Baird et al. 1997), or tail colour (Kwiatkowski & Sullivan 2002). Although some colour traits, particularly throat or dewlap colours (Thompson & Moore 1991; Sinervo & Lively 1996) have been implicated in male–male competition, relatively few investigators have directly addressed the role of these colours in mate choice (but see Smith & Zucker 1997). In addition to morphology, we found that male coloration played a role in attraction of females. Of the colour variables measured, blue scales on the tail and the size of belly patches were most conspicuous to human observers, and these were also traits implicated in mate attraction. This is one of the first studies documenting a female preference for more conspicuously coloured males (see also Kwiatkowski & Sullivan 2002). This is somewhat surprising given the number and diversity of colour badges in many lizards and hypotheses concerning their evolution (e.g. Wiens 1999). Unlike belly and tail colours, throat colours were not found to influence mate attraction. However, these subtle throat colours were probably not discernable to females from their starting positions in our arena (ca. 2.5 m). Future studies may address these potentially important colours by the use of close-range discrimination trials and longer time periods for selection. These conditions would mirror those found in the field with this species, in which courtship can sometimes involve numerous close-range interactions with a male courting a female for extended periods (P. Hamilton, personal observations). Our study design was limited in that we did not assess the contribution of particular traits to female mate choice while holding other characters constant, as is a standard approach in investigations of female mate choice using discrimination experiments (Andersson 1994). However, the ‘one trait at a time’ discrimination trial paradigm may fail with some taxa if the females of these forms require stimulation by a variety of male characters. In nature, females no doubt make use of multiple aspects of a male’s phenotype when selecting a mate (e.g. Calkins & Burley 2003). In this study, no single trait explained a significant proportion of the variance of mate attraction by itself. This implies that while each of these traits might convey unique information to the female above the contribution of all others, selection is acting simultaneously on many traits combined. Univariate tests clearly do not allow such examinations. Multivariate approaches, in contrast, require no a priori assumptions about the salience of any
HAMILTON & SULLIVAN: MULTIVARIATE MATE CHOICE IN LIZARDS
0.2 1
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Figure 2. Phenotypic correlates of mate attraction in U. ornatus.
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single character, and allow identification of traits that may be assessed in a univariate fashion in subsequent manipulated discrimination tests. Such multivariate approaches have been used successfully in studies of the roles of colour and morphology in male–male dominance in U. ornatus (Carpenter 1995; Zucker & Murray 1996), and we encourage additional applications of these methods in investigations of female choice. Acknowledgments J. Alcock, J. Sabo, J. Macedonia, D. Hews and two anonymous referees each provided insightful comments on the manuscript. M. Moore, K. Hughes, M. Douglass and M. Kwiatkowski provided comments on initial analyses. N. DeBellis and S. Hoss assisted with catching and observing lizards in the Phoenix sun. S. Laage assisted with image digitization. We are grateful to Estrella Mountain Regional Park for granting permission to work and collect in the park. All animals were captured under a Arizona Game and Fish Scientific Collecting Permit. All procedures described herein were carried out under supervision of the Arizona State University Institutional Animal Care and Use Committee. References Andersson, M. 1994. Sexual Selection. Princeton, New Jersey: Princeton University Press. Baird, T. A., Fox, S. E. & McCoy, J. K. 1997. Population differences in the roles of size and coloration in intra- and intersexual selection in the collared lizard, Crotaphytus collaris: influence of habitat and social organization. Behavioral Ecology, 8, 506–517. Calkins, J. D. & Burley, N. T. 2003. Mate choice for multiple ornaments in the California quail, Callipepla californica. Animal Behaviour, 65, 69–81. Candolin, U. 2003. The use of multiple cues in mate choice. Biological Review, 78, 575–595. Carpenter, G. C. 1995. Modeling dominance: the influence of size, coloration, and experience on dominance relations in tree lizards (Urosaurus ornatus). Herpetological Monographs, 9, 88–101. Censky, E. J. 1997. Female mate choice in the non-territorial lizard, Ameiva plei. Behavioral Ecology and Sociobiology, 40, 221–225. Cooper, W. E., Jr & Burns, N. 1987. Social significance of ventrolateral coloration in the fence lizard, Sceloporus undulatus. Animal Behaviour, 35, 526–532. Cooper, W. E., Jr & Vitt, L. J. 1993. Female mate choice of large male broad-headed skinks. Animal Behaviour, 45, 683–693. GretagMacbeth. 1998. Color Checker Color Rendition Chart. New Windsor, New York: GretagMacbeth. Hews, D. K. 1990. Examining hypotheses generated by field measures of sexual selection on male lizards, Uta palmeri. Evolution, 44, 1956–1966. Holland, B. & Rice, W. R. 1998. Perspective: chase-away sexual selection: antagonistic seduction versus resistance. Evolution, 521, 1–7. Hover, E. L. 1985. Differences in aggressive behavior between two throat color morphs in a lizard, Urosaurus ornatus. Copeia, 1985, 933–940. Jennions, M. D. & Petrie, M. 1997. Variation in mate choice and mating preferences: a review of causes and consequences. Cambridge Biological Review, 72, 283–327.
Jenssen, T. A. 1970. Female response to filmed displays of Anolis nebulosus (Sauria, Iguanidae). Animal Behaviour, 18, 640–647. Kodric-Brown, A. & Brown, J. H. 1984. Truth in advertisingdthe kind of traits favored by sexual selection. American Naturalist, 124, 309–323. Kwiatkowski, M. A. & Sullivan, B. K. 2002. Geographic variation in sexual selection variation among populations of an iguanid lizard, Sauromalus obesus (Zater). Evolution, 56, 2039–2051. Lebas, N. R. 2001. Microsatellite determination of male reproductive success in a natural population of the territorial ornate dragon lizard, Ctenophorus ornatus. Molecular Ecology, 10, 193–203. Lebas, N. R. & Marshall, N. J. 2000. The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus. Proceedings of the Royal Society of London, Series B, 267, 445–452. Marchetti, K. 1998. The evolution of multiple male traits in the yellow-browed leafwarbler. Animal Behaviour, 55, 361–376. Møller, A. P. & Pomiankowski, A. 1993. Why have birds got multiple sexual ornaments? Behavioral Ecology and Sociobiology, 32, 167–176. Olsson, M. 1993. Male preference for large females and assortative mating for body size in the sand lizard (Lacerta agilis). Behavioral Ecology and Sociobiology, 32, 337–341. Olsson, M. 1994. Why are sand lizard males (Lacerta agilis) not equally green? Behavioral Ecology and Sociobiology, 35, 169–173. Olsson, M. 2001. No female mate choice in Mallee dragon lizards, Ctenophorus fordi. Evolutionary Ecology, 15, 129–141. Olsson, M. & Madsen, T. 1995. Female choice on male quantitative traits in lizards: why is it so rare? Behavioral Ecology and Sociobiology, 36, 179–184. Partan, S. & Marler, P. 1999. Communication goes multimodal. Science, 283, 1272–1273. Salvador, A. & Veiga, J. P. 2001. Male traits and pairing success in the lizard Psammodromus algirus. Herpetologica, 57, 77–86. Schoener, T. W. 1967. The ecological significance of sexual size dimorphism in the lizard Anolis conspersus. Science, 155, 474–477. ScionCorp. 2000. Scion Image 4.0.2. http://www.scioncorp.com. Shine, R. 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology, 64, 419–461. Sigmund, W. R. 1983. Female preference for Anolis carolinensis males as a function of dewlap color and background coloration. Journal of Herpetology, 17, 137–143. Sinervo, B. & Lively, C. M. 1996. The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240–243. Smith, J. M. & Zucker, N. 1997. Do female tree lizards, Urosaurus ornatus, exhibit mate choice? Journal of Herpetology, 31, 179–186. Thompson, C. W. & Moore, M. C. 1991. Throat colour reliably signals status in male tree lizards, Urosaurus ornatus. Animal Behaviour, 42, 745–753. Tokarz, R. R. 1995. Mate choice in lizards: a review. Herpetological Monographs, 9, 17–40. Tokarz, R. R. 2002. An experimental test of the importance of the dewlap in male mating success in the lizard Anolis sagrei. Herpetologica, 58, 87–94. UTHSCSA. 2002. ImageTool 3.0. http://ddsdx.uthscsa.edu/dig/ itdesc.html. Wiens, J. J. 1999. Phylogenetic evidence for multiple losses of a sexually selected character in phrynosomatid lizards. Proceedings of the Royal Society of London, Series B, 266, 1529–1535. Zucker, N. 1994. Social influence on the use of a modifiable status signal. Animal Behaviour, 48, 1317–1324. Zucker, N. & Murray, L. 1996. Determinants of dominance in the tree lizard Urosaurus ornatus: the relative importance of mass, previous experience and coloration. Ethology, 102, 812–824.