The Relationship Between Morphology, Escape Behaviour and Microhabitat Occupation in the Lizard Clade Liolaemus (Iguanidae: Tropidurinae*: Liolaemini)
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doi: 10.1046/j.1420-9101.2003.00659.x The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae*: Liolaemini) J. A. SCHULTE II,* J. B. LOSOS,* F. B. CRUZ &H.NU´ N˜ EZà *Department of Biology, Washington University, St Louis, MO, USA CONICET-CRUB-Universidad Nacional del Comahue. Quintral 1250, San Carlos de Bariloche, Rio Negro, Argentina àMuseo Nacional de Historia Natural, Casilla, Santiago, Chile Keywords: Abstract Argentina; Phenotypic differences among species are known to have functional conse- behaviour; quences that in turn allow species to use different habitats. However, the role Chile; of behaviour in this ecomorphological paradigm is not well defined. We ecomorphology; investigated the relationship between morphology, ecology and escape Iguanidae; behaviour among 25 species of the lizard clade Liolaemus in a phylogenetic independent contrasts; framework. We demonstrate that the relationship between morphology and Liolaemus; characteristics of habitat structure shows little or no association, consistent lizard; with a previous study on this group. However, a significant relationship was Squamata. found between morphology and escape behaviour with the distance a lizard moved from a potential predator correlated with body width, axilla-groin length, and pelvis width. A significant relationship between escape behaviour and habitat structure occupation was found; lizards that occupied tree trunks and open ground ran longer distances from predators and were found greater distances from shelter. Behavioural strategies used by these lizards in open habitats appear to have made unnecessary the evolution of limb morphology that has occurred in other lizards from other clades that are found in open settings. Understanding differences in patterns of ecomorphological relation- ships among clades is an important component for studying adaptive diversification. differences in functional capabilities, which, in turn, are Introduction adaptive for the differing demands of different environ- In recent years, the field of ecological morphology has ments (Greene, 1986; Coddington, 1988; Emerson & blossomed. Integrating state-of-the-art methods in func- Arnold, 1989; Arnold, 1994; Garland & Losos, 1994). tional morphology, behaviour, and ecology, synthesized The role of behaviour in this paradigm is not and analysed in a phylogenetic context, studies of straightforward (Garland & Losos, 1994; Huey et al., ecological morphology have provided important insights 2003). On one hand, behavioural differences may pro- into the process of adaptation and evolutionary diversi- mote evolutionary change; as populations or species find fication (Wainwright & Reilly, 1994; Luczkovich et al., themselves in different habitats, they may exhibit differ- 1995; Aerts et al., 2002). The classic paradigm in ecolog- ent behaviours which in turn lead to selection for ical morphology of the phenotype fi perform- phenotypes that maximize the effectiveness of these ance fi environment relationship was formally behaviours (Mayr, 1963). As a result, comparative articulated by Arnold (1983) and states that differences studies would find that interspecific differences in beha- in phenotype (e.g. morphology, physiology) lead to viour would be concordant with differences in morphol- ogy, performance ability, and habitat use. In Caribbean Correspondence: James A. Schulte II, Division of Amphibians and Reptiles, Anolis lizards, for example, species that use broad surfaces PO Box 37012, MRC 162, National Museum of Natural History, Washington, DC 20013-7012, USA. have long legs and can run rapidly, whereas species that Tel.: 202 357 4594; fax: 202 786 2979; use narrow surfaces have short legs and poor sprinting e-mail: [email protected] capabilities (Losos, 1990a). As one might predict, 408 J. EVOL. BIOL. 17 (2004) 408–420 ª 2004 BLACKWELL PUBLISHING LTD Ecomorphological relationship in Liolaemus 409 behavioural differences parallel morphological, func- performance capability as the mechanistic link between tional, and ecological ones: the long-legged species morphology and ecology (Table 1). However, few studies frequently make use of their great running capabilities, have examined the role of behaviour in lizard ecomor- whereas short-legged species depend more on stealth to phological relationships. capture prey and escape predators (Losos, 1990b; Irschick The iguanid lizard clade Liolaemus is an ideal candidate & Losos, 1998). for a comparative study of ecological morphology both Conversely, behavioural adjustments can prevent for its exceptional diversity and because it is one of the ecomorphological differentiation; a phenomenon few clades in which previous research did not find a recently termed the ‘Bogert effect’ (Huey et al., 2003). relationship between ecology and morphology (Jaksic If species are able to reduce the effect of environmental et al., 1980), despite the fact that a relationship may exist differences solely by altering their behaviour, then between habitat use and behaviour (Jaksic & Nu´n˜ ez, phenotypic differentiation may not result from differ- 1979). Jaksic et al. (1980) examined the habitat use and ences in habitat use. For example, lizards of many species limb and tail morphology of 12 species of Chilean alter their escape behaviour when their running ability is Liolaemus finding almost no relationship. Species found compromised by internal conditions such as, gravidity, a on rocks, trees, or the ground showed few significant full stomach, or low body temperature (Rand, 1964; differences in forelimb, hind limb, and tail morphology Ballinger, 1973; Bauwens & Thoen, 1981; Hertz et al., (Jaksic et al., 1980; see also Sage, 1973). However, in a 1982; Dial & Fitzpatrick, 1984; Formanowicz et al., 1990; comparison of the escape behaviour of two species, Jaksic Schieffelin & de Queiroz, 1991; Nu´n˜ ez, 1996). Lizards &Nu´n˜ ez (1979) found that the species that escaped into also may change their behaviour because of differences the grass, L. lemniscatus, had significantly shorter limbs in external conditions, such as Anolis that adjust their than the species which escaped into rocky areas, L. fuscus. basking behaviour with changes in average ambient For several reasons, the relationship between ecology, temperature (Huey et al., 2003). Thus, to the extent that morphology and behaviour in Liolaemus bears further morphologically similar lizards can use alternative scrutiny. First, the species studied by Jaksic et al. (1980) behaviours in different contexts, one would not neces- did not sample either the geographic or phylogenetic sarily expect a relationship to exist between morphology range of this clade. In particular, Jaksic et al.’s (1980) and environment. study was restricted to the region of Mediterranean scrub Squamate reptiles have been a model group for in central Chile (between 30 and 33°S) and all 12 were examination of ecomorphological relationships. Clades members of a single clade. However, the Chilean radi- of a wide variety of lizards and a few snakes have been ation of Liolaemus (subgenus Liolaemus) contains approxi- studied. Focusing primarily on the demands placed by mately 60 species that use a wide variety of habitats. the structural environment on locomotion and associated Moreover, an independent radiation of Liolaemus pri- morphology, studies have been conducted in taxa from marily distributed in Argentina (subgenus Eulaemus) around the world living in a variety of habitats (Table 1). contains almost twice as many species. Thus, one possible With very few exceptions, relationships between mor- explanation for Jaksic et al.’s (1980) finding is that the phology and habitat use are apparent; many studies have diversity of the clade was not sufficiently sampled. In also involved functional studies illustrating the role of addition, Jaksic et al.’s study was conducted before an Table 1 Relationship between morphology and ecology in squamate reptiles. Taxon Morphology Ecology Reference Anolis – Island Long limbs, heavy-bodied, Perch type, perch height, Losos, 1990a Tail length perch diameter (neg.), closest perch distance Anolis – Mainland Toepad size Perch height Irschick et al., 1997 Tail length perch diameter Niveoscincus Long limbs, heavy-bodied Microhabitat openness Melville & Swain, 2000 Tropidurines Short tibia Closed habitat Kohlsdorf et al., 2001 Short tail and hind limbs Branch-dwelling Long feet Sand-dwelling Ctenotus Long limbs Microhabitat openness Pianka, 1969 Phrynosomatinae Long limbs, broad pelvis Terrestrial habitat Miles, 1994; Herrel et al., 2002 Slender-bodied, long tail and toes Arboreal habitat Bothrops Long tail, slender body Arboreal habitat Martins et al., 2001 Liolaemus Short limbs Escape into grasses Jaksic & Nu´ n˜ ez, 1979 Chameleons Long tail, long limbs, Small head Arboreal habitat Bickel & Losos, 2002 Squamates Slender head and body, long feet, short front legs Microhabitat openness Scheibe, 1987 J. EVOL. BIOL. 17 (2004) 408–420 ª 2004 BLACKWELL PUBLISHING LTD 410 J. A. SCHULTE II ET AL. explicit phylogenetic hypothesis for Liolaemus was avail- considerable ecological, physiological, and morphological able and before the importance of conducting compar- variation. The clade comprises more than 160 species and ative studies in a phylogenetic context was appreciated. has one of the largest latitudinal, elevational, and Consequently, a study of ecomorphological relationships climatic distributions among lizards worldwide, with