Evolution and Ecology of Lizard Body Sizes PAPER Shai Meiri
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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2008) 17, 724–734 Blackwell Publishing Ltd RESEARCH Evolution and ecology of lizard body sizes PAPER Shai Meiri NERC Centre for Population Biology, Imperial ABSTRACT College London, Silwood Park, Ascot, Berkshire Aim Body size is instrumental in influencing animal physiology, morphology, SL5 7PY, UK ecology and evolution, as well as extinction risk. I examine several hypotheses regarding the influence of body size on lizard evolution and extinction risk, assessing whether body size influences, or is influenced by, species richness, herbivory, island dwelling and extinction risk. Location World-wide. Methods I used literature data and measurements of museum and live specimens to estimate lizard body size distributions. Results I obtained body size data for 99% of the world’s lizard species. The body size–frequency distribution is highly modal and right skewed and similar distributions characterize most lizard families and lizard assemblages across biogeographical realms. There is a strong negative correlation between mean body size within families and species richness. Herbivorous lizards are larger than omnivorous and carnivorous ones, and aquatic lizards are larger than non-aquatic species. Diurnal activity is associated with small body size. Insular lizards tend towards both extremes of the size spectrum. Extinction risk increases with body size of species for which risk has been assessed. Main conclusions Small size seems to promote fast diversification of disparate body plans. The absence of mammalian predators allows insular lizards to attain larger body sizes by means of release from predation and allows them to evolve into the top predator niche. Island living also promotes a high frequency of herbivory, which is also associated with large size. Aquatic and nocturnal lizards probably evolve large size because of thermal constraints. The association between large size and high extinction risk, however, probably reflects a bias in the species in which risk *Correspondence: Shai Meiri, NERC Centre has been studied. for Population Biology, Imperial College Keywords London, Silwood Park, Ascot, Berkshire SL5 7PY, UK. Body size, description dates, diversification rates, extinction risk, insularity, lizard E-mail: [email protected] diets, snout–vent length, size–frequency distributions, species richness. logarithmic scale (Hutchinson & MacArthur, 1959; Gardezi & da INTRODUCTION Silva, 1999; Olden et al., 2007. cf. Roy et al., 2000; Boback & Guyer, Body size is known to greatly influence many aspects of the 2003). Thus most species are smaller than the midpoint and morphology, physiology and ecology of organisms. Furthermore, mean of the size range. Most research on global-scale patterns size often is linked to the likelihood of speciation and extinction of size distributions has focused on vertebrates and sampling is and to the rate of evolution, as well as to current levels of anthro- relatively complete for birds (65% of species; Maurer, 1998), pogenically induced extinction risk (Stanley, 1973; Cardillo et al., mammals (73% of extant and historically extinct species; Smith 2005; Olden et al., 2007). et al., 2003) and fishes (81%; Olden et al., 2007). However, At large geographical and taxonomic scales, body size–frequency although lizards have featured prominently as model organisms distributions are typically unimodal and right skewed on a in studies of the evolution of body size (e.g. Schoener, 1969; Case, DOI: 10.1111/j.1466-8238.2008.00414.x © 2008 The Author 724 Journal compilation © 2008 Blackwell Publishing Ltd www.blackwellpublishing.com/geb Lizard body size 1978, Espinoza et al., 2004; Meiri, 2007) there have been no has been challenged by Espinoza et al. (2004), studying the evo- efforts to study patterns of size evolution for the whole group lution of herbivory in small-sized lizards of the genus Liolaemus. (but see Avery, 1996, and Greer, 2001 for skinks). I therefore test whether there are associations between lizard size Here I examine the shape of the size–frequency distributions and activity times, use of space, mode of reproduction and dietary of lizards at the global and continental scales, both for the group preferences. as a whole and at the family level, where most of the variation of lizard body size lies (Dunham et al., 1988 and see below). I use Body size and insularity these distributions to test the following hypotheses. Island living is thought to enable lizards to evolve large sizes in the absence of mammalian predators (Szarski, 1962; Pregill, 1986; Body size and species richness Greer, 2001). However, cases of insular dwarfism are also well Because in many groups most species are small (Hutchinson & known (Hedges & Thomas, 2001). I test whether insular lizards MacArthur, 1959; Stanley, 1973), and small animals have high rates tend to occupy more extreme sizes than mainland lizards (as was of molecular evolution (Fontanillas et al., 2007), it is often thought found intraspecifically; Meiri, 2007), or whether insular lizards that small size promotes high speciation rates (e.g. Maurer et al., tend to be show less extreme sizes than mainland ones, as predicted 1992). However, Orme et al. (2002) have shown that richness is by theories of optimal body size (Marquet & Taper, 1998; Lomolino usually not associated with body size when clade ages and phylo- et al., 2005, cf. Meiri et al., 2005). These theories invoke the island genetic affinities are modelled. I therefore test for the association rule to suggest that small taxa evolve larger size and large ones between body size, species richness and diversification rates. evolve smaller sizes on islands, a process that will result in insular size distribution tending towards medium body sizes (Price & Phillimore, 2007). I further test whether extreme sizes are more Ecological correlates of body size likely to have evolved on islands lacking mammalian carnivores. Small lizards can gain heat more quickly, but will also tend to lose heat quicker than larger ones. Therefore it is reasonable to expect Body size and extinction risk body size to interact with factors related to thermal regimes such as daily activity patterns. Smaller size may facilitate faster heating Large size has often been associated with anthropogenically and cooling rates in diurnal lizards (Huey & Slatkin, 1976), induced extinction risk (Cardillo et al., 2005; Olden et al., 2007). which are likely to be thermoregulators. Nocturnal lizards may Many lizard species that went extinct in recent times were among be more likely to be thermoconformers (Huey & Slatkin, 1976), the largest in their clades (Case et al., 1998). I therefore test and thus less affected by body-size related cooling and heating whether current levels of threat are associated with lizard body rates. Thus I predict that diurnal species will be smaller to facilitate size. Because risk status is published for only a small number of faster heating. Likewise aquatic species may be more likely to be lizard species, this analysis may be biased if small species are less affected by fast cooling. I therefore hypothesize they will tend to likely to have been assessed or described (e.g. Reed & Boback, be large, to reduce the rates of heat loss. Fossorial habits are 2002). However, if there is no such bias, or if most newly thought to be associated with large size (Dunham et al., 1988), described species result from well-known species being split, perhaps because fossorial lizards often have reduced legs, and then no relationship between size, description date and threat serpentiform movement is easier at large sizes (Avery, 1996; will be found. Greer, 2001). I therefore examine whether the use of space influences lizard size. METHODS Some authors report that viviparous lizards are larger than oviparous ones (e.g. Shine, 1985; Dunham et al., 1988). Greer Data (2001) hypothesized that viviparity is difficult to fit into the short life cycle of very small species, and that over the long development I used data obtained from published literature on the body size times needed by large species embryos may be safer within the of lizards (Appendix S1 in Supplementary Material), and mother’s body than inside a nest. However, his finding that small supplemented it by measurements of live lizards (mostly at the size may be constrained by minimum egg size can suggest that Meier Segal’s Garden for Zoological Research, Tel-Aviv University), oviparous species are constrained to larger sizes (see also Kratochvil museum specimens and personal communication with museum & Frynta, 2006). curators. Taxonomy follows Uetz (2006). While most lizards are carnivorous, Cooper & Vitt (2002) Snakes and amphisbaenians probably evolved from lizards estimated that some 12% of lizard species include a significant (e.g. Townsend et al., 2004; Kumazawa, 2007; but see Zhou et al., amount of plant material (> 10%) in their diets. Plant consumption 2006, who found snakes and lizards are sister taxa). However, in lizards has frequently been associated with large body size these taxa are highly derived (e.g. in respect to life history and (Sokol, 1967; Van Damme, 1999), and it is often assumed that skull kinetism; see Dunham et al., 1988, Zug et al., 2001, and large size is required for lizards to efficiently process plant Pough et al., 2003), and are both, on average, much larger than material, or that herbivory allows lizards to grow large, or both lizards (Avery, 1996). Using the Squamata as a whole, while (Pough, 1973; Cooper & Vitt, 2002; Herrel et al., 2004). This view making the group examined monophyletic, may therefore © 2008 The Author Global Ecology and Biogeography, 17, 724–734, Journal compilation © 2008 Blackwell Publishing Ltd 725 S. Meiri obscure rather than clarify the forces affecting size evolution (see I examined the relationship between SVL and species richness below). The omission of highly morphologically and ecologically within both families and genera. To account for phylogenetic derived taxa is commonplace in macroecology. For example, structure (Orme et al., 2002) I repeated the analysis using the marine mammals and bats are often omitted from studies of family-level phylogeny of Townsend et al.