Research examining the mechanistic basis of species distributions is accelerating (Angilletta, 2009; Kingsolver, 2009). Mechanistic range models (which describe physiological, energetic and demographic constraints on species ranges) can be informative in inferring how the environment sets range limits (Kearney & Porter, 2009; Buckley et al., 2010). Biophysical models compute the energy budget of an organism to estimate metrics such as activity time or discretionary energy and can thus be used to assess how environmental conditions differentially influence ectotherms and endotherms. While low temperatures sharply reduce the activity times and thus the distributions of vertebrate ectotherms (Kearney & Porter, 2009; Buckley et al., 2010), they increase the energetic expenditures of vertebrate endotherms (Porter et al., 2002). In a classic demonstration of energetic constraints on distributions, Root (1988) found that the northern range limits of numerous bird species corresponded to an isotherm where the metabolic rate required was c. 2.5 times the basal metabolic rate (Repasky, 1991; but see Canterbury, 2002). For ectotherms, comparing estimates of potential activity time from biophysical models with observed distributions suggests that the thermal dependence of activity is a strong constraint on distributions (Kearney & Porter, 2009; Buckley et al., 2010).
Mountains, with their drastic climatic changes over small distances, also highlight the implications of ectotherm versus endotherm physiology for distributions. Janzen (1967) proposed that the more constant environmental conditions in the tropics would lead to the evolution of greater thermal specialization of tropical organisms. Mountain passes would thus be physiologically ‘higher’ in the tropics (Janzen, 1967; Ghalambor et al., 2004). This thermal specialization is expected to be more pronounced for ectotherms due to the thermal dependence of their activity. McCain (2009) used data from elevation gradients to test Janzen's key prediction: that the elevational range sizes of organisms on mountains increase with increasing latitude. Although elevational range size increased with increasing latitudes for all ectothermic taxa examined, the only endothermic group to show a strong increase in range size was bats (potentially due to thermoregulatory tradeoffs to enable flight). Overall, there is strong evidence that ectotherm distributions tend to be strongly constrained by activity time. For endotherm distributions in cold environments, metabolic costs may play an important role (Figs 3 & 4).
As ectotherms have low energy requirements (Bennett & Nagy, 1977; Pough, 1980), we expect that coarse estimates of overall energy availability (e.g. NPP) may have a limited influence on ectotherm abundance relative to that of temperature. Specifically, we expect that the total amount of energy utilized by ectotherms will be more strongly influenced by thermal constraints on resource acquisition and assimilation than by resource availability (Diaz, 1997). However, where the environment is sufficiently warm for activity, thermoregulation toward preferred temperatures reduces the influence of environmental temperatures on metabolic rates and performance (Huey et al., 2003). The cost of behavioural thermoregulation can be substantial, but these costs are scarcely quantified despite a long-standing cost–benefit model of thermoregulation (Huey & Slatkin, 1976; see also Angilletta, 2009). In contrast, energy availability is likely to have a greater influence on endotherms, which are able to maintain optimal body temperatures if sufficient resources exist to meet their high metabolic demands in cold environments (Wieser, 1985).
To the extent that abundance mirrors patterns in energy availability, the pattern should be stronger at the community level, summing over all of the species that collectively face that constraint, than at the population level. Nevertheless, population-level patterns have been more thoroughly examined due to the types of data most commonly available. Energetic constraints on both endotherm and ectotherm abundance are evidenced by the decrease in population density with increasing body mass, since larger organisms have greater energetic needs (reviewed by Blackburn & Gaston, 1999). Populations have been termed energy equivalent because density decreases at approximately the same rate as metabolic rates increase, resulting in equal energy use among populations. Energetic equivalence has been documented for groups including mammals (Damuth, 1987), birds (Meehan et al., 2004) and lizards (Buckley et al., 2008). Energetic use in ectotherms is expected to increase with environmental temperature in the absence of major behavioural thermoregulation, while energetic use for endotherms is expected to be independent of temperature within their thermoneutral zone. Allen et al. (2002) found that mass-corrected population densities were inversely related to temperature for ectotherms but not endotherms as predicted. However, using a larger dataset of lizard population densities, Buckley et al. (2008) showed that population energetic equivalence did not extend to temperature. Meehan et al. (2004) demonstrated that total bird community abundance decreases in low-temperature environments where the birds must expend more energy to raise body temperatures into their thermoneutral zone. The influence of temperature on abundance may be buffered in ectotherms by thermoregulation but is acute in endotherms due to their energetic costs for thermoregulation.
In a comparison of density–body size relationships across taxa, Currie & Fritz (1993) found that the relationships for vertebrate ectotherms and endotherms had similar slopes but that ectotherms were nearly three orders of magnitude more abundant than endotherms. They observed little influence of productivity on population densities for either group. Community bird abundance has been found to increase with increasing energy availability in several studies (Hurlbert, 2004; Meehan et al., 2004). Buckley et al. (2008) observed a relatively weak increase in lizard population density with increasing productivity. Obtaining relevant measures of energy availability over geographic scales is notoriously difficult (reviewed by Evans et al., 2005), and may contribute to the heterogeneity of results. Yet, overall, observations support the prediction that the abundance of endotherms is jointly limited by temperature and energy availability whereas thermal constraints tend to dominate for ectotherms.
Diversity: species richness and turnover
Many hypotheses have been put forward to explain geographic patterns of species richness (Rohde, 1992; reviewed in Mittelbach et al., 2007), and although they invoke a variety of mechanisms, all mechanisms ultimately must explain differential rates of origination, extinction or immigration over geographical gradients. Some of these hypotheses, particularly those based on temperature averages or variability, are expected to operate differently on endothermic versus ectothermic groups. As mentioned above, Janzen (1967) thought that climatic variability might explain latitudinal variation in thermal niche breadths, and others (Stevens, 1989) have subsequently argued that such variation could ultimately explain latitudinal richness gradients. In addition, some researchers have proposed that rates of molecular evolution, microevolution and even speciation increase with increasing environmental temperature in ectothermic groups (Rohde, 1992) and could drive latitudinal gradients. This may be due to the greater levels of mutagenesis ectotherms are exposed to in warmer conditions, but ecological and co-evolutionary processes may play an additional role (Gillman et al., 2009). Wiens (2007) identified an increase in diversification rates with decreasing latitude in some amphibians. One analysis suggests faster speciation rates at high latitudes in mammals and birds but no latitudinal trend in diversification rates (Weir & Schluter, 2007). Separate evidence points to increased rates of mammalian microevolution in warmer climates (Gillman et al., 2009).
A third richness hypothesis that might lead to stronger latitudinal gradients for ectotherms than endotherms is phylogenetic niche conservatism (Wiens et al., 2010). For ectotherms in particular, molecular and biochemical constraints on the evolution of thermal performance curves coupled with the geographic origin of clades may influence patterns of richness and species turnover. For example, the latitudinal richness gradient for several major frog clades has been attributed to their tropical origin and conservatism of physiological constraints (Wiens et al., 2009). Endotherms may be better able to escape thermal limits on distributions if sufficient energetic resources exist for thermoregulation.
All four classes of terrestrial vertebrates show broadly similar global patterns of species richness (Grenyer et al., 2006; Lamoreux et al., 2006), with values greatest in tropical areas and decreasing toward the poles. In a large meta-analysis of pre-existing studies, Hillebrand (2004) found no difference in the slope of the latitudinal gradient between endotherms and ectotherms. More detailed examinations of these richness patterns do identify important differences among these vertebrate groups, however. Reptile and amphibian richness appears to be more strongly related to temperature and temperature-related variables (e.g. potential evapotranspiration) compared with mammal and bird richness (Pianka, 1966; Schall & Pianka, 1978; Currie 1991; Fig. 5). Grenyer et al. (2006) found greater congruence in bird and mammal global richness patterns than between amphibians and either endothermic group. Belmaker & Jetz (2011) confirmed substantial differences between amphibians and birds or mammals in the strengths and slopes of environment–richness associations. We conclude that despite fairly high congruence at the global scale, the richness of vertebrate ectotherm communities appears to be more strongly related to temperature than endotherm richness.
Figure 5. A comparison of broad-scale ecological patterns for lizards (left) and birds (right). We depict (a) spatial patterns of species richness and (b) correlate species richness to temperature and summer NDVI (normalized difference vegetation index). In (c), we present the relationship between the number of individuals and the number of species and rarefaction curves (warmer red colours indicate higher temperatures and darker green colours depict higher NDVI). All bird data are from analyses of the North American Breeding Bird Survey by Hurlbert (2004). The lizard data are from species range maps (a, and circles in b) and from the National Park Service Inventory and Monitoring initiative (red stars in b and all data in c) (Buckley & Jetz, 2010). See Appendix S1 for additional methods.
Download figure to PowerPoint
One hypothesized mechanism to account for the link between energy availability and species richness is species–energy theory, which contends that energy availability constrains population size and that more species can persist in a community with more individuals as larger population sizes lead to reduced extinction risk (Wright, 1983). Datasets that span broad spatial gradients and that include information on community-level abundance are uncommon, making tests of these relationships rare over large scales. Buckley & Jetz (2010) found that neither lizard abundance nor species richness vary predictably with a coarse estimate of resource availability (NPP) (Fig. 5). In birds, total abundance increases with NPP or surrogates thereof, and species richness tends to increase with abundance (Fig. 5; Hurlbert, 2004; Pautasso & Gaston, 2005). However, as with lizards, bird communities with more species tend to have abundances distributed more evenly, as evidenced by the divergent rarefaction curves in Fig. 5. Thus, even in birds, a purely individuals-based explanation of species richness remains inadequate (Currie et al., 2004; Hurlbert, 2004; Hurlbert & Jetz, 2010).
Of course, important biological differences exist among birds, mammals, reptiles and amphibians besides thermoregulatory behaviour, and consequently it is difficult to attribute differences in richness patterns to any particular cause with certainty. For example, amphibians clearly differ from the other groups in their water requirements, and are consequently most diverse in places that are wet as well as warm (Buckley & Jetz, 2007). In contrast, some of the most species-rich regions for reptiles occur in areas that are warm and dry (Schall & Pianka, 1978; Currie, 1991). Indeed, reptiles appear to have the strongest relationship with temperature or solar radiation among the vertebrate and invertebrate groups that have been examined thus far (Whittaker et al., 2007), and they exhibit the most spatially disparate richness pattern of the four terrestrial vertebrate classes (Lamoreux et al., 2006). Birds, on the other hand, are able to escape seasonally harsh environments and take advantage of seasonal resource pulses via migration (Hurlbert & Haskell, 2003).
Ectotherms are expected to have a higher rate of spatial turnover in species composition compared with endotherms due to their smaller range sizes (Soininen et al., 2007), which are generally thought to result from their smaller body sizes and their being sharply constrained by thermal tolerances. Broad-scale analyses of species turnover have been much less common than broad-scale analyses of species richness (but see Gaston et al., 2007). The first such study to compare turnover between vertebrate endotherms (birds and mammals) and ectotherms (amphibians) found that although areas of high turnover are congruent in the New World, areas of low turnover are not (McKnight et al., 2007). Congruence was highest between birds and amphibians, with each group exhibiting similar congruence with mammals. Species turnover across space does generally occur faster for ectotherms than endotherms (Buckley & Jetz, 2008; Qian, 2009).