Intraspecific variation in lizard heat tolerance alters estimates of climate impact

Abstract

Research addressing the effects of global warming on the distribution and persistence of species generally assumes that population variation in thermal tolerance is spatially constant or overridden by interspecific variation. Typically, this rationale is implicit in sourcing one critical thermal maximum (CTmax) population estimate per species to model spatiotemporal cross‐taxa variation in heat tolerance. Theory suggests that such an approach could result in biased or imprecise estimates and forecasts of impact from climate warming, but limited empirical evidence in support of those expectations exists. We experimentally quantify the magnitude of intraspecific variation in CTmax among lizard populations, and the extent to which incorporating such variability can alter estimates of climate impact through a biophysical model. To do so, we measured CTmax from 59 populations of 15 Iberian lizard species (304 individuals). The overall median CTmax across all individuals from all species was 42.8°C and ranged from 40.5 to 48.3°C, with species medians decreasing through xeric, climate‐generalist and mesic taxa. We found strong statistical support for intraspecific differentiation in CTmax by up to a median of 3°C among populations. We show that annual restricted activity (operative temperature > CTmax) over the Iberian distribution of our study species differs by a median of >80 hr per 25‐km2 grid cell based on different population‐level CTmax estimates. This discrepancy leads to predictions of spatial variation in annual restricted activity to change by more than 20 days for six of the study species. Considering that during restriction periods, reptiles should be unable to feed and reproduce, current projections of climate‐change impacts on the fitness of ectotherm fauna could be under‐ or over‐estimated depending on which population is chosen to represent the physiological spectra of the species in question. Mapping heat tolerance over the full geographical ranges of single species is thus critical to address cross‐taxa patterns and drivers of heat tolerance in a biologically comprehensive way.

Heat tolerance is more variable than cold tolerance across species of Iberian lizards after controlling for intraspecific variation

“…Sampling effort totalled 2–5 populations per species (median = 4 populations/species with 90% interquartile ranges of [3, 4]), and 3–10 males/population (5 [5, 6]). A minimum sample size of three males per population should accurately capture the mean population CT max estimated from larger sample sizes (Herrando‐Pérez, Ferri‐Yáñez, et al, ), and is within the range of published work (e.g. Beal, Lattanzio, & Miles, ; Muñoz et al, ).…”

“…This seems unsurprising given that the thermal environment experienced by lizards can vary by up to 20°C as a result of the landscape heterogeneity imposed by vegetation, topography and geology (Sears, Raskin, & Angilletta, ), and such thermal variation compares well with the magnitude of warming expected in the most pessimistic scenarios of future climate change (Suggitt et al, ). Without population‐level data and quantitative methods incorporating population‐level trait variation (discussed by Herrando‐Pérez, Ferri‐Yáñez, et al, ), coarse climatic indices can fail to capture how heat and cold tolerances of species interact with regional climatic shifts (Garcia, Allen, & Clusella‐Trullas, ; Sears & Angilletta, ) in both the cold and warm margins of species distributions (Nadeau & Urban, ). For instance, latitudinal clines of thermal tolerance for several beetle species are more pronounced for heat tolerance in the southern (hot) margins of species distributions than for cold tolerance in the northern (cold) margins (Calosi, Bilton, Spicer, Votier, & Atfield, ).…”

“…Such scenario can be relevant for Iberian high‐altitude species ( Iberolacerta spp.) and, particularly, the endangered Spanish algyroides Algyroides marchi by virtue of its confined distribution to the Alcaraz, Cazorla and Segura mountain ranges, low CT max (comparable to that of high‐altitude species; see Table ; Herrando‐Pérez, Ferri‐Yáñez, et al, ) and preference for shady, humid environments (Rubio & Martín, ).…”

“…Our populations were identical to those used by Herrando‐Pérez, Ferri‐Yáñez, et al ()—barring one Spanish population of the common wall lizard Podarcis muralis from Moncayo (Soria), which we excluded because only CT max data were available. Owing to the amount of fieldwork required, our sampling scheme was designed to cover a grid of localities maximizing species richness with minimum travelled distance, and capturing at least half of the length of the climate gradients occupied by each species (described by Herrando‐Pérez, Ferri‐Yáñez, et al, ). Thus, for most of our study species, their climatic ranges vary over regions experiencing a gradient from high Spring‐to‐Autumn precipitation to high Summer temperatures.…”

“…Here, we explicitly test this assumption by querying the extent to which intraspecific variability in thermal limits can change the frequency and direction of thermal‐tolerance asymmetries using CT max and CT min from 58 populations of 15 species of Iberian lizards. This is an important area of enquiry because intraspecific variation in thermal tolerance of ectotherm fauna (see Clusella‐Trullas & Chown, ; Sinclair et al, ) is a major component structuring biological communities (Violle et al, ), can improve our forecasts of biodiversity responses to environmental change (Artacho, Saravia, Perret, Bartheld, & Galliard, ; Kolbe, Kearney, & Shine, ; Lancaster, ; Valladares et al, ) and, if disregarded, result in rival predictions of the amount of time over which environmental temperatures might exceed a species' CT max (Herrando‐Pérez, Ferri‐Yáñez, et al, ).…”