How seasonality influences the thermal biology of lizards with different thermoregulatory strategies: a meta‐analysis

Abstract

Ectotherms that maintain thermal balance in the face of varying climates should be able to colonise a wide range of habitats. In lizards, thermoregulation usually appears as a variety of behaviours that buffer external influences over physiology. Basking species rely on solar radiation to raise body temperatures and usually show high thermoregulatory precision. By contrast, species that do not bask are often constrained by climatic conditions in their habitats, thus having lower thermoregulatory precision. While much focus has been given to the effects of mean habitat temperatures, relatively less is known about how seasonality affects the thermal biology of lizards on a macroecological scale. Considering the current climate crisis, assessing how lizards cope with temporal variations in environmental temperature is essential to understand better how these organisms will fare under climate change. Activity body temperatures (Tb) represent the internal temperature of an animal measured in nature during its active period (i.e. realised thermal niche), and preferred body temperatures (Tpref) are those selected by an animal in a laboratory thermal gradient that lacks thermoregulatory costs (i.e. fundamental thermal niche). Both traits form the bulk of thermal ecology research and are often studied in the context of seasonality. In this study, we used a meta‐analysis to test how environmental temperature seasonality influences the seasonal variation in the Tb and Tpref of lizards that differ in thermoregulatory strategy (basking versus non‐basking). Based on 333 effect sizes from 137 species, we found that Tb varied over a greater magnitude than Tpref across seasons. Variations in Tb were not influenced by environmental temperature seasonality; however, body size and thermoregulatory strategy mediated Tb responses. Specifically, larger species were subjected to greater seasonal variations in Tb, and basking species endured greater seasonal variations in Tb compared to non‐basking species. On the other hand, the seasonal variation in Tpref increased with environmental temperature seasonality regardless of body size. Thermoregulatory strategy also influenced Tpref, suggesting that behaviour has an important role in mediating Tpref responses to seasonal variations in the thermal landscape. After controlling for phylogenetic effects, we showed that Tb and Tpref varied significantly across lizard families. Taken together, our results support the notion that the relationship between thermal biology responses and climatic parameters can be taxon and trait dependent. Our results also showcase the importance of considering ecological and behavioural aspects in macroecological studies. We further highlight current systematic, geographical, and knowledge gaps in thermal ecology research. Our work should benefit those who aim to understand more fully how seasonality shapes thermal biology in lizards, ultimately contributing to the goal of elucidating the evolution of temperature‐sensitive traits in ectotherms.

Seasonal variation of behavioural thermoregulation in the Spotted Salamander (Ambystoma maculatum)

“…Long-lived organisms experience seasonal shifts in climate multiple times over their lives (Williams et al, 2017), and seasonality has been shown to exert a strong selection pressure over the thermal biology of ectotherms (Clusella-Trullas et al, 2011; Giacometti et al, 2023). To cope with seasonality, some species may enter dormancy during periods of low environmental temperatures (Tattersall et al, 2016) or drought (Carvalho et al, 2010).…”

“…As a result, ectotherms from seasonal habitats typically exhibit different thermoregulatory behaviours, target different T b s between seasons, and are able to sustain activity across a wide range of T b s (Gilchrist, 1995; Hadamová and Gvoždík, 2011; Sepúlveda et al, 2008). Thus, by documenting seasonal changes in thermoregulatory parameters one may gain insight into the behavioural processes that underlie T b control in ectotherms (Giacometti et al, 2023). Among vertebrate ectotherms, inquiry into the effect of seasonality over thermoregulation is taxonomically biased toward lizards (e.g., Clusella-Trullas and Chown, 2014; Giacometti et al, 2023; Huey and Pianka, 1977).…”

“…Thus, by documenting seasonal changes in thermoregulatory parameters one may gain insight into the behavioural processes that underlie T b control in ectotherms (Giacometti et al, 2023). Among vertebrate ectotherms, inquiry into the effect of seasonality over thermoregulation is taxonomically biased toward lizards (e.g., Clusella-Trullas and Chown, 2014; Giacometti et al, 2023; Huey and Pianka, 1977). Truly, despite the relatively large number of studies using amphibians as model systems in thermal biology research (e.g., Carilo Filho et al, 2022; Hutchison and Dupré, 1992), the extent to which thermal traits are capable of seasonal acclimation (i.e., response to a single environmental parameter) or acclimatisation (i.e., response to multiple environmental parameters) remains unclear (Navas et al, 2021; but see Pottier et al, 2022).…”

“…However, solely highlighting patterns of T sel change does not provide enough information on the behavioural processes that underlie T b control. Thus, it is important not to assume a priori that any seasonal change in T sel occurs due to a shift in the motivation to thermoregulate (Giacometti et al, 2023), especially in species that may not use overt behaviours for T b control. To overcome this limitation, behavioural observations may be integrated with T sel measurements; past information on the study species is key to determine which behaviours should be scored (Giacometti et al, 2021).…”

“…Theory predicts that overt thermoregulatory behaviours should not be favoured in species from thermally stable habitats, given the limited thermoregulatory benefit (Ruibal, 1961; Shine and Madsen, 1996). Thus, one may expect that fossorial species should show relatively low evidence of thermotactic behaviours, and that seasonal fluctuations in temperature should not have a relevant impact over the thermal biology of these species (Giacometti et al, 2023; Wu et al, 2009). Importantly, although A .…”