Beyond Janzen's Hypothesis: How Amphibians That Climb Tropical Mountains Respond to Climate Variation

Abstract

Janzen's Hypothesis (JH) posits that low thermal variation selects for narrow physiological tolerances, and thus small species distributional ranges and high species turnover along tropical elevational gradients. Although this hypothesis has been intensely revisited, it does not explain how many tropical species may exhibit broad distributions, encompassing altitudinal gradients. Moreover, the physiological responses of tropical species remain largely unknown, limiting our understanding on how they respond to climate variation. To fill these knowledge gaps, we tested a major component of JH, the Climate Variability Hypothesis (CVH), which predicts broader thermal tolerance breadth (Tbr = CTmax—CTmin) with broader temperature variation. Specifically, we sampled populations of five amphibian species distributed in two mountain ranges in Brazil's Atlantic Forest to test how CTmin and CTmax vary along elevational gradients. Since both thermal and water balance traits are pivotal to the evolutionary history of amphibians, we also measured rates of dehydration and rehydration and their relations with thermal tolerances. We found that broader temperature variation with increasing altitude did not always lead to broader Tbr, since changes in CTmin and CTmax were species-specific. In addition, we found that water balance did not show consistent variation with altitude, also with low correlations between hydric and thermal traits. While we also found that highland populations are at lower risk of thermal stress than lowland counterparts, both are living far from their upper thermal limits. As a consequence of intraspecific variation in physiological traits and spatial variation in climate along altitude, responses to climate variation in tropical amphibian species were context-dependent and heterogeneous. Together with recent studies showing thermal tolerances of some tropical amphibians comparable to temperate taxa, our findings highlight that several responses to climate variation in tropical species may not conform to predictions made by either the CVH or other important hypotheses concerning physiological variation. This reinforces the need to overcome geographical bias in physiological data to improve predictions of climate change impacts on biodiversity.

Acclimation Capacity to Global Warming of Amphibians and Freshwater Fishes: Drivers, Patterns, and Data Limitations

“…Addressing this issue can yield additional, important insights, as such geographic bias in existing data sets has been shown to limit our ability to predict organismal responses in these (Bovo et al, 2023).…”

“…Therefore, focusing on large-scale geographical patterns for predicting how biodiversity will respond to future environmental change might bear the risk of overlooking context-dependent variation in thermal traits and thus, intraspecific differences in vulnerability to changing thermal conditions (Duarte et al 2012, Gutierrez-Pesquera et al 2016). For example, Bovo et al (2023) demonstrated that responses of tropical amphibians to climate variation were heterogenous as a consequence of intraspecific variation in physiological traits and spatial variation in climate with elevation. Furthermore, Sunday et al (2011) and Pinsky et al (2019) reported that the physiological sensitivity of ectotherms across all latitudes depended on the realm, with terrestrial ectotherms being less sensitive to warming than aquatic ectotherms due to their higher capacity for behavioral thermoregulation.…”

“…Therefore, focusing on large-scale geographical patterns for predicting how biodiversity will respond to future environmental change might bear the risk of overlooking context-dependent variation in thermal traits and thus, intraspecific differences in vulnerability to changing thermal conditions. For example, Bovo et al (2023) demonstrated that responses of tropical amphibians to climate variation were heterogenous as a consequence of intraspecific variation in physiological traits and spatial variation in climate with elevation.…”

“…However, our key findings emphasize that assessing species' vulnerability to changing thermal conditions based on large-scale geographic and/or phylogenetic patterns in thermal traits might cover up context-dependent physiological adaptations. In other words, tropical ectothermic species are considered particularly vulnerable to global warming as they live close to their physiological limits and have poor acclimation ability (Tewksbury et al 2008;Huey et al 2009;Sunday et al 2014), but such generalizations might for instance ignore intraspecific variation in physiological limits across variation in climate with elevation (Bovo et al 2023). Physiological adaptations are driven by the interplay between microclimate temperature heterogeneity and the behavioral thermoregulatory abilities of ectotherms (Huey et al 2012;Pincebourde et al 2016; present study) depending on their habitat characteristics (Pinsky et al 2019;Kulkarni et al 2017), ontogeny (Enriquez-Urzelai et al 2019Ruthsatz et al 2022a), life history traits such as body size (Rubalcaba et al 2020;Peralta-Maraver & Rezende 2021) or activity patterns (Navas et al 2007;Ruthsatz et al 2022b), and/or energy balance (Pörtner et al 2005;Muñoz et al 2022).…”

“…This biogeographical pattern is consistent with the climate variability hypothesis (Janzen 1967; Ghalambor et al 2006), suggesting that climatic differences across altitudinal and latitudinal gradients lead to corresponding adaptations in thermal physiology (but see: Gutiérrez-Pesquera et al 2022). Low-latitude species adapted to relatively stable temperature conditions may have a lower acclimation capacity and, therefore, may be more vulnerable to climate change (Tewksbury et al 2008; Sunday et al 2014; but see: Bovo et al 2023). However, there is still little empirical evidence supporting the climate variability hypothesis, possibly due to the limited geographical and phylogenetic coverage of observations, and because of the inconsistency of the methods applied to measure the acclimation capacity of different species and life stages (Gutiérrez-Pesquera et al 2016; Shah et al 2017).…”