Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers

Abstract

Global warming appears to favour smaller-bodied organisms, but whether larger species are also more vulnerable to thermal extremes, as suggested for past mass-extinction events, is still an open question. Here, we tested whether interspecific differences in thermal tolerance (heat and cold) of ectotherm organisms are linked to differences in their body mass and genome size (as a proxy for cell size). Since the vulnerability of larger, aquatic taxa to warming has been attributed to the oxygen limitation hypothesis, we also assessed how body mass and genome size modulate thermal tolerance in species with contrasting breathing modes, habitats and life stages. A database with the upper (CTmax) and lower (CTmin) critical thermal limits and their methodological aspects was assembled comprising more than 500 species of ectotherms. Our results demonstrate that thermal tolerance in ectotherms is dependent on body mass and genome size and these relationships became especially evident in prolonged experimental trials where energy efficiency gains importance. During long-term trials, CTmax was impaired in larger-bodied water-breathers, consistent with a role for oxygen limitation. Variation in CTmin was mostly explained by the combined effects of body mass and genome size and it was enhanced in larger-celled, air-breathing species during long-term trials, consistent with a role for depolarization of cell membranes. Our results also highlight the importance of accounting for phylogeny and exposure duration. Especially when considering long-term trials, the observed effects on thermal limits are more in line with the warming-induced reduction in body mass observed during long-term rearing experiments. This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.

The biogeography of thermal risk for terrestrial ectotherms: Scaling of thermal tolerance with body size and latitude

“…Because large ants exhibit greater thermal inertia, they can resist warmer surface temperatures (Kaspari & Weiser, 1999), which should allow large animals to escape suboptimal microhabitats that could rather be fatal for smaller individuals (Kaspari et al, 2015). Evidence for the oppo- Leiva et al, 2019). The oxygen limitation hypothesis provides an explanation for this negative relationship between heat tolerance and body size in aquatic organisms (Leiva et al, 2019;Verberk & Bilton, 2011).…”

“…Evidence for the oppo- Leiva et al, 2019). The oxygen limitation hypothesis provides an explanation for this negative relationship between heat tolerance and body size in aquatic organisms (Leiva et al, 2019;Verberk & Bilton, 2011). Quite interestingly, the hypotheses based on different mechanisms such as the oxygen-limitation or heat-balance hypotheses (Figure 1) A large body of evidence shows that temperature determines growth rates and body size in ectotherms resulting in a widespread temperature-size rule (Angilletta & Dunham, 2003;Kingsolver & Huey, 2008;Ohlberger, 2013).…”

“…In terrestrial ectotherms, however, empirical studies investigating the effect of body size on body temperature and thermal tolerance limits have reported mixed results, showing positive (e.g. Kaspari, Clay, Lucas, Yanoviak, & Kay, 2015;Ribeiro, Camacho, & Navas, 2012), negative or absence of relationship between body size and thermal traits, with a much-debated mechanistic basis (Clusella-Trullas, Blackburn, & Chown, 2011;Clusella-Trullas & Chown, 2014;Leiva et al, 2019;Meiri et al, 2013). The use of null models based on biophysical mechanisms linking body size and temperature can provide baseline expectations with which to address this lack of consensus on how thermal traits scale with size in terrestrial ectotherms.…”

“…These latitudinal gradients in heat balance may also influence thermal tolerance breadths (the difference between critical thermal maximum, CT max , and critical thermal minimum, CT min ), which have been documented to increase with latitude in terrestrial environments owing to the greater thermal amplitudes found in temperate regions (Clusella-Trullas et al, 2011;Clusella-Trullas & Chown, 2014;Deutsch et al, 2008;Sunday, Bates, & Dulvy, 2010). However, our current knowledge on the mechanisms underpinning these broad-scale variations in physiological and morphological traits is hampered by multiple methodological issues (reviewed in Kovacevic, Latombe, & Chown, 2019;Leiva et al, 2019). For example, the latitudinal effect on both body mass and thermal tolerance limits can either give rise to spurious relationships or erode the statistical effect of mechanisms determining how organisms respond to climate.…”

City limits: Heat tolerance is influenced by body size and hydration state in an urban ant community

“…4.6b, open‐access) was used to perform linear regression analyses that accounted for the effects of phylogeny. Previous work on heat tolerance indicates that using phylogenetically informed models results in consistently better fits of the data than noninformed models (Leiva, Calosi, & Verberk, 2019). Thus, CT max was regressed on each dependent variable from Hypotheses 1–3 (dry body mass, T active , and relative [%] body water content, respectively) using three linear regression analyses (i.e., one analysis for each independent variable) and phylogenetically generalized least squares methods (PGLS).…”