Rethinking the scale and formulation of indices assessing organism vulnerability to warmer habitats

García, Raquel; Allen, Jessica L.; Clusella‐Trullas, Susana

doi:10.1111/ecog.04226

Cited by 26 publications

(34 citation statements)

References 87 publications

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“…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, ).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2020

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The widespread observation that heat tolerance is less variable than cold tolerance (‘cold‐tolerance asymmetry’) leads to the prediction that species exposed to temperatures near their thermal maxima should have reduced evolutionary potential for adapting to climate warming. However, the prediction is largely supported by species‐level global studies based on single estimates of both physiological metrics per taxon. We ask whether cold‐tolerance asymmetry holds for Iberian lizards after accounting for intraspecific variation in critical thermal maxima (CTmax) and minima (CTmin). To do so, we quantified CTmax and CTmin for 58 populations of 15 Iberian lizard species (299 individuals). Then, we randomly selected one population from each study species (population sample = 15 CTmax and CTmin values), tested for differences between the variance of both thermal metrics across species, and repeated the test for thousands of population samples as if we had undertaken the same study thousands of times, each time sampling one different population per species (as implemented in global studies). The ratio of variances in CTmax to CTmin across species varied up to 16‐fold depending on the populations chosen. Variance ratios show how much CTmax departs from the cross‐species mean compared to CTmin, with a unitary ratio indicating equal variance of both thermal limits. Sampling one population per species was six times more likely to result in the observation of greater CTmax variance (‘heat‐tolerance asymmetry’) than cold‐tolerance asymmetry. The probability of obtaining the data (given the null hypothesis of equal variance being true) was twice as likely for cases of cold‐tolerance asymmetry than for the opposite scenario. Range‐wide, population‐level studies that quantify heat and cold tolerance of individual species are urgently needed to ascertain the global prevalence of cold‐tolerance asymmetry. While broad latitudinal clines of cold tolerance have been strongly supported, heat tolerance might respond to smaller‐scale climatic and habitat factors hence go unnoticed in global studies. Studies investigating physiological responses to climate change should incorporate the extent to which thermal traits are characteristic of individuals, populations and/or species. A free Plain Language Summary can be found within the Supporting Information of this article.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2020

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“…These two means are separated by a given number of generations g. Thus, Haldanes express evolutionary change expected for the temperature, in units of standard deviations (SD), per generation (Gingerich 2001, Kopp andMatuszewski 2014). In a certain sense, a high Haldane indicates a distance between future and current climate, and so is correlated with vulnerability to warming climates (assuming that species are currently in equilibrium with climate; Garcia et al 2019 for a recent review of indices).…”

Section: A Brief Overview Of Evolutionary Rescue Models Evolutionary mentioning

confidence: 99%

A macroecological approach to evolutionary rescue and adaptation to climate change

et al. 2019

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Despite the widespread use of ecological niche models (ENMs) for predicting the responses of species to climate change, these models do not explicitly incorporate any population‐level mechanism. On the other hand, mechanistic models adding population processes (e.g. biotic interactions, dispersal and adaptive potential to abiotic conditions) are much more complex and difficult to parameterize, especially if the goal is to predict range shifts for many species simultaneously. In particular, the adaptive potential (based on genetic adaptations, phenotypic plasticity and behavioral adjustments for physiological responses) of local populations has been a less studied mechanism affecting species’ responses to climatic change so far. Here, we discuss and apply an alternative macroecological framework to evaluate the potential role of evolutionary rescue under climate change based on ENMs. We begin by reviewing eco‐evolutionary models that evaluate the maximum sustainable evolutionary rate under a scenario of environmental change, showing how they can be used to understand the impact of temperature change on a Neotropical anuran species, the Schneider's toad Rhinella diptycha. Then we show how to evaluate spatial patterns of species’ geographic range shift using such models, by estimating evolutionary rates at the trailing edge of species distribution estimated by ENMs and by recalculating the relative amount of total range loss under climate change. We show how different models can reduce the expected range loss predicted for the studied species by potential ecophysiological adaptations in some regions of the trailing edge predicted by ENMs. For general applications, we believe that parameters for large numbers of species and populations can be obtained from macroecological generalizations (e.g. allometric equations and ecogeographical rules), so our framework coupling ENMs with eco‐evolutionary models can be applied to achieve a more accurate picture of potential impacts from climate change and other threats to biodiversity.

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“…Cold is a prominent limiting factor in the distribution of animals. Not only is it a pronounced and widespread abiotic challenge for many species (Franks et al 1990, Williams et al 2015), but it also profoundly affects the ecological communities within which species interact (Garcia et al 2019). Ambient temperature change thus simultaneously presents direct thermoregulatory challenges for animals and imposes biotic stresses via, for example, its impact on food availability (Hou et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Cold and hungry: combined effects of low temperature and resource scarcity on an edge‐of‐range temperate primate, the golden snub‐nose monkey

et al. 2020

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Both biotic and abiotic factors play important roles in influencing ecological distributions and niche limits. Where biotic and abiotic stressors co‐occur in space and time, homeostatic systems face a scenario in which stressors can compound to impose a challenge that is greater than the sum of the separate factors. We studied the homeostatic strategies of the golden snub‐nosed monkey Rhinopithecus roxellana, a species living in temperate deciduous forests at the edge of the global distribution range for folivorous primates, to cope with the co‐occurrence of cold temperatures and resource scarcity during winter. We discovered that in winter the monkeys experience a dietary energy deficit of 101 kJ mbm−1 d−1 compared with calculated needs, despite increased feeding. This is partly offset by behavioral changes (reduced locomotion and increased resting) and reducing skin temperature by an average of 3.2°C through a cutaneous vasoconstriction to decrease heat loss. However, their major strategy is ingesting surplus energy and accumulating fat reserves when food was not limiting during summer and autumn. Their 14% of body mass lost over the winter represented an energy yield of 102 kJ mbm−1 d−1, which closely matched the calculated winter energy deficit of 101 kJ mbm−1 d−1. However, the latter value assumes that all the 75.41 kJ mbm−1 d−1 of protein ingested in winter was available for energy metabolism. This is almost certainly an over‐estimate, suggesting that the study population was in negative energy balance over the study period. Our study therefore suggests that despite its suit of integrated homeostatic responses, the confluence of low temperatures and resource limitation during winter places this edge‐of‐range primate close the threshold of what is energetically viable. It also provides a framework for quantitative models predicting the vulnerability of temperate primates to global change.

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Rethinking the scale and formulation of indices assessing organism vulnerability to warmer habitats

Cited by 26 publications

References 87 publications

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

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

A macroecological approach to evolutionary rescue and adaptation to climate change

Cold and hungry: combined effects of low temperature and resource scarcity on an edge‐of‐range temperate primate, the golden snub‐nose monkey

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