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Thermal performance across levels of biological organization.

ABSTRACT: Thermal performance curves are widely used to describe how ambient temperature impacts different attributes of ectothermic organisms, from protein function to life-history traits, and to predict the potential effects of global warming on ecological systems. Nonetheless, from an analytical standpoint, they remain primarily heuristic and few attempts have been made to develop a formal framework to characterize these curves and disentangle which factors contribute to their variation. Here we employ a nonlinear regression approach to assess if they vary systematically in shape depending on the performance proxy of choice. We compare curves at contrasting levels of organization, namely photosynthetic rates in plants ( n = 43), running speeds in lizards ( n = 51) and intrinsic rates of population increase in insects ( n = 47), and show with discriminant analyses that differences lie in a single dimension accounting for 99.1% of the variation, resulting in 75.8% of classification accuracy. Differences revolve primarily around the thermal range for elevated performance (greater than or equal to 50% of maximum performance), which is broader for photosynthetic rates (median of 26.4°C), intermediate for running speeds (19.5°C) and narrower for intrinsic rates of increase (12.5°C). We contend, confounding taxonomic factors aside, that these differences reflect contrasting levels of biological organization, and hypothesize that the thermal range for elevated performance should decrease at higher organization levels. In this scenario, instantaneous or short-term measures of performance may grossly overestimate the thermal safety margins for population growth and reproduction. Taken together, our analyses suggest that descriptors of the curve are highly correlated and respond in tandem, potentially resulting in systematic variation in shape across organization levels. Future studies should take into consideration this potential bias, address if it constitutes a general pattern and, if so, explain why and how it emerges. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.

SUBMITTER: Rezende EL

PROVIDER: S-EPMC6606466 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Thermal performance across levels of biological organization.

Rezende Enrico L EL Bozinovic Francisco F

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20190617 1778

Thermal performance curves are widely used to describe how ambient temperature impacts different attributes of ectothermic organisms, from protein function to life-history traits, and to predict the potential effects of global warming on ecological systems. Nonetheless, from an analytical standpoint, they remain primarily heuristic and few attempts have been made to develop a formal framework to characterize these curves and disentangle which factors contribute to their variation. Here we employ ...[more]

PMID: 31203764

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Project description:Understanding links between thermal performance and environmental variation is necessary to predict organismal responses to climate change, and remains an ongoing challenge for ectotherms with complex life cycles. Distinct life stages can differ in thermal sensitivity, experience different environmental conditions as development unfolds, and, because stages are by nature interdependent, environmental effects can carry over from one stage to affect performance at others. Thermal performance may therefore respond to carryover effects of prior thermal environments, yet detailed insights into the nature, strength, and direction of those responses are still lacking. Here, in an aquatic ectotherm whose early planktonic stages (gametes, embryos, and larvae) govern adult abundances and dynamics, we explore the effects of prior thermal environments at fertilization and embryogenesis on thermal performance curves at the end of planktonic development. We factorially manipulate temperatures at fertilization and embryogenesis, then, for each combination of prior temperatures, measure thermal performance curves for survival of planktonic development (end of the larval stage) throughout the performance range. By combining generalized linear mixed modeling with parametric bootstrapping, we formally estimate and compare curve descriptors (thermal optima, limits, and breadth) among prior environments, and reveal carryover effects of temperature at embryogenesis, but not fertilization, on thermal optima at completion of development. Specifically, thermal optima shifted to track temperature during embryogenesis, while thermal limits and breadth remained unchanged. Our results argue that key aspects of thermal performance are shaped by prior thermal environment in early life, warranting further investigation of the possible mechanisms underpinning that response, and closer consideration of thermal carryover effects when predicting organismal responses to climate change.

Dataset Information

Thermal performance across levels of biological organization.

Publications

Thermal performance across levels of biological organization.

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