TY - JOUR
T1 - Impact of warming on aquatic body sizes explained by metabolic scaling from microbes to macrofauna
AU - Deutsch, Curtis
AU - Penn, Justin L.
AU - Verberk, Wilco C.E.P.
AU - Inomura, Keisuke
AU - Endress, Martin Georg
AU - Payne, Jonathan L.
N1 - Publisher Copyright:
Copyright © 2022 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
PY - 2022/7/12
Y1 - 2022/7/12
N2 - Rising temperatures are associated with reduced body size in many marine species, but the biological cause and generality of the phenomenon is debated. We derive a predictive model for body size responses to temperature and oxygen (O2) changes based on thermal and geometric constraints on organismal O2 supply and demand across the size spectrum. The model reproduces three key aspects of the observed patterns of intergenerational size reductions measured in laboratory warming experiments of diverse aquatic ectotherms (i.e., the “temperature-size rule” [TSR]). First, the interspecific mean and variability of the TSR is predicted from species' temperature sensitivities of hypoxia tolerance, whose nonlinearity with temperature also explains the second TSR pattern-its amplification as temperatures rise. Third, as body size increases across the tree of life, the impact of growth on O2 demand declines while its benefit to O2 supply rises, decreasing the size dependence of hypoxia tolerance and requiring larger animals to contract by a larger fraction to compensate for a thermally driven rise in metabolism. Together our results support O2 limitation as the mechanism underlying the TSR, and they provide a physiological basis for projecting ectotherm body size responses to climate change from microbes to macrofauna. For small species unable to rapidly migrate or evolve greater hypoxia tolerance, ocean warming and O2 loss in this century are projected to induce >20% reductions in body mass. Size reductions at higher trophic levels could be even stronger and more variable, compounding the direct impact of human harvesting on size-structured ocean food webs.
AB - Rising temperatures are associated with reduced body size in many marine species, but the biological cause and generality of the phenomenon is debated. We derive a predictive model for body size responses to temperature and oxygen (O2) changes based on thermal and geometric constraints on organismal O2 supply and demand across the size spectrum. The model reproduces three key aspects of the observed patterns of intergenerational size reductions measured in laboratory warming experiments of diverse aquatic ectotherms (i.e., the “temperature-size rule” [TSR]). First, the interspecific mean and variability of the TSR is predicted from species' temperature sensitivities of hypoxia tolerance, whose nonlinearity with temperature also explains the second TSR pattern-its amplification as temperatures rise. Third, as body size increases across the tree of life, the impact of growth on O2 demand declines while its benefit to O2 supply rises, decreasing the size dependence of hypoxia tolerance and requiring larger animals to contract by a larger fraction to compensate for a thermally driven rise in metabolism. Together our results support O2 limitation as the mechanism underlying the TSR, and they provide a physiological basis for projecting ectotherm body size responses to climate change from microbes to macrofauna. For small species unable to rapidly migrate or evolve greater hypoxia tolerance, ocean warming and O2 loss in this century are projected to induce >20% reductions in body mass. Size reductions at higher trophic levels could be even stronger and more variable, compounding the direct impact of human harvesting on size-structured ocean food webs.
KW - climate change
KW - ecophysiology
KW - hypoxia
KW - metabolic index
KW - temperature-size rule
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U2 - 10.1073/pnas.2201345119
DO - 10.1073/pnas.2201345119
M3 - Article
C2 - 35787059
AN - SCOPUS:85133228915
SN - 0027-8424
VL - 119
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 28
M1 - e2201345119
ER -