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Anthropogenic disruptions to longstanding patterns of trophic-size structure in vertebrates

Nature Ecology & Evolution volume 6, pages 684–692 (2022)Cite this article

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Abstract

Diet and body mass are inextricably linked in vertebrates: while herbivores and carnivores have converged on much larger sizes, invertivores and omnivores are, on average, much smaller, leading to a roughly U-shaped relationship between body size and trophic guild. Although this U-shaped trophic-size structure is well documented in extant terrestrial mammals, whether this pattern manifests across diverse vertebrate clades and biomes is unknown. Moreover, emergence of the U-shape over geological time and future persistence are unknown. Here we compiled a comprehensive dataset of diet and body size spanning several vertebrate classes and show that the U-shaped pattern is taxonomically and biogeographically universal in modern vertebrate groups, except for marine mammals and seabirds. We further found that, for terrestrial mammals, this U-shape emerged by the Palaeocene and has thus persisted for at least 66 million years. Yet disruption of this fundamental trophic-size structure in mammals appears likely in the next century, based on projected extinctions. Actions to prevent declines in the largest animals will sustain the functioning of Earth’s wild ecosystems and biomass energy distributions that have persisted through deep time.

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Fig. 1: Observed limits and conceptual mechanisms relating body size to trophic guild across the world’s terrestrial mammals.
Fig. 2: Contemporary global trophic-size structure across taxa.
Fig. 3: Trophic-size structure across global biomes for terrestrial mammals.
Fig. 4: Trophic-size structure of 5,427 terrestrial mammal species through time.
Fig. 5: Change in mass into the future.

Data availability

All data are available at https://github.com/willgearty/Trophic-Extremes.

Code availability

All code is available at https://github.com/willgearty/Trophic-Extremes.

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Acknowledgements

We thank the Synthesis Centre for Biodiversity Sciences of the German Centre for Integrative Biodiversity Research for funding that led to the concept of this paper (grant no. DFG FZT 118). W.G. was supported by the Population Biology Program of Excellence Postdoctoral Fellowship from the University of Nebraska-Lincoln School of Biological Sciences. J.S.L. was supported by the Michael E. Tennenbaum Secretarial Scholar gift to the Smithsonian Institution. We thank J. Csotonyi for his commissioned artwork. We thank B. Wynd and M. Tucker for feedback on earlier versions of this manuscript. This is contribution 98 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network. This is Paleobiology Database publication 420.

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Author notes

  1. These authors contributed equally: Rob Cooke, William Gearty.

Authors and Affiliations

  1. UK Centre for Ecology & Hydrology, Wallingford, UK

    Rob Cooke

  2. Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden

    Rob Cooke

  3. Gothenburg Global Biodiversity Centre, Gothenburg, Sweden

    Rob Cooke

  4. School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, USA

    William Gearty & S. Kathleen Lyons

  5. Centre for Biodiversity and Environment Research, Department of Genetics, Evolution and Environment, University College London, London, UK

    Abbie S. A. Chapman

  6. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    Jillian Dunic

  7. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia

    Graham J. Edgar & Rick D. Stuart-Smith

  8. Tennenbaum Marine Observatories Network and MarineGEO Program, Smithsonian Environmental Research Center, Edgewater, MD, USA

    Jonathan S. Lefcheck

  9. National Institute of Oceanography, Israel Limnological and Oceanographic Research, Haifa, Israel

    Gil Rilov

  10. Louisiana Universities Marine Consortium, Chauvin, LA, USA

    Craig R. McClain

  11. Biology Department, University of Victoria, Victoria, British Columbia, Canada

    Amanda E. Bates

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Contributions

R.C., W.G., A.S.A.C., J.D., G.J.E., J.S.L., G.R., C.R.M., R.D.S.-S., S.K.L. and A.E.B. conceived the project. R.C., W.G., S.K.L., A.E.B., G.J.E., R.D.S.-S., G.R. and J.S.L. contributed the data. R.C., W.G., S.K.L. and A.E.B. developed the methodology and performed the statistical analyses. R.C. and W.G. created the visualizations. A.S.A.C. and A.E.B. acquired the funding for the project. S.K.L. and A.E.B. jointly supervised the project. R.C. and W.G. wrote the original draft of the manuscript. R.C., W.G., A.S.A.C., J.D., G.J.E., J.S.L., G.R., C.R.M., R.D.S.-S., S.K.L. and A.E.B. helped revise the manuscript.

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Correspondence to Rob Cooke or William Gearty.

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Nature Ecology & Evolution thanks Marlee Tucker, Brenen Wynd and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Trophic-size structure across global biomes for terrestrial birds.

Body mass distributions per trophic guild for 8,991 terrestrial bird species across biomes. Birds were assigned to all biomes in which they occur. Labels indicate the number of species per boxplot. Biomes are ordered by their absolute latitudinal distribution. Boxplot elements and stars as in Fig. 2.

Extended Data Fig. 2 Trophic-size structure across global marine biomes for fishes.

Maximum body length distributions per trophic guild for 2,795 fish species across marine biomes. Fishes were assigned to all biomes in which they occur. Labels indicate the number of species per boxplot. Marine biomes are ordered by their absolute latitudinal distribution. Boxplot elements and stars as in Fig. 2.

Extended Data Fig. 3 Distributions of bootstrap means of terrestrial mammal body masses by trophic guild since the Early Cretaceous, 145 million years ago.

Each boxplot represents the results of 1,000 bootstrap replicates. Silhouettes show example species for each time interval. Boxplot elements as in Fig. 2. Silhouettes show example species for each time interval. Icons are all from PhyloPic.org. Creator credits: (left to right) T. Michael Keesey; Scott Hartman; Heinrich Harder; Zimices; Christine Axon; T. Michael Keesey; US National Park Service; Steven Traver, Steven Traver.

Extended Data Fig. 4 Weighted bootstrap means (±1.96 weighted standard deviation) of terrestrial mammal body masses by trophic guild since the Early Cretaceous, 145 million years ago.

Silhouettes show example species for each time interval. Icons are all from PhyloPic.org. Creator credits: (left to right) T. Michael Keesey; Scott Hartman; Heinrich Harder; Zimices; Christine Axon; T. Michael Keesey; US National Park Service; Steven Traver, Steven Traver.

Extended Data Fig. 5 Distributions of subsample means of terrestrial mammal body masses by trophic guild since the Early Cretaceous, 145 million years ago.

Each boxplot represents the results of 100 subsamples. Each panel indicates the increasing size of the subsamples (indicated by the panel titles). Boxplot elements as in Fig. 2.

Extended Data Fig. 6 Comparison of effects of predicted future extinctions and observed Pleistocene extinctions on rate of change of median body size split by trophic guild and continent.

Text near points corresponds to the continent names (AF: Africa, AUS: Australia, EA: Eurasia, NA: North America, SA: South America). Pleistocene extinctions are blue, predicted future extinctions are green. Dashed lines indicate 5th and 95th quantile regressions of Pleistocene extinctions.

Extended Data Table 1 Theoretical mechanisms of body size constraints in vertebrates by trophic guild from the primary literature
Full size table

Supplementary information

Reporting Summary

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Supplementary Tables

Supplementary Table 1: Results (P values) of pairwise Mann–Whitney U-tests of extant mammal body size distributions between different biomes by trophic guild; P values have been corrected for multiple tests. Supplementary Table 2: Results (P values) of pairwise 90th quantile permutation tests of extant mammal body size distributions between different biomes by trophic guild; P values have been corrected for multiple tests. Supplementary Table 3: List of supplementary fossil mammal body size estimates (including measurement and allometric equation sources) compiled for this paper. Supplementary Table 4: Full citation information for references used as sources for mass estimates, element measurements and allometric equations in Supplementary Table 3. Supplementary Table 5: List of all fossil mammals (Early Cretaceous to Holocene) used in the fossil analyses and their diet, estimated body size and fossil temporal range. Supplementary Table 6: List of extant mammals used for future projection analyses and their diet, body size and median extinction probability.

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Cooke, R., Gearty, W., Chapman, A.S.A. et al. Anthropogenic disruptions to longstanding patterns of trophic-size structure in vertebrates. Nat Ecol Evol 6, 684–692 (2022). https://doi.org/10.1038/s41559-022-01726-x

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