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Frugivore gut passage increases seed germination: an updated meta-analysis

View ORCID ProfileHaldre S. Rogers, Brittany R. Cavazos, Ann Marie Gawel, Alex Karnish, Courtenay A. Ray, Ethan Rose, Hugo Thierry, View ORCID ProfileEvan C. Fricke
doi: https://doi.org/10.1101/2021.10.12.462022
Haldre S. Rogers
1Department of Ecology, Evolution, and Organismal Biology. Iowa State University, Ames, IA, USA
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  • For correspondence: haldre@iastate.edu
Brittany R. Cavazos
1Department of Ecology, Evolution, and Organismal Biology. Iowa State University, Ames, IA, USA
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Ann Marie Gawel
1Department of Ecology, Evolution, and Organismal Biology. Iowa State University, Ames, IA, USA
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Alex Karnish
2Department of Ecology and Evolutionary Biology. University of Arizona, Tucson, AZ, USA
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Courtenay A. Ray
3Department of Environmental Science, Policy, and Management. University of California, Berkeley, CA, USA
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Ethan Rose
4Department of Biological Sciences. Marquette University, Milwaukee, WI, USA
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Hugo Thierry
5Department of Geography. McGill University, Montreal, QC, Canada
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Evan C. Fricke
6Department of BioSciences. Rice University, Houston, TX, USA
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ABSTRACT

Many plants rely on animal mutualists for reproduction. Quantifying how animal mutualists impact plant performance provides a foundation for modelling how change in animal communities affects the composition and functioning of plant communities. We performed a meta-analysis of 2539 experiments, 6 times more than the last comprehensive meta-analysis, examining how gut passage by frugivores influences seed germination. We simultaneously analyzed multiple predictor variables related to study methodology, location, and frugivore identity to disentangle methodological from ecological impacts on effect sizes. We found that gut passage by birds, fish, reptiles, bats, primates, and other mammals on average increased seed germination, but that the magnitude varied across vertebrate groups. The positive effects of gut passage were largely explained by the de-inhibitory effects of pulp removal rather than by the scarification of seed tissues. Some previous studies and meta-analyses that found no effect of gut passage only tested scarification or did not distinguish between these tests of scarification and pulp removal. We found that, for a typical fleshy-fruited plant species, the lack of gut passage reduces germination by 60%. From an evolutionary perspective, this indicates a large risk associated with reliance on animal mutualists that is balanced against the benefits of animal-mediated seed dispersal. From a conservation perspective, this highlights the potential for large demographic consequences of frugivore declines on plant populations. Our database and findings advance quantitative predictions for the role of fruit-frugivore interactions in shaping plant communities in the Anthropocene.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Authorship: HSR conceived of the project, organized data collection and designed the database with AK, and wrote the first draft of the manuscript. ECF conducted analyses and produced figures. All authors contributed to data collection and revision of the manuscript.

  • https://github.com/EBL-Marianas/gut-passage-germination-metaanalysis.git

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 13, 2021.
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Frugivore gut passage increases seed germination: an updated meta-analysis
Haldre S. Rogers, Brittany R. Cavazos, Ann Marie Gawel, Alex Karnish, Courtenay A. Ray, Ethan Rose, Hugo Thierry, Evan C. Fricke
bioRxiv 2021.10.12.462022; doi: https://doi.org/10.1101/2021.10.12.462022
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Frugivore gut passage increases seed germination: an updated meta-analysis
Haldre S. Rogers, Brittany R. Cavazos, Ann Marie Gawel, Alex Karnish, Courtenay A. Ray, Ethan Rose, Hugo Thierry, Evan C. Fricke
bioRxiv 2021.10.12.462022; doi: https://doi.org/10.1101/2021.10.12.462022

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