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Social group size influences pathogen transmission in salamanders

Abstract

Individuals within animal societies are expected to mitigate the costs and enhance the benefits associated with group living. For example, sociality can facilitate the sharing of beneficial microbes among individuals, but can also increase transmission of pathogens, representing a major cost of group living. We examined the costs of sociality in the California slender salamander (Batrachoseps attenuatus), a terrestrial salamander which naturally forms close social aggregations. We investigated whether innate sociality (e.g., skin-to-skin contact) increases an individual’s transmission risk of Batrachochytrium dendrobatidis (Bd), a fungal pathogen that emerged throughout the salamander’s range over the last 50 years and has decimated hundreds of amphibian species globally. We found that in captivity, B. attenuatus exhibit random mixing within social groups, resulting in high contact rates and high potential for Bd transmission. Our experimental infection trials resulted in 50% mortality after 1 month in moist conditions. In order to test how group size affects pathogen transmission, we manipulated social group size and found a marked effect on the spread Bd among individuals; a single, uninfected individual contracted Bd much more rapidly in larger groups of infected individuals. Surprisingly, this did not translate into a more rapid death rate or higher pathogen infection loads. Our results show that the innate behavior of group formation represents a per-individual risk of socially acquired pathogens, with direct transmission being magnified in larger social groups. This study highlights one important cost of sociality in terrestrial salamanders and underscores the general susceptibility of social animals to novel invasive pathogens.

Significance statement

Social behaviors typically evolve due to the benefits of associating with others, but they can also present risks such as disease transmission. The California slender salamander is highly social, with individuals forming close aggregations underneath cover items. Populations of this species have recently been discovered to suffer from the widespread and deadly fungal pathogen Batrachochytrium dendrobatidis (Bd) which is transmitted through aquatic zoospores. Because this salamander host species is fully terrestrial, we set out to determine if close aggregations (leading to skin-to-skin contact) provide opportunities for direct transmission of Bd. Infection trials in larger social groups revealed a more rapid spread of Bd; however, we did not witness more rapid death rates or ultimately higher pathogen infection loads. Our results show that the social behavior of these salamanders leads to a higher probability of acquiring Bd, highlighting the complex effects that emergent pathogens may have on social species.

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Data availability

All data are on Dryad (https://doi.org/10.5061/dryad.9cnp5hqj5).

Code availability

R code is available in Dryad (https://doi.org/10.5061/dryad.9cnp5hqj5).

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Acknowledgements

We are grateful to undergraduate students Stephenie Phan Huynh, Ivet Lolham, and Jessica Fiest for assistance with animal swabbing and qPCR assays. Thank you to laboratory members Silas Ellison, Sofia Prado-Irwin, Mae Cowgill, and Alicia Bird for help with field collection and experiment setup. Sincere thanks to Dr. Andrea Swei for invaluable input during data interpretation and to the editor plus two anonymous reviewers who all provided excellent feedback and suggestions for improvement.

Funding

NSF Grant (IOS-1258133) awarded to AZ and VV. IRA Grant awarded to KR by the SFSU Department of Biology.

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KR, AZ, and VV conceived and designed study, performed statistical analyses, and wrote the manuscript. SC and HB assisted throughout study with behavioral observations, data collection, qPCR assays, and manuscript revisions. All authors gave final approval before publication.

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Correspondence to Andrew G. Zink.

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All procedures were carried out under the approval of the San Francisco State University IACUC committee (#A15-05 Zink and Ritchie). All applicable international, national, and institutional guidelines for the use of animals were followed.

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The authors have no competing interests.

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This article is a contribution to the Topical Collection Sociality and Disease – Guest Editors: Rebeca Rosengaus, James Traniello, and Theo Bakker

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Ritchie, K.L., Vredenburg, V.T., Chaukulkar, S. et al. Social group size influences pathogen transmission in salamanders. Behav Ecol Sociobiol 75, 136 (2021). https://doi.org/10.1007/s00265-021-03057-6

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Keywords

  • Amphibians
  • Chytridiomycosis
  • Disease
  • Social behavior
  • Salamanders
  • Batrachochytrium dendrobatidis