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Social network characteristics and predicted pathogen transmission in summer colonies of female big brown bats (Eptesicus fuscus)

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Abstract

Host behavior can affect host-pathogen dynamics, and sociality is predicted to increase risk of pathogen exposure. Many species minimize costs of parasitism by only aggregating seasonally, such as during reproductive periods, but colonial species may still be limited in their potential to evade pathogens. Bats are among the most gregarious mammals and females of many temperate species form maternity colonies in summer where they communally raise pups in both natural and anthropogenic roost structures. Social network structure may differ between natural and anthropogenic roosts in ways that affect pathogen dynamics. We used social network analysis to quantify interactions of big brown bats (Eptesicus fuscus) in a tree-roosting colony, where the colony is divided among multiple trees each day, and a building colony, where most of the colony roosts together each day. We simulated transmission of a pathogen throughout both sets of networks. We tested three hypotheses: (1) network metrics differ between pregnancy and lactation; (2) changing network structure between reproductive stages influences predicted pathogen dynamics; and (3) network metrics and predicted pathogen dynamics differ between colonies of bats in trees versus buildings. Network structure was weaker for bats roosting in trees during pregnancy and lactation compared to bats roosting in a building, and our models showed that a hypothetical pathogen would spread more rapidly for bats in the building colony. Our results are important for understanding variation in social tendencies and pathogen transmission among colonies of bats and have implications for conservation and public health.

Significance statement

Host behavior, particularly social behavior, can affect dynamics of wildlife pathogens. Bats are highly social mammals and females of temperate species form colonies in spring and early summer in tree or building roosts. Thermal characteristics of trees and buildings appear to differ in ways that affect roosting behavior and social interactions. We used social network analyses to quantify interactions of big brown bats in tree and building roosts and simulated consequences for pathogen dynamics. Network structure was weaker for bats roosting in trees with more frequent roost switching and relatively diffuse contacts across the network. Our models showed that a hypothetical pathogen could spread up to four times faster in a building colony compared to a colony of bats roosting in trees. Our results are important for understanding how sociality can influence pathogen dynamics in bats and have implications for conservation and public health.

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Acknowledgments

We are grateful to Julie Adams, Ryan Fisher, Quinn Fletcher, Amanda Karst, Kristen Kolar, Seb Martinez, Melissa Ranalli, Christine Voss, and Michael Yaremko for helping with fieldwork in the Cypress Hills. We thank all staff and volunteers who collected data in Fort Collins. We also thank Alex Silvis for help with social network analysis, Quinn Fletcher, Gerald Wilkinson, and two anonymous reviewers for outstanding suggestions on earlier versions of this manuscript. Funding was provided by a Discovery Grant to CKRW from the Natural Sciences and Engineering Research Council (NSERC, Canada), a Manitoba Graduate Scholarship to QMRW, a Discovery Grant to RMB from NSERC, and field portions of the Fort Collins study were funded by a grant from the National Science Foundation Ecology of Infectious Diseases Program (#0094959).

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Authors and Affiliations

  1. Department of Biology and Centre for Forest Interdisciplinary Research (C-FIR), University of Winnipeg, Winnipeg, MB, Canada

    Quinn M. R. Webber, Andrew D. Park & Craig K. R. Willis

  2. Department of Biology, University of Regina, Regina, SK, Canada

    R. Mark Brigham

  3. Department of Biological Sciences, North Dakota State University, Fargo, ND, USA

    Erin H. Gillam

  4. US Geological Survey (retired), P.O. Box 65, Glen Haven, CO, 80532, USA

    Thomas J. O’Shea

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  1. Quinn M. R. Webber
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Correspondence to Quinn M. R. Webber.

Ethics declarations

All protocols applied in Cypress Hills were approved by the University of Regina President’s Committee on Animal Care and were in accordance with the Guidelines of the Canadian Council on Animal Care. All procedures involving bats in Fort Collins were approved by the Animal Care and Use Committee of Colorado State University and the US Geological Survey.

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Communicated by G. S. Wilkinson

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Fig. S1

Histograms of randomized mean half-weight index (A-D) and strength (E-H) for big brown bat roosting conditions compared to the observed mean half-weight index and strength for each roosting condition. Note the observed values (i.e., vertical red lines) fall outside 95 % quantiles (i.e., vertical dashed lines) of random distributions for both half-weight index and strength (PDF 760 kb)

Fig. S2

Histograms of randomized test statistics comparing half-weight index between roosting conditions. A) tree-roosting lactation vs. tree-roosting pregnant (p = 0.97); B) tree-roosting lactation vs. building-roosting pregnant (p = 0.001); C) tree-roosting lactation vs. building-roosting lactation (p = 0.002); D) tree-roosting pregnant vs. building-roosting pregnant (p = 0.001); E) tree-roosting pregnant vs. building-roosting lactation (p = 0.001); F) building-roosting pregnant vs. building-roosting lactation (p = 0.13). Vertical red lines represent observed test statistic and vertical dashed lines represent 95 % quantiles from the distribution of randomized test statistics (PDF 615 kb)

Fig. S3

Histograms of randomized test statistics comparing strength between roosting conditions. A) tree-roosting lactation vs. treeroosting pregnant (p = 0.32); B) tree-roosting lactation vs. building roosting pregnant (p = 0.22); C) tree-roosting lactation vs. building roosting lactation (p = 0.23); D) tree-roosting pregnant vs. building roosting pregnant (p = 0.001); E) tree-roosting pregnant vs. building roosting lactation (p = 0.001); F) building roosting pregnant vs. building roosting lactation (p = 0.23). Vertical red lines represent observed test statistic and vertical dashed lines represent 95 % quantiles from the distribution of randomized test statistics (PDF 590 kb)

Fig. S4

Network epidemic simulation of a hypothetical pathogen in a colony of big brown bats generated using an SI model over a 60-day time period. Dark lines represent mean proportion of bats infected across all models and grey shaded areas are 95 % confidence intervals. Note: β values are consistent across horizontal row of panels: A-B) β = 1 %; C-D) β = 10 %; and E-F) β = 25 % and roosting scenarios are consistent within each vertical column of panels: A,C,E) treeroosting bats; B,D,F) building-roosting bats (PDF 619 kb)

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Webber, Q.M.R., Brigham, R.M., Park, A.D. et al. Social network characteristics and predicted pathogen transmission in summer colonies of female big brown bats (Eptesicus fuscus). Behav Ecol Sociobiol 70, 701–712 (2016). https://doi.org/10.1007/s00265-016-2093-3

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