Abstract
Environmental and biological context play significant roles in modulating physiological stress responses of individuals in wildlife populations yet are often overlooked when evaluating consequences of human disturbance on individual health and fitness. Furthermore, most studies gauge individual stress responses based on a single physiological biomarker, typically circulating glucocorticoid concentrations, which limits interpretation of the complex, multifaceted responses of individuals to stressors. We selected four physiological biomarkers to capture short-term and prolonged stress responses in a widespread cave-roosting bat, Hipposideros diadema, across multiple gradients of human disturbance in and around caves in the Philippines. We used conditional inference trees and random forest analysis to determine the role of environmental quality (cave complexity, available roosting area), assemblage composition (intra- and interspecific associations and species richness), and intrinsic characteristics of individuals (sex and reproductive status) in modulating responses to disturbance. Direct cave disturbance (hunting pressure and human visitation) was the primary driver of neutrophil-to-lymphocyte ratios, with lower ratios associated with increased disturbance, while context-specific factors were more important in explaining total leukocyte count, body condition, and ectoparasite load. Moreover, conditional inference trees revealed complex interactions among human disturbance and modulating factors. Cave complexity often ameliorated individual responses to human disturbance, whereas conspecific abundance often compounded responses. Our study demonstrates the importance of an integrated approach that incorporates environmental and biological context when identifying drivers of physiological responses, and that assesses responses to gradients of direct and indirect disturbance using multiple complementary biomarkers.
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Acknowledgements
We thank the Department of Environment and Natural Resources of the Philippines for permission to conduct this study and Bohol Island State University for providing lodging and transportation during this project. We appreciate the undergraduate researchers at Bohol Island State University and Texas Tech University for help during fieldwork and analyzing blood smears, respectively, and Marina Fisher-Phelps for preparing our map. This study was funded by U.S. Department of State Fulbright Fellowship, Bat Conservation International, American Philosophical Society, The Explorers Club, American Society of Mammalogists, National Speleological Society, Cave Research Foundation, John Ball Zoo, Sigma Xi, Texas Tech Association of Biologists, and National Science Foundation (DEB Grant no. 1051363). We thank the two anonymous reviewers that provided useful comments that improved our manuscript.
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KLP and TK conceived and designed the study. KLP collected and analyzed the data. Both authors wrote the manuscript.
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Phelps, K.L., Kingston, T. Environmental and biological context modulates the physiological stress response of bats to human disturbance. Oecologia 188, 41–52 (2018). https://doi.org/10.1007/s00442-018-4179-2
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DOI: https://doi.org/10.1007/s00442-018-4179-2