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Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels

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Abstract

Non-consumptive effects (NCEs) of predators are ubiquitous in food webs with well-detailed impacts on trophic cascades over multiple levels. However, integrating NCEs with other predator–mediated interactions, like intraguild predation, as well as context-specific habitat factors that shape top–down pressure, remains a challenge. Focusing on two common seed predators, mice (Peromyscus spp.) and carabid beetles (Coleoptera: Carabidae), we quantify trophic and behavioral consequences of predation risk and availability of refuge vegetation on both intraguild predators (mice) and intraguild prey (beetles). In a 2-year field experiment, we manipulated refuge habitat (red clover), small mammal access, and moonlight, which small mammals use as an indirect cue of predation risk. We found that avoidance of predation risk by mice in simulated moonlight reduced carabid activity density in vegetation by up to 50% compared to exposed habitat, but had no cascading effects on seed predation. We linked patterns observed in the field with behavioral mechanisms by observing beetle foraging activity, and found that exposure to both indirect and direct vertebrate predator cues reduced movement by 50%, consistent with predator–mediated activity reductions observed in the field. However, predation risk increased carabid seed consumption by 43%. Thus, weak effects of predation risk on seed removal in the field may be explained by overcompensatory seed feeding by beetles. This work demonstrates that predators elicit responses that cascade over multiple trophic levels, triggering behavioral changes in species lower on the food chain. These behavior-mediated cascades are controlled by their spatiotemporal context and have important downstream impacts on predator–prey dynamics.

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Acknowledgements

This material is based upon work that is supported by the National Institute of Food and Agriculture, US Department of Agriculture, under Award No. 10-51300-21305, and by NSF Award No. 1401795. We are grateful to Curt Hardin, Gareth Powell, and Christie Shee, for assistance with data collection, and several Kaplan lab members for helpful feedback on previous drafts of this manuscript. Rob Swihart, Patrick Zollner, and John Orrock offered advice on methods, and Ken Kellner helped with analysis. Jamin Dreyer, Elinor Lichtenberg, Jim Cronin and several anonymous reviewers provided valuable comments that shaped the final version of this paper.

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CKB and IK conceived and designed the experiment; CKB and IVW conducted fieldwork; CKB and IVW analyzed the data. CKB, IVW, and IK wrote the manuscript.

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Correspondence to Carmen K. Blubaugh.

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All applicable institutional and/or national guidelines for the care and use of animals were followed.

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Communicated by Jennifer Thaler.

While most studies examine trophic consequences of predation risk, we show that anti-predator behavior may in turn trigger another series of predator avoidance responses at lower trophic levels, or ‘fear cascades’ mediated by refuge and resource availability. This discovery is important because it emphasizes the central importance of spatiotemporal context for understanding predator–prey interactions; these should be examined explicitly in future work.

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Supplemental Figure 1 Photo of a main plot at the field site (TIFF 1910 kb)

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Blubaugh, C.K., Widick, I.V. & Kaplan, I. Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels. Oecologia 185, 1–11 (2017). https://doi.org/10.1007/s00442-017-3909-1

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