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      Fear of predators in free-living wildlife reduces population growth over generations

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          Significance

          Accurately evaluating the total impact of predators on prey population growth rates is fundamental to forecasting the consequences of predator conservation and management. That the fear (antipredator responses) predators inspire could contribute to this total impact has only relatively recently been recognized. We experimentally demonstrate that fear itself can impact prey population growth rates in free-living wildlife, extending to transgenerational impacts reducing population growth beyond the parental generation. We report how fear may contribute considerably to the total impact of predators and why this may be the norm in birds and mammals. The critical significance of our work lies in experimentally establishing that inferring the effects of predators using data on direct killing alone risks dramatically underestimating their total impact.

          Abstract

          Correctly assessing the total impact of predators on prey population growth rates (lambda, λ) is critical to comprehending the importance of predators in species conservation and wildlife management. Experiments over the past decade have demonstrated that the fear (antipredator responses) predators inspire can affect prey fecundity and early offspring survival in free-living wildlife, but recent reviews have highlighted the absence of evidence experimentally linking such effects to significant impacts on prey population growth. We experimentally manipulated fear in free-living wild songbird populations over three annual breeding seasons by intermittently broadcasting playbacks of either predator or nonpredator vocalizations and comprehensively quantified the effects on all the components of population growth, together with evidence of a transgenerational impact on offspring survival as adults. Fear itself significantly reduced the population growth rate (predator playback mean λ = 0.91, 95% CI = 0.80 to 1.04; nonpredator mean λ = 1.06, 95% CI = 0.96 to 1.16) by causing cumulative, compounding adverse effects on fecundity and every component of offspring survival, resulting in predator playback parents producing 53% fewer recruits to the adult breeding population. Fear itself was consequently projected to halve the population size in just 5 years, or just 4 years when the evidence of a transgenerational impact was additionally considered (λ = 0.85). Our results not only demonstrate that fear itself can significantly impact prey population growth rates in free-living wildlife, comparing them with those from hundreds of predator manipulation experiments indicates that fear may constitute a very considerable part of the total impact of predators.

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          Most cited references54

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          Status and ecological effects of the world's largest carnivores.

          Large carnivores face serious threats and are experiencing massive declines in their populations and geographic ranges around the world. We highlight how these threats have affected the conservation status and ecological functioning of the 31 largest mammalian carnivores on Earth. Consistent with theory, empirical studies increasingly show that large carnivores have substantial effects on the structure and function of diverse ecosystems. Significant cascading trophic interactions, mediated by their prey or sympatric mesopredators, arise when some of these carnivores are extirpated from or repatriated to ecosystems. Unexpected effects of trophic cascades on various taxa and processes include changes to bird, mammal, invertebrate, and herpetofauna abundance or richness; subsidies to scavengers; altered disease dynamics; carbon sequestration; modified stream morphology; and crop damage. Promoting tolerance and coexistence with large carnivores is a crucial societal challenge that will ultimately determine the fate of Earth's largest carnivores and all that depends upon them, including humans.
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            Trophic downgrading of planet Earth.

            Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. The loss of these animals may be humankind's most pervasive influence on nature. Although such losses are widely viewed as an ethical and aesthetic problem, recent research reveals extensive cascading effects of their disappearance in marine, terrestrial, and freshwater ecosystems worldwide. This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles. These findings emphasize the urgent need for interdisciplinary research to forecast the effects of trophic downgrading on process, function, and resilience in global ecosystems.
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              Nonlethal Effects in the Ecology of Predator-Prey Interactions

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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                7 February 2022
                15 February 2022
                7 February 2022
                : 119
                : 7
                : e2112404119
                Affiliations
                [1] aDepartment of Biology, Western University , London, ON N6A 5B7, Canada
                Author notes
                1To whom correspondence may be addressed. Email: lzanette@ 123456uwo.ca .

                Edited by John Terborgh, Biology, University of Florida, Cedar Key, FL; received July 7, 2021; accepted December 13, 2021

                Author contributions: M.C.A., M.C., and L.Y.Z. designed research; M.C.A., M.C., and L.Y.Z. performed research; M.C.A. and L.Y.Z. analyzed data; and M.C. and L.Y.Z. wrote the paper.

                Author information
                https://orcid.org/0000-0001-9396-8704
                https://orcid.org/0000-0003-4691-3879
                https://orcid.org/0000-0003-2574-3452
                Article
                202112404
                10.1073/pnas.2112404119
                8851447
                35131939
                c786c7db-c8ec-4996-b129-b8436621d75d
                Copyright © 2022 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 13 December 2021
                Page count
                Pages: 6
                Funding
                Funded by: Animal Behavior Society (ABS) 100009702
                Award ID: Recipient''''s Name: Marek Charles Allen
                Award Recipient : Marek Charles Allen
                Funded by: American Museum of Natural History (AMNH) 100005835
                Award ID: Recipient''''s Name: Marek Charles Allen
                Award Recipient : Marek Charles Allen
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: Recipient''''s Name: Michael Clinchy
                Award Recipient : Michael Clinchy Award Recipient : Liana Yvonne Zanette
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: Recipient''''s Name: Liana Yvonne Zanette
                Award Recipient : Michael Clinchy Award Recipient : Liana Yvonne Zanette
                Categories
                414
                Biological Sciences
                Ecology
                From the Cover

                ecology of fear,perceived predation risk,population growth rate,predator–prey interactions,antipredator behavior

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