Warming can alter host behavior in a similar manner to infection with behavior-manipulating parasites

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BEHAVIORAL ECOLOGY –ORIGINAL RESEARCH

Warming can alter host behavior in a similar manner to infection with behavior‑manipulating parasites Maureen A. Williams1,2   · Celia V. Holland1   · Ian Donohue1  Received: 17 January 2020 / Accepted: 26 August 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Parasites are ecologically ubiquitous and, by modifying the physiology and behavior of their host organisms, act as key regulators of the dynamics and stability of ecosystems. It is, however, as yet unclear how parasitic relationships will act to moderate or accelerate the ecological impacts of global climate change. Here, we explore experimentally how the effects of parasites on both the physiology and behavior of their hosts can be moderated by warming, utilising a well-established aquatic host-parasite model system—the ecologically important amphipod Gammarus duebeni and its acanthocephalan parasite Polymorphus minutus. We show that, while only warming affected measured components of host physiology, parasite infection and warming both supressed predator-avoidance behavior of the host independently, yet in a similar manner. Six degrees of warming altered geotactic behaviors to the same extent as infection with behavior-manipulating parasites. These results indicate a novel mechanism by which parasites impact their ecosystems that could be critical to predicting the ecological impacts of warming. Our findings highlight the need for holistic knowledge of interaction networks, incorporating multiple interaction types and behaviors, to predict the effects of both warming and parasitism on the dynamics and stability of ecosystems. Keywords  Acanthocephala · Behaviour · Gammarus · Host-parasite interactions · Warming

Introduction As climate change accelerates (IPCC 2014), the importance of warming and its effects on ecosystems around the globe will continue to grow. While the direct effects of warming have been quantified for many species (Wernberg et al. 2012), relatively little is known about its indirect effects, mediated by interspecific interactions (Shaver et al. 2000; Post and Pedersen 2008; White et al. 2018). Though the nature and magnitude of these effects are considerably more Communicated by Pieter Johnson. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0044​2-020-04745​-2) contains supplementary material, which is available to authorized users. * Maureen A. Williams [email protected] 1



Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin Dublin 2, Ireland



School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, USA

2

difficult to predict (Sanford 1999; Wernberg et al. 2012), they can be at least as important as direct effects in determining the overall impacts of warming on ecosystems (Chapin 1983; Dell et al. 2014; Donohue et al. 2017; Kordas et al. 2017). However, the complexity of ecological networks can lead to significant uncertainty in predictions, where small changes i