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      Keep calm and don’t stop growing: Non-consumptive effects of a sympatric predator on two invasive Ponto-Caspian gammarids Dikerogammarus villosus and Pontogammarus robustoides

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          Abstract

          Predators shape prey populations by elimination of individuals (consumptive effects) and by inducing modifications in prey behaviour, physiology or morphology (NCE—non-consumptive effects). Due to the resource allocation to defence, decreased feeding and higher stress, the costs of predator NCEs can be considerable. Therefore, the resistance to NCEs may be crucial for population growth and interspecific competition. We tested the resistance of Ponto-Caspian gammarids Dikerogammarus villosus and Pontogammarus robustoides to NCEs imposed by their predator, the racer goby Babka gymnotrachelus. As D. villosus is often avoided by predators in the presence of alternative food, we hypothesised that it would bear lower behavioural and physiological costs of anti-predator responses. We tested gammarid feeding in short-time experiments (2–4 h) with food (chironomid larvae) located at various distances from the stony shelter (to enforce food searching, Experiment I) or in the direct gammarid proximity (no searching needed, Experiment II). Moreover, we checked the predator effect on gammarid growth in a 2-week Experiment III. Both gammarids exposed to predators reduced feeding efficiency outside the shelter (Experiment I). Contrary to our expectations, the response of D. villosus was stronger. When food was provided in their direct proximity (Experiment II), the feeding of both species was unaffected by predators, indicating that a shelter supplied with food can reduce predator NCEs. The growth of P. robustoides was reduced in the presence of predators (Experiment III), whereas that of D. villosus was unaffected. Although D. villosus has a more effective defence strategy than P. robustoides, it bears similar or even higher behavioural costs of NCEs. However, it exhibits the higher resistance to the long-term predator presence, sustaining its growth rate under such conditions. This may be one of the factors contributing to the great invasion success of D. villosus, currently taking place in European fresh waters.

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          Most cited references58

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          SCARED TO DEATH? THE EFFECTS OF INTIMIDATION AND CONSUMPTION IN PREDATOR–PREY INTERACTIONS

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            Trophic cascades: the primacy of trait-mediated indirect interactions

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              Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions.

              Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – original draft
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: Validation
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 August 2017
                2017
                : 12
                : 8
                : e0182481
                Affiliations
                [001]Department of Invertebrate Zoology, Nicolaus Copernicus University, Toruń, Poland
                Consejo Superior de Investigaciones Cientificas, SPAIN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-9182-116X
                Article
                PONE-D-17-22687
                10.1371/journal.pone.0182481
                5542608
                28771578
                9adb85e4-aee1-4670-b426-80805795cd27
                © 2017 Jermacz, Kobak

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 20 June 2017
                : 19 July 2017
                Page count
                Figures: 5, Tables: 4, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: 2016/21/B/NZ8/00418
                Award Recipient :
                Our study was supported by the grant of the National Science Centre, Poland No. 2016/21/B/NZ8/00418.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Species Colonization
                Invasive Species
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Food Consumption
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Food Consumption
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Fishes
                Biology and Life Sciences
                Population Biology
                Population Dynamics
                Predator-Prey Dynamics
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Nutrition
                Diet
                Food
                Medicine and Health Sciences
                Nutrition
                Diet
                Food
                Biology and Life Sciences
                Species Interactions
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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