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      Dietary specialization is conditionally associated with increased ant predation risk in a temperate forest caterpillar community

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          Abstract

          The enemy‐free space hypothesis (EFSH) contends that generalist predators select for dietary specialization in insect herbivores. At a community level, the EFSH predicts that dietary specialization reduces predation risk, and this pattern has been found in several studies addressing the impact of individual predator taxa or guilds. However, predation at a community level is also subject to combinatorial effects of multiple‐predator types, raising the question of how so‐called multiple‐predator effects relate to dietary specialization in insect herbivores. Here, we test the EFSH with a field experiment quantifying ant predation risk to insect herbivores (caterpillars) with and without the combined predation effects of birds. Assessing a community of 20 caterpillar species, we use model selection in a phylogenetic comparative framework to identify the caterpillar traits that best predict the risk of ant predation. A caterpillar species' abundance, dietary specialization, and behavioral defenses were important predictors of its ant predation risk. Abundant caterpillar species had increased risk of ant predation irrespective of bird predation. Caterpillar species with broad diet breadth and behavioral responsiveness to attack had reduced ant predation risk, but these ant effects only occurred when birds also had access to the caterpillar community. These findings suggest that ant predation of caterpillar species is density‐ or frequency‐dependent, that ants and birds may impose countervailing selection on dietary specialization within the same herbivore community, and that contingent effects of multiple predators may generate behaviorally mediated life‐history trade‐offs associated with herbivore diet breadth.

          Abstract

          This study is an experimental test of the hypothesis that dietary specialization of insect herbivores reduces their predation risk. Unexpectedly, ant predation of caterpillars increased with dietary specialization and depended on bird predation. In this community, dietary specialization was associated with reduced behavioral defenses, which predicted ant predation risk in a way that was also contingent upon bird predation.

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          Most cited references39

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

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            The global distribution of diet breadth in insect herbivores.

            Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.
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              Darwin's abominable mystery: Insights from a supertree of the angiosperms.

              Angiosperms are among the major terrestrial radiations of life and a model group for studying patterns and processes of diversification. As a tool for future comparative studies, we compiled a supertree of angiosperm families from published phylogenetic studies. Sequence data from the plastid rbcL gene were used to estimate relative timing of branching events, calibrated by using robust fossil dates. The frequency of shifts in diversification rate is largely constant among time windows but with an apparent increase in diversification rates within the more recent time frames. Analyses of species numbers among families revealed that diversification rate is a labile attribute of lineages at all levels of the tree. An examination of the top 10 major shifts in diversification rates indicates they cannot easily be attributed to the action of a few key innovations but instead are consistent with a more complex process of diversification, reflecting the interactive effects of biological traits and the environment.
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                Author and article information

                Contributors
                msinger@wesleyan.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                11 October 2019
                November 2019
                : 9
                : 21 ( doiID: 10.1002/ece3.v9.21 )
                : 12099-12112
                Affiliations
                [ 1 ] Department of Biology Wesleyan University Middletown CT USA
                [ 2 ] Department of Ecology and Evolutionary Biology University of California at Irvine Irvine CA USA
                [ 3 ] Department of Biological Sciences University of New Mexico Albuquerque NM USA
                Author notes
                [*] [* ] Correspondence

                Michael S. Singer, Department of Biology, Wesleyan University, Middletown, CT, USA.

                Email: msinger@ 123456wesleyan.edu

                Author information
                https://orcid.org/0000-0002-0164-3767
                Article
                ECE35662
                10.1002/ece3.5662
                6854387
                31844517
                2b01d83e-b9d4-42df-9e22-c03ee3daad5c
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 04 October 2018
                : 15 July 2019
                : 27 August 2019
                Page count
                Figures: 2, Tables: 4, Pages: 14, Words: 11478
                Funding
                Funded by: NSF
                Award ID: DEB 1257965
                Award ID: DEB 1354734
                Award ID: DEB 1457029
                Award ID: DEB 1557086
                Funded by: Wesleyan University
                Funded by: Howard Hughes Medical Institute , open-funder-registry 10.13039/100000011;
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                November 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.2 mode:remove_FC converted:05.12.2019

                Evolutionary Biology
                antipredator defense,enemy‐free space,host specificity,insect herbivores,polyphagy,tritrophic interactions

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