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      Gall-Colonizing Ants and Their Role as Plant Defenders: From ’Bad Job’ to ’Useful Service’

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          Abstract

          Galls are neoformed structures on host plant tissues caused by the attack of insects or other organisms. They support different communities of specialized parasitic insects (the gall inducers), and can also provide refuge to other insects, such as moths, beetles and ants, referred to as secondary occupants. This study focuses on galls induced by the oak gall wasp Andricus quercustozae and secondarily colonized by ants in a mixed oak forest. A field survey and two experiments were carried out to a) study ant (species-specific) preferences for different features of the galls, b) describe differences in gall architecture due to ant activity, c) analyse the effects of the presence of gall-dwelling ants on plant health. The results show that there are differences between ant species in gall colonization and in the alteration of gall opening and inner structure. We verified that gall-dwelling ants protect their host plants efficiently, offering them an indirect defence mechanism against enemies (predators and pathogens). The data suggest a new paradigm in ant–plant relationships mediated by the presence of galls on the plants whose ecological and evolutionary implications are discussed.

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          Indirect defence via tritrophic interactions.

          Many plants interact with carnivores as an indirect defence against herbivores. The release of volatile organic compounds (VOCs) and the secretion of extrafloral nectar (EFN) are induced by insect feeding, a response that is mediated by the plant hormone, jasmonic acid. Although VOCs mainly attract predatory mites and parasitic wasps, while EFN mainly attracts ants, many more animal-plant interactions are influenced by these two traits. Other traits involved in defensive tritrophic interactions are cellular food bodies and domatia, which serve the nutrition and housing of predators. They are not known to respond to herbivory, while food body production can be induced by the presence of the mutualists. Interactions among the different defensive traits, and between them and other biotic and abiotic factors exist on the genetic, physiological, and ecological levels, but so far remain understudied. Indirect defences are increasingly being discussed as an environmentally-friendly crop protection strategy, but much more knowledge on their fitness effects under certain environmental conditions is required before we can understand their ecological and evolutionary relevance, and before tritrophic interactions can serve as a reliable tool in agronomy.
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            Protective Ant-Plant Interactions as Model Systems in Ecological and Evolutionary Research

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              The population biology of oak gall wasps (Hymenoptera: Cynipidae).

              Oak gall wasps (Hymenoptera: Cynipidae, Cynipini) are characterized by possession of complex cyclically parthenogenetic life cycles and the ability to induce a wide diversity of highly complex species- and generation-specific galls on oaks and other Fagaceae. The galls support species-rich, closed communities of inquilines and parasitoids that have become a model system in community ecology. We review recent advances in the ecology of oak cynipids, with particular emphasis on life cycle characteristics and the dynamics of the interactions between host plants, gall wasps, and natural enemies. We assess the importance of gall traits in structuring oak cynipid communities and summarize the evidence for bottom-up and top-down effects across trophic levels. We identify major unanswered questions and suggest approaches for the future.
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                Author and article information

                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                06 November 2019
                November 2019
                : 10
                : 11
                : 392
                Affiliations
                Department of Chemistry, Life Sciences & Environmental Sustainability, University of Parma, 43124 Parma, Italy fiorenzaaugusta.spotti@ 123456unipr.it (F.A.S.); alessandra.mori@ 123456unipr.it (A.M.); donato.grasso@ 123456unipr.it (D.A.G.)
                Author notes
                [†]

                These authors contributed equally.

                Author information
                https://orcid.org/0000-0003-1622-1329
                https://orcid.org/0000-0001-8802-9614
                https://orcid.org/0000-0002-4270-7229
                Article
                insects-10-00392
                10.3390/insects10110392
                6920797
                31698832
                d3d7f64f-eb84-4ab5-9988-b6acf955bac6
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 18 October 2019
                : 05 November 2019
                Categories
                Article

                ant–plant interactions,mutualism,oak-gall secondary fauna,nest architecture,indirect plant defence

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