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      Nectar in Plant–Insect Mutualistic Relationships: From Food Reward to Partner Manipulation

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          Abstract

          It has been known for centuries that floral and extra-floral nectar secreted by plants attracts and rewards animals. Extra-floral nectar is involved in so-called indirect defense by attracting animals (generally ants) that prey on herbivores, or by discouraging herbivores from feeding on the plant. Floral nectar is presented inside the flower close to the reproductive organs and rewards animals that perform pollination while visiting the flower. In both cases nectar is a source of carbon and nitrogen compounds that feed animals, the most abundant solutes being sugars and amino acids. Plant–animal relationships involving the two types of nectar have therefore been used for a long time as text-book examples of symmetric mutualism: services provided by animals to plants in exchange for food provided by plants to animals. Cheating (or deception or exploitation), namely obtaining the reward/service without returning any counterpart, is however, well-known in mutualistic relationships, since the interacting partners have conflicting interests and selection may favor cheating strategies. A more subtle way of exploiting mutualism was recently highlighted. It implies the evolution of strategies to maximize the benefits obtained by one partner while still providing the reward/service to the other partner. Several substances other than sugars and amino acids have been found in nectar and some affect the foraging behavior of insects and potentially increase the benefits to the plant. Such substances can be considered plant cues to exploit mutualism. Recent evidence motivated some authors to use the term “manipulation” of animals by plants in nectar-mediated mutualistic relationships. This review highlights the recent background of the “manipulation” hypothesis, discussing it in the framework of new ecological and evolutionary scenarios in plant–animal interactions, as a stimulus for future research.

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          Most cited references129

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          Optimal Foraging Theory: A Critical Review

          G Pyke (1984)
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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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              Pollinator Diversity: Distribution, Ecological Function, and Conservation

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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                19 July 2018
                2018
                : 9
                : 1063
                Affiliations
                [1] 1Department of Life Sciences, University of Siena , Siena, Italy
                [2] 2Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma , Parma, Italy
                [3] 3Department of Agrifood Production and Environmental Sciences, University of Florence , Florence, Italy
                Author notes

                Edited by: Lukasz Lech Stelinski, University of Florida, United States

                Reviewed by: Martin Heil, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Mexico; Quint Rusman, Wageningen University & Research (WUR), Netherlands

                *Correspondence: Massimo Nepi, massimo.nepi@ 123456unisi.it

                This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.01063
                6060274
                30073014
                3af7e283-0536-47b2-b6bf-6e64b2d504bc
                Copyright © 2018 Nepi, Grasso and Mancuso.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 28 March 2018
                : 29 June 2018
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 147, Pages: 14, Words: 0
                Categories
                Plant Science
                Review

                Plant science & Botany
                nectar,partner manipulation,secondary compounds,mutualistic relationships,exploitation,plant–animal interactions

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