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      Does Plant Origin Influence the Fitness Impact of Flower Damage? A Meta-Analysis

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          Abstract

          Herbivory has been long considered an important component of plant-animal interactions that influences the success of invasive species in novel habitats. One of the most important hypotheses linking herbivory and invasion processes is the enemy-release hypothesis, in which exotic plants are hypothesized to suffer less herbivory and fitness-costs in their novel ranges as they leave behind their enemies in the original range. Most evidence, however, comes from studies on leaf herbivory, and the importance of flower herbivory for the invasion process remains largely unknown. Here we present the results of a meta-analysis of the impact of flower herbivory on plant reproductive success, using as moderators the type of damage caused by floral herbivores and the residence status of the plant species. We found 51 papers that fulfilled our criteria. We also included 60 records from unpublished data of the laboratory, gathering a total of 143 case studies. The effects of florivory and nectar robbing were both negative on plant fitness. The methodology employed in studies of flower herbivory influenced substantially the outcome of flower damage. Experiments using natural herbivory imposed a higher fitness cost than simulated herbivory, such as clipping and petal removal, indicating that studies using artificial herbivory as surrogates of natural herbivory underestimate the real fitness impact of flower herbivory. Although the fitness cost of floral herbivory was high both in native and exotic plant species, floral herbivores had a three-fold stronger fitness impact on exotic than native plants, contravening a critical element of the enemy-release hypothesis. Our results suggest a critical but largely unrecognized role of floral herbivores in preventing the spread of introduced species into newly colonized areas.

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          Most cited references12

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          Florivory: the intersection of pollination and herbivory.

          Plants interact with many visitors who consume a variety of plant tissues. While the consequences of herbivory to leaves and shoots are well known, the implications of florivory, the consumption of flowers prior to seed coat formation, have received less attention. Herbivory and florivory can yield different plant, population and community outcomes; thus, it is critical to distinguish between these two types of consumption. Here, we consider the ecological and evolutionary consequences of florivory. A growing number of studies recognize that florivory is common in natural systems and in some cases surpasses leaf herbivory in magnitude and impact. Florivores can affect male and female plant fitness via direct trophic effects and through altered pathways of species interactions. In particular, florivory can affect pollination and have consequences for plant mating and floral sexual system evolution. Plants are not defenceless against florivore damage. Concepts of resistance and tolerance can be applied to plant-florivore interactions. Moreover, extant theories of plant chemical defence, including optimal defence theory, growth rate hypothesis and growth differentiation-balance hypothesis, can be used to make testable predictions about when and how plants should defend flowers against florivores. The majority of the predictions remain untested, but they provide a theoretical foundation on which to base future experiments. The approaches to studying florivory that we outline may yield novel insights into floral and defence traits not illuminated by studies of pollination or herbivory alone.
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            The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance.

            An explanation for successful invasion is that invasive alien species sustain less pressure from natural enemies than co-occurring native species. Using meta-analysis, we examined whether invasive species: (1) incur less damage, (2) exhibit better performance in the presence of enemies, and (3) tolerate damage more than native species. Invasive alien species did not incur less damage than native species overall. The performance of invasive alien species was reduced compared to natives in the presence of enemies, indicating the invasive alien species were less tolerant to damage than native species. However, there was no overall difference in performance of invasive alien and native species with enemies present. The damage and degree of reduction in performance of invasive alien relative to native species did not depend on relatedness to natives. Our results suggest aliens may not always experience enemy release, and enemy release may not always result in greater plant performance.
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              Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators.

              This paper examines the hypothesis that nectar robbing can affect plant reproductive success either positively or negatively. To this end, I investigated various aspects of the pollination ecology of a population of the herb Anthyllis vulneraria subsp. vulgaris in northwest Spain over 5 yr. By observing floral visitors, I found that the most important pollinator species was the long-tongued bee Anthophora acervorum, which accounted for ∼45% of recorded insect visits. However, just over 45% of visits were by the nectar-robbing bumble bees Bombus terrestris and B. jonellus. Although the incidence of robbing differed considerably over 5 yr of study, the frequency in every season was very high (66.4-76.5% of robbing) except for 1997 (0% robbing). Despite this high frequency of robbing, robbed flowers had a higher probability of setting fruit than nonrobbed flowers in all years of the study (mean: 82.0 vs. 51.0%; excluding 1997). This increased fruit set in robbed flowers is directly related to bumble bee behavior because the robbers' bodies came into contact with both the anthers and stigmas while robbing. Thus, the robbers effect pollination. These results suggest that the effect of nectar robbers on plant reproductive success is dependent both on the robbers' behavior and on flower/inflorescence structure. The importance of nectar-robbing bumble bees on the reproductive success of A. vulneraria and its yearly high frequency suggest that the relationship between robbers and this plant is part of a successful long-term mutualism.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 January 2016
                2016
                : 11
                : 1
                : e0146437
                Affiliations
                [1 ]Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Santiago, Chile
                [2 ]Departamento de Biología Vegetal, Universidad de Vigo, Campus Lagoas-Marcosende, 36200, Vigo, Spain
                Helmholtz Centre for Environmental Research - UFZ, GERMANY
                Author notes

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

                Conceived and designed the experiments: CG MMM LN RM. Performed the experiments: CG MMM LN RM. Analyzed the data: CG MMM LN RM. Contributed reagents/materials/analysis tools: CG MMM LN RM. Wrote the paper: CG MMM LN RM.

                Article
                PONE-D-14-18822
                10.1371/journal.pone.0146437
                4718695
                26785039
                88495f6f-fe6f-4603-b05f-c26aea2f270b
                © 2016 González-Browne et al

                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
                : 26 April 2014
                : 17 December 2015
                Page count
                Figures: 3, Tables: 1, Pages: 17
                Funding
                This research was supported by Fondo Nacional de Ciencia y Tecnologia, Grants 1120155 and 1150112, to RM ( http://www.fondecyt.cl). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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