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Small-scale indirect effects determine the outcome of a tripartite plant–disperser–granivore interaction

  • Plant–Animal Interactions - Original Paper
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Abstract

The microhabitat in which plants grow affects the outcome of their interactions with animals, particularly non-specialist consumers. Nevertheless, as most research on this topic has dealt with either mutualists or antagonists, little is known about the indirect effects of plant microhabitats on the outcome of tripartite interactions involving plants and both mutualists (e.g. seed dispersers) and antagonists (e.g. granivores). During three consecutive years, we analysed small-scale variations in the interaction of a perennial myrmecochore, Helleborus foetidus, with its seed dispersers and consumers as a function of the intensity of plant cover. Most seeds were released during the day and were rapidly removed by ants. Nevertheless, the proportion of ant-removed seeds was higher for plants located in open microhabitats than for plants surrounded by dense vegetation and rocky cover. Ant sampling revealed that seed removers were equally abundant, irrespective of the level of cover. By contrast, a few tiny ant species that feed on the reward without transporting the seeds were more abundant in highly covered microhabitats, irrespective of hellebore diaspore availability. These “cheaters” decrease the chance of removal by removers and increase the probability of seeds remaining on the ground until night, when granivore mice Apodemus sylvaticus become active. Mice also preferred foraging in covered microhabitats, where they consumed a larger proportion of seeds. Therefore, the density of cover indirectly increased seed predation risk by attracting more seed predators and cheater ants that contribute to increase seed availability for seed predators. Our results emphasize the importance of considering the indirect effects of plant microhabitat on their dispersal success. They highlight the indirect effect of cheaters that are likely to interfere in mutualisms and may lead to their collapse unless external factors such as spatio-temporal heterogeneity in seed availability constrain their effect.

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Acknowledgments

This work was funded by the Spanish “Ministerio de Educación y Ciencia” (project BOS2003-01536 and CGL2006-04968/BOS to X.C. and R.B.). It was conducted with the authorization of Parque Natural de la Sierra de Grazalema and Parque Natural de las Sierras Subbéticas. Accommodation at Cabra was kindly provided by the Camacho family and at Grazalema by the authority of the park. Assistance in the field was provided by E. Angulo, A. Carvajal, I. Luque, O. González, E. García Márquez, I. Villalta and M. Vonshak. We also thank J. Minett for editing assistance and Drs J. Cronin and T. Payne for constructive comments on a previous version of the manuscript. R.B. was funded by an I3P fellowship. This work complies with current Spanish laws.

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Authors and Affiliations

  1. Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Avenida Américo Vespucio s/n, 41092, Sevilla, Spain

    Raphaël Boulay, Francisco Carro, Ramón C. Soriguer & Xim Cerdá

  2. Departamento de Biologia Animal, Universidad de Granada, Avenida Severo Ochoa s/n, 18071, Granada, Spain

    Raphaël Boulay

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  1. Raphaël Boulay
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  2. Francisco Carro
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  3. Ramón C. Soriguer
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  4. Xim Cerdá
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Correspondence to Raphaël Boulay.

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Communicated by Florian Schiestl.

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Boulay, R., Carro, F., Soriguer, R.C. et al. Small-scale indirect effects determine the outcome of a tripartite plant–disperser–granivore interaction. Oecologia 161, 529–537 (2009). https://doi.org/10.1007/s00442-009-1404-z

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