Small-scale indirect effects determine the outcome of a tripartite plant-disperser-granivore interaction.
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.
Boulay
Raphaël
R
Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas, Avenida Américo Vespucio s/n, 41092 Sevilla, Spain. boulay@ebd.csic.es
Carro
Francisco
F
Soriguer
Ramón C
RC
Cerdá
Xim
X
D000818:Animals; D001000:Ants / Q000502:physiology*; D017753:Ecosystem; D039322:Helleborus / Q000502:physiology*; D016014:Linear Models; D051189:Murinae / Q000502:physiology*; D012639:Seeds / Q000502:physiology*; D013030:Spain; D013559:Symbiosis