Synchrony between fruit maturation and effective dispersers' foraging activity increases seed protection against seed predators

Abstract

The evolution of pollination and seed dispersal mutualisms is conditioned by the spatial and temporal co-occurrence of animals and plants. In the present study we explore the timing of seed release of a myrmecochorous plant (Helleborus foetidus) and ant activity in two populations in southern Spain during 2 consecutive years. The results indicate that fruit dehiscence and seed shedding occur mostly in the morning and correspond to the period of maximum foraging activity of the most effective ant dispersers. By contrast, ant species that do not transport seeds and/or that do not abound near the plants are active either before or after H. foetidus diaspores are released. Experimental analysis of diet preference for three kinds of food shows that effective ant dispersers are mostly scavengers that readily feed on insect corpses and sugars. Artificial seed depots suggest that seeds deposited on the ground out of the natural daily time window of diaspore releasing are not removed by ants and suffer strong predation by nocturnal rodents Apodemus sylvaticus. Nevertheless, important inter-annual variations in rodent populations cast doubts on their real importance as selection agents. We argue that traits allowing synchrony between seed presentation and effective partners may constitute a crucial pre-adaptation for the evolution of plant-animal mutualisms involving numerous animal partners.

Dispersal of non-myrmecochorous plants by a “keystone disperser” ant in a Mediterranean habitat reveals asymmetric interdependence

“…First, as suggested by Boulay et al (2007a), Aphaenogaster are generally subordinate species that are very quick to discover food items. Conversely, these ants are not efficient at defending food against small, mass recruiting dominant species like Tetramorium forte or Tapinoma nigerrimum.…”

“…After it has been consumed mostly by the larvae (Fischer et al, 2005), the ants discard the intact seed with other food remains. By transporting the vulnerable seeds soon after their release, ants allow plants to colonize new habitats (Gorb and Gorb, 2003), reduce intraspecific competition and decrease mortality by predation and fire (Heithaus, 1981;Bond and Slingsby, 1984;Hughes and Westoby, 1992;Boulay et al, 2007aBoulay et al, , 2009a. However, ant seed dispersal benefits may differ greatly between species (Giladi, 2006).…”

“…We examined non-myrmecochorous seed use and dispersal by ants in a southern Spain shrub habitat as a model system for testing our hypotheses. The ant Aphaenogaster senilis is a keystone disperser of myrmecochores in Mediterranean habitats across the Iberian Peninsula (Boulay et al, 2007a;2009a;Espadaler and Gómez, 1997). We assessed the interdependence between A. senilis and the diaspores of the most abundant non-myrmecochorous plants in our study habitat by estimating both the proportion and number of fruits and seeds in their diet.…”

“…Third, animals can have contrasting qualitative and quantitative effects on seeds including dispersal, predation and exploitative parasitism (i.e. cheating; Horvitz and Schemske, 1986;Bronstein, 1994;Boulay et al, 2007a).…”

Ecological differentiation among key plant mutualists from a cryptic ant guild

“…Indeed, the timing of propagule release may correspond with peak foraging in certain seed-dispersing ant genera and these genera appear far more effective as seed dispersers than other seed-gathering ants (Giladi, 2006;Boulay et al, 2007;Gove et al, 2007;Zelikova et al, 2008;Bas et al, 2009;Manzaneda and Rey, 2009;Ness et al, 2009). In eastern deciduous forests (USA), members of the ant genus Aphaenogaster dominate these mutualist interactions (Ness et al, 2009).…”