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.

Figure 1

Rate of carpel opening throughout the day at Cabra and Grazalema (model-adjusted means ±95% CI). Asterisk indicate significant differences between populations for a given time interval. The inserted graph shows the variation of temperature occurring during the time intervals.

Figure 2

Relation between ant dispersal effectiveness and proportion of diurnal activity during the period of maximum seed release at Grazalema (10.00–12.00, open symbols; fit: dash line) and Cabra (12.00–14.00, closed symbols; fit: solid line). The numbers refer to ant species as follows: 1, Aphaenogaster gibbosa; 2, Aphaenogaster senilis; 3, Camponotus cruentatus; 4, Camponotus lateralis; 5, Camponotus sylvaticus; 6, Cataglyphis rosenhaueri; 7, Cataglyphis velox; 8, Crematogaster auberti; 9, Crematogaster scutellaris; 10, Crematogaster sordidula; 11, Formica subrufa; 12, Messor structor; 13, Pheidole pallidula; 14, Plagiolepis pygmaea; 15, Stenamma orousetti; 16, Tapinoma nigerrimum; 17, Temnothorax spp.; 18, Tetramorium caespitum; 19, Tetramorium impurum.

Figure 3

Activity rhythm of four ant species at Cabra. Values are averages of 2004 and 2005. Aphaenogaster senilis and C. cruentatus are the two best dispersers while T. nigerrimum and C. sylvaticus are the two worst dispersers. The area in grey represents the period of maximum diaspore availability in this population.

Figure 4

Proportion of H. foetidus diaspores removed from the artificial depots in (a) 2004 and (b) 2005. Values are model-adjusted means ±95% CI. Different Roman letters denote significant differences between time intervals for depots accessible to ants and mice (solid line). Different Greek letters denote significant differences between time intervals for depots accessible to ants only (dash line). Stars denote significant differences between treatment for a given time interval and year (^*p<0.05; ^***p<0.001).