Bird Rejection of Unhealthy Fruits Reinforces the Mutualism between Juniper and Its Avian Dispersers

Abstract

We investigated fruit damage by insects as well as fruit abortion in relation to the mutualism between Juniperus communis, a fleshy-fruited plant dominant in the high mountains of southeastern Spain, and its bird disperser assemblage. For two years. we performed field experiments to analyse fruit selection by birds, offering birds different types of anomalous fruits (unripe, aborted, pulp-sucker infested and seed-predator attacked) and comparing the removal rate to that of ripe, healthy, control fruits. In addition, we studied the proportion of fruits attacked by the seed predator in samples of fruits which, after manipulation and rejection by birds, we found lying underneath plants. We compared these data to values in samples of fruits which we took directly from plants. Finally, over four years, the abundance of predispersaldepredated seeds in the seed rain dispersed by birds was compared with the abundance in seeds taken directly from plants. Fruit-choice experiments showed that unripe, aborted and fruits attacked by pest insects (both pulp sucker and seed predator) were strongly counterselected by these frugivorous birds. The proportion of fruits attacked by seed-predator in the sample of fruits manipulated and rejected was significantly higher than in the fruits taken from plants. For all study years, the proportion of depredated seeds was significantly lower in the sample of seeds dispersed by birds than in the sample of seeds taken from plants. Bird response to pests was not categorically to accept or reject fruit, but rather was influenced by pest density. Birds showed two different levels of fruit selection, depending on the type of fruit: visual discrimination, against fruits that are unripe, aborted and infested by the pulp sucker: and within-beak discrimination, against fruits attacked by the seed predator. In the study, both pests either died or left the fruit when ripe, and therefore frugivorous birds did not interfere directly with frugivorous insects. On the contrary, insects did interfere indirectly with birds, promoting the rejection of pest-attacked fruits by birds. Bird dispersers overcame the predispersal interference of pest fruit damage and fruit abortion and increased the proportion of healthy seeds in the seed rain. This fact, together with the great quantity of seeds dispersed by birds, reinforces the importance of birds as plant mutualists.