Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees

Abstract

The responses of plant–animal interactions to forest fragmentation can vary. We hypothesized that large-seeded plant species would be more susceptible to forest fragmentation than small-seeded species because large-seeded species rely on a few, extinction prone dispersers. We compared seed dispersal of the large-seeded, mammal dispersed Duckeodendron cestroides and the small-seeded, avian dispersed Bocageopsis multiflora. The number, percentage, distance, and distributions of dispersed seeds were all reduced in fragments for Duckeodendron but not for Bocageopsis. Other fragmentation research in tropical communities supports this hypothesis through three lines of evidence: (1) Large-seeded plant species are more prone to extinction, (2) Fragmentation restricts or alters the movement of large animal dispersers more than small dispersers, and (3) Large and small-seeded species seem to be differentially linked to primary and secondary forest habitats. Therefore, small-seeded plants may be more resilient to forest fragmentation while large-seeded species may be more susceptible and should be a priority for conservation.

Introduction

Responses of mutualisms to forest fragmentation can be very diverse. Declines in animal or plant species can result in the loss of mutualistic functions, jeopardizing connected species (Andresen and Levey, 2004, Bruna et al., 2005). Alternatively, some mutualisms are more resilient to fragmentation because the behavior of animal mutualists is not altered, lost mutualists are replaced by other species (Dick, 2001), or lost mutualistic functions are replaced by the plant itself through self-fertilization (Powell and Powell, 1987). Given the diversity of individual responses to fragmentation, are there generalizations that allow us to predict the effects of forest fragmentation for some tropical rainforest trees?

It has been hypothesized that populations of large-seeded plants will be highly susceptible to fragmentation (Fortuna and Bascompte, 2006, Jones and Crome, 1990, Kitamura et al., 2004, Melo et al., 2006, Silva and Tabarelli, 2000, Tabarelli and Peres, 2002). In contrast, small seeded plants may sustain viable populations in or across forest fragments (Silva and Tabarelli, 2000, Tabarelli and Peres, 2002). Seed dispersal of large and small-seeded tree species may be differentially affected by forest fragmentation because their dispersers have varying responses to fragmentation for several reasons. First, large-seeded species rely on fewer animal species for dispersal (Christian, 2001, Hamann and Curio, 1999). Second, dispersal agents of large-seeded species are often larger and therefore at greater risk of extirpation in fragments, given greater hunting pressures, their low reproductive rates, and small populations (Bodmer et al., 1997, Gilbert and Setz, 2001, Hamann and Curio, 1999, Willis, 1979). In addition, large-animals cannot subsist even in large fragments (100-ha) because their home ranges are too extensive (Chapman, 1989, Woodroffe and Ginsberg, 1998). After forest fragmentation, the loss of the few dispersal agents available for large-seeded plants can effectively eliminate all seed dispersal. On the other hand, small-seeded fruits can be dispersed by many species of frugivores and extinction of any single disperser might have little effect on a tree’s net dispersal ability (Corlett, 1998). The added vegetative diversity provided by edge habitats and the matrix around fragment attracts small, omnivorous frugivores (Galetti et al., 2003, Pizo, 1997), potentially increasing the dispersal community for small-seeded species (Blake and Loiselle, 2001, Jules and Shahani, 2003).

Here, we offer a preliminary test of the hypothesis that forest fragmentation negatively impacts seed dispersal of a large-seeded tree species more than that of a small-seeded tree species. We examined the effects of forest fragmentation on the seed dispersal of two Amazonian tree species in a year of high fruit production. Duckeodendron cestroides Kuhlm. (Solanaceae) is a Central Amazon endemic with large fruits (5.9 cm long). Bocageopsis multiflora Mart. (Annonaceae) is more widely distributed and has small fleshy berries (0.8 cm diameter).

This study is the first comparison of fragmentation effects on the seed dispersal of two coexisting tree species with different fruit sizes in the aseasonal tropics. As such, we confronted several challenges: individuals of most species are rare (Oliveira, 1997), tree species fruit supra-annually usually with different fruiting phenologies; furthermore, measuring dispersal of large and small-seeded species requires different sampling methods (Herrera et al., 1998). Our results are tempered accordingly.