Fruiting phenology of palms and trees in an Atlantic rainforest land-bridge island

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Abstract

Tropical forests show periods of scarcity and high fruit production in the same year and/or between years. Palms are an important component of Neotropical rainforests and a significant food resource for several frugivores. Therefore, their role as keystone resource may be exacerbated in highly impoverished areas. In Anchieta Island, São Paulo/Brazil, human settlements have modified and impoverished the forest, mainly through overharvesting and the introduction of exotic plants and several mammal species. We assessed the offer of fruits consumed by vertebrate frugivores at this island, the vegetation of which is belonging to the Brazilian Atlantic rainforest. We compared whether the fruiting patterns and fruit fall differ between palms and trees, and discuss the importance of palms as a food resource for frugivores and the implications for Anchieta Island conservation. Phenological patterns were seasonal for both trees and palms; however, the times of fruiting occurrence differed. Fruit fall biomass was at least twice lower than reported for other Atlantic rain forests and was also different between trees and palms. Palms contributed more than 80% of the overall fruit fall biomass. Palms may constitute an alternative food resource in periods of low fruit availability, although they do not provide resources for the entire assemblage of vertebrate frugivores. Energy-rich fruits, such as those produced by palms, may play an important role in the maintenance of frugivore populations in isolated, disturbed environments with a high density of vertebrate frugivores, low diversity of fruiting species and fruit biomass such as those found on Anchieta Island.

Introduction

Tropical rainforests are considered one of the world's most productive habitats, where fruit biomass ranges between 180 and 1000 kg ha−1 yr−1 (Jordano, 1992). Of this biomass, about 70–94% is produced by woody species, and the seeds and fruits are dispersed by vertebrates (Howe and Smallwood, 1982; Jordano, 1992). Despite this high fruit production, phenology patterns display both, temporal and spatial fluctuations in well-preserved tropical rain forests (Castro et al., 2007; Frankie et al., 1974; Morellato et al., 2000; Wright et al., 1999). Although seasonal reproduction patterns are frequently found in most tropical rain forests, weak or non-seasonal fruiting patterns have been also reported for some communities (Hilty, 1980; Koptur et al., 1988; Morellato et al., 2000). Phenological patterns are also influenced by the successional status of the forest and secondary forests might present more extended fruiting patterns and larger crop sizes per area than primary forests (Fleming, 1985; Levey, 1988a, Levey, 1988b).

Palms are an important food resource for a wide assemblage of vertebrate frugivores (Forget et al., 1994; Galetti et al., 1999; Kiltie, 1981; Peres, 1994a; Zona and Henderson, 1989), and have been regarded as a “keystone resource” for frugivores in tropical forests (Kinnaird, 1992; Terborgh, 1986a). The Arecaceae family presents a wide distribution in tropical and subtropical areas of the world with approximately 189 genera and 3000 species (Henderson et al., 1995). Neotropical forests comprise 60 genera and 550 species of palms, with at least 10 genera and 40 species occurring in the Brazilian Atlantic forest, many of which are endemic (Henderson et al., 1995).

Reproductive phenological studies on palms are frequently based on a single species (Borchsenius, 2002; Castro et al., 2007; Galetti et al., 1999; Henderson et al., 2000; Scariot and Lleras, 1995), and less frequently on several species or communities (Borchsenius, 1997; De Steven et al., 1987; Henderson et al., 2000; Ibarra-Manríquez, 1992; Peres, 1994b). As far as we know, this is the first study to compare palm fruiting phenology patterns with the wider tree community.

Insular environments have long been used by biologists to test basic principles of ecology, evolution and biogeography (Vitousek et al., 1995; Whitaker, 1998). More recently, insular environments have played a prominent role in conservation ecology, where the aim has usually been to conserve species or assemblages unique to isolated habitats (Drake et al., 2002). Islands, because of their peculiar attributes (isolation, small populations, community “impoverishment”, absence of entire taxonomic groups and high levels of endemism) (Whitaker, 1998), are more susceptible than continental habitats and have historically been disturbed due to human intervention mostly through the introduction of invasive plants and feral animals that are conducive to the disruption of mutualism (Courchamp et al., 2003; Fernandez Palácios and Morici, 2002; Maunder et al., 2002).

In the coastal area of Brazil, land-bridge and oceanic islands have been highly disturbed by the introduction of exotic species (Bovendorp and Galetti, 2007). One of these islands is Anchieta Island (Parque Estadual Ilha Anchieta), located 530 m off the coast of the state of São Paulo, southeast Brazil. In 1983, Anchieta Island suffered from the introduction of several mammal species such as agoutis, coatis, capybaras, deer and armadillos (Bovendorp and Galetti, 2007). The establishment of human settlements in the area resulted in the modification and impoverishment of the forest, mainly through overharvesting and the introduction of exotic plants species (Guillaumon et al., 1989). Therefore, common vertebrate-dispersed families of Atlantic rainforest trees such as Lauraceae, Myristicaceae and Myrtaceae are rare and most of the natural vegetation has been altered (Guillaumon et al., 1989). Nine palms with seeds dispersed by vertebrates occur on the island, of which six are native and three are exotic.

We evaluated the temporal variation in the offer of fruit species consumed by vertebrate frugivores on Anchieta Island from a comparative perspective. We contrast the fruiting patterns and fruit fall between palms and trees and discuss the importance of palms as a food resource for frugivores in this disturbed habitat. We expected to find longer fruiting patterns for palms in relation to that presented by trees, therefore emphasizing the importance of palms as a reliable and high-quality food resource (De Steven et al., 1987; Peres, 1994b) for introduced and native vertebrate frugivores in the impoverished environment of Anchieta Island. We suggest that palms may represent a keystone resource, supporting vertebrate frugivores on highly disturbed, isolated environments.

Section snippets

Study site

The study was carried out at Anchieta Island, a land-bridge island of 806 ha located in Ubatuba, Northeast of São Paulo State, Brazil (45°02′W, 23°31S) (Fig. 1).

By the middle of the 19th century, the original indigenous settlements of Anchieta Island were supplanted by Europeans, who subsisted through activities such as fishing, and coffee, sugarcane, corn and potato cultures (Guillaumon et al., 1989). In 1904, the residents of the island were transferred to the continent due to the

Results

We observed the phenology of 57 species, where 67% were vertebrate-dispersed species, 12% were wind dispersed, 5% were autochoric and 16% were undetermined (see Appendix A). Of the 272 trees sampled, 29.8% did not show any reproductive event, 51.1% just flowered and 19.1% flowered and fruited. We observed 50 tree species from which 8% did not show reproductive activity, 12% just flowered and 80% flowered and fruited. From the 116 palms sampled, 16.4% did not show any reproductive event, 10.3%

Discussion

Contrary to our expectations palms, similar to trees, presented seasonal fruiting patterns on Anchieta Island. However, the divergent timing of occurrence of ripe fruits between palms and trees suggests a complementary ripe fruiting pattern, thereby providing food resources for frugivores throughout the year, as expected. Seasonal and non-seasonal fruiting patterns have been reported for tropical rain forest trees (Hilty, 1980; Koptur et al., 1988; Morellato et al., 2000; Williams-Linera, 1997

Acknowledgments

We thank M.A. Pizo (Universidade do Vale do Rio do Sinos, UNISINOS) for suggestions on early versions of this manuscript, and the State of São Paulo Research Council (Fundação de Amparo à Pesquisa do Estado de São Paulo, FAPESP) for financial support and to the Instituto Florestal from São Paulo State for permission to work at Anchieta Island. We also thank Idea Wild for providing field equipment. J. Genini received a fellowship from CAPES and from the Brazilian International Student Program

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