Original articleReduced availability of large seeds constrains Atlantic forest regeneration
Highlights
► Seed rain is critical for forest recovery after slash-and-burn agriculture. ► We assessed successional shifts in seed rain in the highly fragmented Atlantic forest. ► Large-seeded species were surprisingly underrepresented throughout the chronosequence. ► This may reduce forest resilience and its ability to provide ecosystem services.
Introduction
Secondary forests are becoming increasingly common in the tropics as abandoned agricultural lands recover through secondary succession (FAO, 2009, Gardner et al., 2009). Global estimations indicate that around half of the world’s remaining tropical forest is second-growth forests or degraded old-growth forests affected by selective logging, road opening, fire, fragmentation, overhunting, and other anthropogenic forces (ITTO, 2002). Unfortunately, the rapid expansion of secondary tropical forests has been not paralleled by a similar understanding on their functioning. Recent studies highlight the potential of these novel forests to protect soils, cycle nutrients, support wildlife, store carbon, maintain watershed function, and mitigate species extinction (Wright and Muller-Landau, 2006, Chazdon et al., 2009, Lugo, 2009), but the ecological processes involved in the maintenance of these functions are not completely understood.
It is well-known that the continuous influx of native seeds is among the most important ecological processes involved in forest regeneration (Guariguata and Ostertag, 2001). Altered seed rain invariably results in biased seedling assemblages (e.g. Melo et al., 2006, Melo et al., 2007), which in turn result in impoverished tree assemblages (Laurance et al., 2006, Santos et al., 2008, Santos et al., 2010) and possibly entire communities with limited ability to maintain biodiversity and provide ecosystem services (see Gardner et al., 2009, Parry et al., 2009, Schindler et al., 2010). Nevertheless, seed rain remains scantly studied in secondary tropical forests (e.g. Barbosa and Pizo, 2006, Castillo and Ríos, 2008), particularly in older forest stands (>45-yr old) where community structure, composition, and functioning start to approach those of old-growth forests (Saldarriaga et al., 1988, Guariguata and Ostertag, 2001, Chazdon et al., 2007).
Seed arrival from adjacent areas assumes a disproportional importance in the first years of regeneration when deforestation is followed by fire (Uhl, 1982), given that fire eliminates the soil seed bank, pre-existing seedlings and saplings, resprouting of broken trees and other sources of plant recruitment (Yao et al., 1999). As regeneration advances and the first colonizers achieve maturity, seeds produced locally also contribute to forest recovery (Guariguata and Ostertag, 2001). Some decades later, the arrival of late-successional seeds from adjacent old-growth forests − most large seeds dispersed by large-bodied vertebrates (e.g. monkeys) − is critical to drive mid-successional stages toward older successional ones. Assuming that deforestation and forest fragmentation negatively affect large-bodied seed dispersers, reduce the amount of old-growth forests locally and regionally, and favor the hyper-proliferation of early-successional small-seeded pioneer trees (Silva and Tabarelli, 2000, Laurance et al., 2008, Tabarelli et al., 2010), it is likely that local reduction in the availability of large seeds constrains forest regeneration following slash-and-burn agriculture in fragmented neotropical landscapes. This phenomenon has been described for Atlantic forest edges (Melo et al., 2006) and helped to explain why these degraded habitats are not able to attain older successional stages or maintain old-growth forests (Santos et al., 2008, Santos et al., 2010, Tabarelli et al., 2008).
In this study we examined successional shifts in seed rain across 19, 32, and 62-yr old forest stands recovering after slash-and-burn agriculture in the Atlantic forest of Northeast Brazil, a severely fragmented region now reduced to less than 6% of its original pre-Colombian extent (Galindo-Leal and Câmara, 2003). We selected forest stands completely immersed into a large (3500 ha) forest remnant that still retains large tracts of old-growth forest, but not all large frugivores recorded for the Atlantic forest (see Methods). Every 15 days during 12 months we monitored seed rain in terms of seed density, species richness, taxonomic and functional composition, and spatial distribution at the forest stand level. We predicted that local seed density would decrease and per capita species richness would increase during forest succession due to the replacement of pioneer trees by a more diverse group of late-successional trees that reproduce less frequently and more scantly. The proportion of vertebrate-dispersed species was expected to be elevated at any forest stand because zoochory is a widespread dispersal syndrome in the local flora (see Oliveira et al., 2004, Santos et al., 2008). The proportion of large-seeded species in the seed rain was predicted to increase with forest age because active dispersal of large seeds in the study site is greater in old-growth than second-growth-like areas (Melo et al., 2006). As long described in the literature of tropical forest regeneration (reviewed by Guariguata and Ostertag, 2001), we expected gradual changes in species composition and floristic divergence during the regeneration process. Finally, because copious seed production is expected for forest stands dominated by pioneer plants (i.e. earlier successional forest stands) and more than 99% of the seeds in tropical forests usually fall down near parents (Terborgh et al., 2002, Bentos et al., 2008), we predicted a gradual reduction in spatial aggregation of seed rain, which may further minimize negative density dependence effects and result in more diverse seedling assemblages (Harms et al., 2000).
Section snippets
Study site
The study was carried out at Usina Serra Grande, a 667-km2 private sugar-cane landholding in the state of Alagoas, northeastern Brazil (Fig. 1). Serra Grande is located on a low altitude plateau (300–400 m above sea level) covered by two similar classes of dystrophic and clay-laden soils: yellow-red latosol and yellow-red podzol according to the Brazilian system of soil classification (IBGE, 1985). Annual rainfall is ∼2000 mm, with a three-month dry season (<60 mm per month) from November to
Results
After a 12-month period, a total of 418,713 seeds belonging to 180 morphospecies were recorded across the three second-growth stands. Both number of seeds (F2,57 = 4.62; P = 0.0138) and species (F2,57 = 5.54; P = 0.0063) per squared meter declined along forest regeneration (Table 2). However, the number of species per seed (per capita species richness) was highest in the 62-yr stand, where individual/species accumulation curves rose more rapidly than in the other stands (Fig. 2).
Only 0.2% (833
Discussion
In general, our results suggest that advancing forest regeneration in Coimbra is experiencing successional changes in seed rain as predicted by other studies on neotropical secondary forest succession (reviewed by Guariguata and Ostertag, 2001). From early to late-successional stage, seed rain decreased in density, increased in per capita species richness, gradually changed in species composition and became less aggregate spatially. All these directional changes in seed rain can be explained by
Acknowledgments
We thank Ray Froend and two anonymous reviewers for valuable comments on a previous version of this manuscript. We are grateful to Usina Serra Grande for research facilities and Conselho Nacional de Desenvolvimento Científico e Tecnológio (CNPq), Conservation International (CI-Brazil), and Centro de Pesquisas Ambientais do Nordeste (CEPAN) for essential financial support. BAS and MT are thankful to CNPq for postdoctoral fellowship and research grant, respectively.
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