The challenge of maintaining Atlantic forest biodiversity: A multi-taxa conservation assessment of specialist and generalist species in an agro-forestry mosaic in southern Bahia
Introduction
Habitat loss and fragmentation are two closely linked anthropogenic threats with a significant influence on extant patterns of species distribution and abundance (Pimm and Raven, 2000). Today a significant part of the terrestrial biodiversity is found in fragmented landscapes, and since the landmark publication of island biogeography theory (MacArthur and Wilson, 1967), a growing body of research has allowed ecologists to start disentangling the main effects of habitat loss and fragmentation upon biological assemblages (Fahrig, 2003, Ewers and Didham, 2006, Fischer and Lindenmayer, 2007).
Habitat loss and fragmentation adversely affect species persistence mainly through reduction in available native core habitat, increase in isolation among remnant patches and edge effects (Laurance et al., 2002, Fahrig, 2003, Kupfer et al., 2006). In general, habitat reduction increases the likelihood of stochastic extinction in fragments; an effect that is rarely offset by migrants due to increased patch isolation (Hanski, 1998). The influence of the modified habitats that surround remnants, the so called edge effect, is known to affect forest microclimate (Didham and Lawton, 1999), vegetation structure (Laurance et al., 2006) and, thus the structure of animal communities (Didham et al., 1998, Laurance et al., 2002). The interaction between fragmentation and other human-induced pressures (hunting, logging, fire) further threatens species in fragmented landscapes (Gascon et al., 2000, Silva and Tabarelli, 2000, Laurance, 2004).
Most of the conceptual framework of habitat fragmentation studies, derived from the island biogeography theory, was built under the assumption that only two components of a given landscape are important in determining species persistence: remnants of native forest or habitat and non-forest/non-habitat areas (Kupfer et al., 2006). This simplification emphasizes the importance of native remnants for the maintenance of native biodiversity while underestimates the role of landscape structure and composition, including the amount and spatial arrangement of remaining habitats and the structure and quality of the intervening matrix (Haila, 2002, Ewers and Didham, 2006).
Given the non linear relationship between habitat loss at the landscape scale and the characteristics of remaining patches (such as mean patch size or mean distance among patches, see Andrén, 1994, Fahrig, 1997, Fahrig, 2003), the likelihood of species extinction is expected to increase drastically when the area of remaining habitat is suppressed below a threshold value. This fragmentation threshold, however, has been demonstrated to vary among taxa, regions and spatial scales (With and Crist, 1995, Huggett, 2005, Lindenmayer and Luck, 2005, Radford et al., 2005).
The importance of heterogeneous anthropogenic habitats in the intervening matrix is not limited to their potential for promoting species movements across landscapes, but also in providing suitable habitat and resources for the native biota (Ewers and Didham, 2006, Fischer and Lindenmayer, 2007). These surrounding modified habitats can be of particular importance for species persistence when they present low structural contrast with the primary habitat (Collinge and Palmer, 2002). In tropical landscapes, although second-growth forests are not surrogates for primary forest, they can provide suitable habitat for a component of local assemblages (Barlow et al., 2007). The potential of modified habitats to harbor forest species, however, varies among biological groups (Schulze et al., 2004, Pineda et al., 2005, Harvey et al., 2006, Faria et al., 2006, Faria et al., 2007). Considering the rapid pace of deforestation, it is important to establish the actual conservation value of these modified habitats for biodiversity conservation (Gardner et al., 2007).
In the light of these recent research developments it is expected that fragmented landscapes comprising high amounts of remaining habitat, and heterogeneous anthropogenic habitats that are relatively structurally complex, may harbor an appreciable component of the native biota. This would allow, therefore, the potential for reducing biodiversity loss in altered tropical landscapes through the maintenance of a relatively high percentage of forest combined with sensitive management of anthropogenic areas. However, few attempts have been made to test this prediction in fragmented tropical forest landscapes (Lindenmayer and Luck, 2005), especially for multiple taxonomic groups.
The Atlantic forest stretched along most of the Brazilian coast and has been reduced, except for few large conservation units, to small remnants (<100 ha), mainly composed of second-growth forest, and immersed in agricultural or urban matrices (Ribeiro et al., 2009). An exception to this pattern is observed in some regions of the cacao-producing zone of southern Bahia, where mature forest remnants are inserted in a mosaic of cleared land, second-growth forests and cacao plantations shaded by native trees.
We conducted a large-scale, multi-taxa, standardized survey in a landscape in the cacao-growing region of southern Bahia to evaluate its potential for maintaining native biodiversity. Using standardized field protocols we sampled ferns, frugivorous butterflies, leaf-litter frogs and lizards, bats, small mammals and birds in six replicates of six habitat categories – second-growth forests, shade cacao plantations, interiors and edges of large (>1000 ha) and small (<100 ha) mature forest remnants, as well as trees in a subset of these habitats (interiors of large and small mature forest remnants). We investigated the biodiversity value of matrix habitats (shade cacao plantations and second-growth forest) compared to mature forest (interiors of large mature forest remnants) for ferns and all animal groups. By comparing habitat categories within mature forest remnants, we also evaluated the effects on biodiversity of area reduction (for ferns, trees and all animal groups), and edge proximity (for ferns and all animal groups). For each taxonomic group we considered the richness, abundance and composition of two distinct sets of species, forest specialists and habitat generalists, that vary in their dependence to humid forest, an thus, extinction proneness.
Section snippets
Study area and sites
Southern Bahia encompasses some of the largest remnants of Atlantic forest in northeastern Brazil. The study was carried out in the Una municipality (15°17′S, 39°04′W), located in the coastal zone of the cacao-growing region. By the time the project was carried out, 7000 ha of forest was protected as a conservation unit (Una Biological Reserve – RebioUna). The forest is classified as tropical lowland rainforest, the mean annual temperature is 24 °C and mean rainfall is around 2000 mm year−1, with
Results
We found a total of 431 species in the 36 sites in Una – 60 species of ferns, 86 frugivorous butterflies, 15 leaf-litter frogs, 13 leaf-litter lizards, 39 bats, 19 small mammals and 199 birds. From those, 151 were classified as forest specialists and 280 as generalists. Among the 498 species of trees recorded in the 12 sites in Una (260 among dominant trees, 309 among understory trees and 397 among tree saplings), 334 were classified as shade tolerant, 126 as shade intolerant and 38 could not
Discussion
The results of studies designed to investigate the effects of habitat or landscape modification on biodiversity depend strongly on which taxonomic groups are sampled as well as on which metric is used to analyze assemblage responses (Barlow et al., 2007). With the exception of small mammals and ferns, the six remaining taxonomic groups considered in this study were shown to be among the seven best ecological indicators of coarse-scale changes in habitat integrity as suggested by a recent
Acknowledgements
We thank W.F. Laurance for encouragement and assistance in designing the project; S.G. Laurance and J.P. Metzger for help on landscape analysis; T.A. Gardner, P.I. Prado and three anonymous referees for valuable comments on the manuscript; PROBIO-PRONABIO/MMA – CNPq/BIRD-GEF, FAPESP, WWF/Brasil, Ford Foundation/IESB and Lincoln Zoo – Scott Neotropical Fund for Grants; and IESB-Instituto de Estudos Sócio Ambientais do Sul da Bahia for providing the aerial photographs.
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- 1
Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Rodovia Ilhéus Itabuna, Km 16, CEP 45650-000 Ilhéus, BA, Brazil.
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Departamento de Ciências Naturais, Universidade Regional de Blumenau (FURB), CP 1507, CEP 89010-971 Blumenau, SC, Brazil.
- 3
Departamento de Ciências Biológicas, Universidade Estadual do Sudoeste da Bahia, Campus Jequié, Rua José Moreira Sobrinho, CEP 45206-190 Jequiezinho, Jequié, BA, Brazil.
- 4
Herbário UNIP, Universidade Paulista, Avenida Paulista, 900, Bela Vista, CEP 01310-100 São Paulo, SP, Brazil.