Effects of habitat loss on taxonomic and phylogenetic diversity of understory Rubiaceae in Atlantic forest landscapes
Introduction
Habitat loss is a major driver of the current rates of species extinction, considered the main global threat to biodiversity, especially in ecosystems with high endemism such as the Atlantic Forest in South America (Tabarelli et al., 2005). The Atlantic Forest from South America leads the world statistics of habitat loss, with over 93% of the original area lost (Galindo-Leal and Câmara, 2005). In Brazil, 11.4–16.0% of the Atlantic Forest still remains, including secondary forest areas and small fragments (Ribeiro et al., 2009), but only 3.5% of natural intact forest (Sloan et al., 2014). This high level of forest conversion results mainly from the accelerated population growth and the consequent increase of anthropogenic actions harmful to the environment.
In this context, habitat loss and the synergistic effects of habitat fragmentation adversely affect biodiversity patterns and population persistence in anthropogenic landscapes (Andrén, 1994, Fahrig, 2003). These landscapes are usually represented by few and small remaining patches (Andrén, 1994), which are subjected to a myriad of modifications due to increasing forest area exposed to edge effects (Laurance et al., 2001, Murcia, 1995, Oliveira et al., 2004, Saunders et al., 1991). As a consequence the microclimatic conditions are modified (Murcia, 1995). Besides, habitat loss might also change the canopy structure, which in turn modifies the amount of light that reaches the understory (Nicotra et al., 1999), influencing the distribution and persistence of many species mainly in this stratum. In Atlantic Forest fragments, there is little information about the understory flora, as most studies focus only the tree stratum (Kozera, 2001). Understory species have been highly neglected despite the fact that they represent almost two-thirds of the woody plant diversity in tropical forests, playing specific functions in the plant community (Poulsen and Balslev, 1991). In tropical forests, understory plants are also of key importance to the maintenance of many animal pollinators and seed dispersers (de Souza et al., 2009).
Among the plants in the Neotropics, Rubiaceae is an outstanding family, with the fourth highest number of individuals among all angiosperms (Chiquieri et al., 2004). The family is represented by approximately 13,100 species distributed in 611 genera (Govaerts et al., 2007). Brazil, is one of the numerous hotspots of the family diversity in the tropics (Govaerts et al., 2007), harboring approximately 1396 species in 120 genera (Barbosa et al., 2014). In addition, the Rubiaceae family is distinguish in the forest understory (Guaratini et al., 2008, de Lima et al., 2012; Martini et al., 2008; de Souza et al., 2009), exerting a strong influence on vegetation structure. Several species are important resources for animals that feed on pollen and nectar (Castro and Oliveira, 2002, Lopes and Buzato, 2005), and Rubiaceae is appointed as one the main sources of fleshy fruits to frugivores (Poulin et al., 1999, Snow, 1981, Tabarelli et al., 1999). Thus, this family is one of the most well-suited to be used in ecological analyses in tropical vegetation due to its representativeness, fewer taxonomical problems, and representation in all kinds of growth habits (Delprete and Jardim, 2012).
Identifying species that are being lost is undoubtedly very important for conservation. However, species identities per se often bring little information regarding their function or evolutionary history, which are also components of biodiversity (Cianciaruso et al., 2009, Swenson, 2011). Diversity measures such as phylogenetic information are increasingly being used to assess biological communities responses to environmental changes (Helmus et al., 2010). Important advances in this field are helping us to understand the effects of fires on community assembly (Cavender-Bares and Reich, 2012, Cianciaruso et al., 2012, Verdú and Pausas, 2007), the processes involved in community organization during forest regeneration (Letcher, 2010, Letcher et al., 2012), and the outcome of species loss and gain on community phylogenetic diversity (Arroyo-Rodríguez et al., 2012, Cadotte and Strauss, 2011, Santos et al., 2010, Santos et al., 2014).
Species susceptibility to habitat modifications might reduce phylogenetic diversity if traits associated to those modifications are evolutionarily conserved along particular lineages (Cavender-Bares et al., 2004, Webb et al., 2002). A recent study has demonstrated such a phylogenetic trait conservatism in Psychotria, the most common Rubiaceae genus, especially in hydraulic traits related to tolerance to changes in soil moisture (Sedio et al., 2012). If this evolutionary pattern also holds for other traits associated to vulnerability to deforestation, it is likely that remaining communities in more deforested areas are formed by closer relatives, being more phylogenetically clustered and poorer than those inhabiting less deforested areas (see also Arroyo-Rodríguez et al., 2012, Santos et al., 2010, Santos et al., 2014). Given that the extinction of highly distinct species from old and species-poor clades results in greater loss of evolutionary information (Redding et al., 2008, Winter et al., 2013), we also evaluated how forest loss affects the most original species.
Our goal was to evaluate how habitat loss at the landscape scale can affect species diversity of the understory Rubiaceae family. To accomplish this goal, we sampled nine forest fragments located within 16 km2 landscapes ranging from 9% to 71% of remaining forest cover, a proxy for habitat amount, and assessed not only common descriptors of diversity – such as species composition, richness, and abundance – but also measures of species originality, alpha and beta phylogenetic diversity. We predicted that the reduction of forest cover at the landscape scale would have a detectable negative impact on species diversity, with greater impact of rare species in more deforested landscapes. We also expected that forest cover reduction will favor the coexistence of closely related species, resulting in decreased phylogenetic diversity at both local (alpha) and regional (beta) scales.
Section snippets
Study sites
We conducted this study in Atlantic forest remnants from the south of the state of Bahia, northeastern Brazil, in the surroundings of Una, Mascote, and Belmonte municipalities, where we could identify representative patches of the original forests. These municipalities are located between the Jequitinhonha and the Contas rivers, where forest fragments have similar soil types, topography, and floristic composition (Thomas et al., 1998, Thomas, 2003), although human occupation has led to land use
Results
We collected 1857 Rubiaceae individuals in all forests remnants surveyed, encompassing a total of 21 genera and 68 species (Appendix C). Psychotria was the genus with the highest number of species (21), followed by Faramea (7) (Appendix C).
Species composition was variable among sampling sites, with 22 species (32.4%) present in only one forest remnant, 18 species (26.5%) in two, only six species (8.7%) recorded in six or more areas, and only one species, Psychotria platypoda, occurring in all
Discussion
Our results demonstrated that habitat loss, measured as the amount of forest cover at landscape scale, is strongly and negatively related to species richness, abundance, and diversity patterns of understory Rubiaceae. Previous studies have consistently shown the negative effects of habitat loss on species richness in general (Fahrig, 2003). However, empirical and theoretical evidence points to a non-linear relationship between habitat loss and biodiversity metrics, with more pronounced
Acknowledgments
The present study is a publication number #8 of the REDE SISBIOTA, funded by the Brazilian Council of Science and Technology (CNPq Proc. 563216/2010-7). We are grateful to the landowners for allowing us to work on their properties and to all who helped in the field work (especially Priscila Soares). We also thank the English editing service funding by PROPP/Universidade Estadual de Santa Cruz. ERA received fellowships from FAPESB (BOL 0492/2011) and DF is granted with a CNPq fellowship
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