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Disentangling the Drivers of Reduced Long-Distance Seed Dispersal by Birds in an Experimentally Fragmented Landscape

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Disentangling the Drivers of Reduced Long-Distance Seed Dispersal by Birds in an Experimentally Fragmented Landscape Ecology, 92(4), 2011, pp. 924–937 Ó 2011 by the Ecological Society of America Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape 1,5 1,2 2 2 3 MARI´A URIARTE, MARINA ANCIA˜ ES, MARIANA T. B. DA SILVA, PAULO RUBIM, ERIK JOHNSON, 4 AND EMILIO M. BRUNA 1Department of Ecology, Evolution and Environmental Biology, Columbia University, 1200 Amsterdam Ave., New York, New York 10027 USA 2Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazoˆnia and Smithsonian Tropical Research Institute, Manaus, AM 69011-970 Brazil 3School of Renewable Resources, Louisiana State University, 227 RNR Building, Baton Rouge, Louisiana 70803-6202 USA 4Department of Wildlife Ecology and Conservation and Center for Latin American Studies, University of Florida, Gainesville, Florida 32611-0430 USA Abstract. Seed dispersal is a crucial component of plant population dynamics. Human landscape modifications, such as habitat destruction and fragmentation, can alter the abundance of fruiting plants and animal dispersers, foraging rates, vector movement, and the composition of the disperser community, all of which can singly or in concert affect seed dispersal. Here, we quantify and tease apart the effects of landscape configuration, namely, fragmentation of primary forest and the composition of the surrounding forest matrix, on individual components of seed dispersal of Heliconia acuminata, an Amazonian understory herb. First we identified the effects of landscape configuration on the abundance of fruiting plants and six bird disperser species. Although highly variable in space and time, densities of fruiting plants were similar in continuous forest and fragments. However, the two largest- bodied avian dispersers were less common or absent in small fragments. Second, we determined whether fragmentation affected foraging rates. Fruit removal rates were similar and very high across the landscape, suggesting that Heliconia fruits are a key resource for small frugivores in this landscape. Third, we used radiotelemetry and statistical models to quantify how landscape configuration influences vector movement patterns. Bird dispersers flew farther and faster, and perched longer in primary relative to secondary forests. One species also altered its movement direction in response to habitat boundaries between primary and secondary forests. Finally, we parameterized a simulation model linking data on fruit density and disperser abundance and behavior with empirical estimates of seed retention times to generate seed dispersal patterns in two hypothetical landscapes. Despite clear changes in bird movement in response to landscape configuration, our simulations demonstrate that these differences had negligible effects on dispersal distances. However, small fragments had reduced densities of Turdus albicollis, the largest-bodied disperser and the only one to both regurgitate and defecate seeds. This change in Turdus abundance acted together with lower numbers of fruiting plants in small fragments to decrease the probability of long-distance dispersal events from small patches. These findings emphasize the importance of foraging style for seed dispersal and highlight the primacy of habitat size relative to spatial configuration in preserving biotic interactions. Key words: Amazonian rain forest; dispersal kernels; frugivory; habitat fragmentation; Heliconia acuminata; manakins; Manaus, Brazil; patch size; spatially explicit model; thrush; tropical forest; Turdus albicollis. INTRODUCTION Willson et al. 1989, Jordano 1992, Tiffney and Mazer 1995). Despite the critical role frugivores play in the Seed dispersal is a crucial component of plant organization of plant communities, general principles population dynamics (Levine and Murrell 2003). In about the effects of animal disperser agents on plant the temperate zone, 25–40% of plant species depend on populations and communities remain elusive (Carlo and frugivores for seed dispersal, whereas in tropical rain Morales 2008). In part, this is because patterns of seed forests, up to 90% of woody species do (Gentry 1982, deposition are an emergent property of disperser–plant interactions resulting from individual- and species-level frugivore behavior (Schupp et al. 2002), the composition Manuscript received 9 April 2010; revised 9 September 2010; of the disperser community (Clark et al. 2005), the accepted 13 September 2010 Corresponding Editor: C. M. Herrera. spatial distribution of food resources (Morales and 5 E-mail: [email protected] Carlo 2006, Carlo and Morales 2008), and landscape 924 April 2011 SEED DISPERSAL AND HABITAT FRAGMENTATION 925 structure (Levey et al. 2005). All of these factors can deforestation and fragmentation, understanding dispers- vary over space and time, often in unexpected ways. er responses to landscape features is particularly critical Frugivore behavior can shape plant populations in in tropical ecosystems. The maintenance of plant myriad ways. Individuals often track the location of populations in habitat fragments and other altered fruit resources in space and time (Levey et al. 1984; but tropical landscapes will require evaluation of the factors see Lehouck et al. 2009a), responding to crop size and that shape animal–plant interactions and the role of the spatial distribution of resources at the landscape animal movement and foraging behavior on seed level (Farwig et al. 2006, Morales and Carlo 2006). dispersal and seedling recruitment (Morales and Carlo Frugivores may move shorter distances when resources 2006). are spatially clustered (Carlo and Morales 2008). In Research on the mechanistic basis of seed dispersal addition, forager density (Carlo and Morales 2008), has often relied on simulation models that vary interactions among dispersers (Schupp et al. 2002), and considerably in the amount of field-based data used their nonrandom use of space (Russo et al. 2006) could for calibration (e.g., Higgins et al. 2003, Carlo 2005, influence the quantity of seeds dispersed at different Levey et al. 2005, Russo et al. 2006). However, few of distances from parent plants and the shape of the these studies have addressed how anthropogenic habitat dispersal kernel (Schupp et al. 2002). For example, modification alters seed dispersal; those that have done certain vertebrate vectors may prefer particular micro- so limit themselves to examining how a single landscape habitats (e.g., lekking sites), or defecate or consume feature (e.g., the presence of corridors) influences fruits at specific locations such as roosts (e.g., Russo et dispersal (e.g., Levey et al. 2005). Other studies have al. 2006). These behaviors can shape the spatial quantified the ultimate effects of landscape configura- configuration of fruit removal (Carlo and Morales tion on seedling recruitment without attempting to 2008) and dispersal-related gene flow (Loiselle et al. disentangle the relative contributions of different com- 1995). ponents of dispersal (e.g., fruit abundance, disperser Plants are commonly visited by several dispersal abundance, disperser behavior) to the observed decline vectors (Wheelwright et al. 1984, Jordano et al. 2007). in establishment (e.g., Bruna 2002; but see Cordeiro et Analyses of frugivore communities have demonstrated al. 2009, Lehouck et al. 2009b). Yet, understanding how species-specific differences in visitation rates, fruit landscape modifications influence different components removal, and post-feeding behavior, which can result of disperser–plant interactions is critical to the develop- in distinct spatial signatures for different dispersal ment of effective management or conservation schemes. vectors (Schupp et al. 2002, Clark et al. 2005, Jordano Here, we examine how anthropogenic landscape et al. 2007, Lehouck et al. 2009b). In general, large modifications influence the dispersal of seeds of the vertebrates (e.g., monkeys) can ingest large numbers of Amazonian herb Heliconia acuminata (Heliconiaceae). seeds and disperse them over long distances. In contrast, To do so, we collect data on plant distribution, fruit smaller animals (e.g., small birds, ants) typically deposit abundance, and the composition, abundance, foraging seeds next to the source plants and, for animals ingesting behavior, and movement of bird dispersers of H. seeds, have faster regurgitation or defecation times acuminata in an experimentally fragmented Amazonian (Clark et al. 2005, Jordano et al. 2007). landscape. Using these data, we develop an individual- Theoretical and empirical studies have demonstrated based, spatially explicit mechanistic model to estimate that landscape heterogeneity such as fragmentation and seed dispersal kernels and to simulate vector movement habitat loss can reduce long-distance dispersal for wind- and seed dissemination in heterogeneous landscapes. We dispersed species (Higgins et al. 2003, Soons et al. 2005). address the following questions: (1) How does landscape Landscape heterogeneity can also alter fruit availability configuration, namely the size of isolated primary forest (Soons et al. 2005, Farwig et al. 2006, Cordeiro et al. fragments and the composition of the surrounding forest 2009), disperser abundance (Bierregaard and Lovejoy matrix, affect fruit availability and bird disperser 1989, Moran et al. 2009), disperser behavior (Jordano diversity, abundance, and behavior? (2) What are the and Schupp 2000, Clark et al. 2005, Lehouck et al. implications of these effects for the dispersal of H. 2009c), and interspecific
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