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The Restoration of Tropical Seed Dispersal Networks Fernanda Ribeiro Da Silva1,2,3, Daniel Montoya4, Rafael Furtado5, Jane Memmott4, Marco A

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The Restoration of Tropical Seed Dispersal Networks Fernanda Ribeiro Da Silva1,2,3, Daniel Montoya4, Rafael Furtado5, Jane Memmott4, Marco A RESEARCH ARTICLE The restoration of tropical seed dispersal networks Fernanda Ribeiro da Silva1,2,3, Daniel Montoya4, Rafael Furtado5, Jane Memmott4, Marco A. Pizo5, Ricardo R. Rodrigues2 Human activities have led to the loss of habitats and biodiversity in the Atlantic Rain Forest in Brazil. Ecological restoration aims to rebuild this biome and should include not only the reinstatement of species but also the reestablishment of complex ecological interactions and the ecological functions that they provide. One such function is seed dispersal, which is provided by the interactions between animal frugivores and plants. We studied seed dispersal networks in 3 different tropical forest sites restored 15, 25, and 57 years ago; temporal scales rarely observed in restoration studies. We investigated changes in network structure (nestedness, modularity, and network specialization) in these communities over restoration time. Although network size and the number of interactions increased with time since restoration, the networks were composed of generalist birds, and the large frugivores remained absent. Contrary to our expectations though, species richness was highest in the 25-year-old site, maybe due to the higher number of species used in the planting. Nestedness values were low in all 3 networks, but the highest nestedness was observed in the intermediate-aged site. However, the oldest network was significantly modular and showed higher complementary specialization. These results suggest that 57 years after restoration, the complexity of mutualistic interactions in seed dispersal networks has increased, this enhancing ecosystem function in the Atlantic forest. Key words: Atlantic forest, birds, ecosystem function, network structure, restoration age less than 12% of the original forest remains distributed Implications for Practice mostly in small and isolated fragments (Ribeiro et al. • Restoring the interactions between species is an excellent 2009). In 2009, NGOs, governments, and research insti- starting point for rebuilding a community structure. tutions combined forces and started a restoration program • Bird-seed dispersal networks can be used as an indicator called the “Atlantic Forest Restoration Pact” (AFRP, of restoration of ecosystem function. http://www.pactomataatlantica.org.br/index.aspx?lang=en), • Measures of network structure could be used as an indi- which aims to restore 15 million hectares of degraded land in cator of restoration success, and frugivorous birds can be the Brazilian Atlantic Forest by 2050 (Calmon et al. 2011; Melo used as a model for evaluating the influence of restoration et al. 2013). However, whether these restoration actions recover in the ecological process in fragmented landscapes. forest communities remains largely unknown, and a general limitation of restoration projects worldwide is that monitoring the outcomes of long-term restoration projects is rarely done. The goal of this study is to analyze restored Atlantic forest sites Introduction using a network approach, whereby species and their interac- It is increasingly evident that restoration efforts should focus tions are recorded and the community is described in terms of not only on recovering species diversity and physiognomic traits community-level properties. To understand changes in network of the vegetation but also on the complex ecological interac- tions involved in the provision of ecosystem functions that ulti- Author contributions: FRS, RRR, MP, JM, DM designed the research; FRS, RF mately allow ecosystem reconstruction and perpetuation over performed the field work; FRS, DM designed analytical methods and analyzed the time (SER 2004; Rodrigues et al. 2009; Devoto et al. 2012). For data; FRS wrote the first draft; all authors contributed substantially to revisions. instance, the reestablishment of mutualistic networks between 1Departamento de Biologia Vegetal, Universidade Estadual de Campinas, Rua Mon- animal seed dispersers and plants is essential for the long-term teiro Lobato, 970, Caixa-postal 6109, Cep 13083-970, Campinas, São Paulo, Brazil 2Departamento de Ciências Biológicas, Laboratório de Ecologia e Restauração Flore- ecological restoration of tropical forests, where the majority of stal (LERF), Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São plant species rely on animals for seed dispersal (Forup et al. Paulo, Avenida Pádua Dias, 11, Cep 13418-900, Piracicaba, São Paulo, Brazil 3 2008; Devoto et al. 2012). Analyzing the architecture of mutual- Address correspondence to F. Ribeiro da Silva, email [email protected] 4School of Biological Sciences, Life Sciences Building, 24 Tyndall Avenue, Bristol istic networks between animals and fruit trees in restored areas BS8 1TQ, UK of forest can provide a useful tool for evaluating and monitor- 5Departamento de Zoologia, UNESP—Universidade Estadual Paulista, Cep 13506-900, Rio Claro, São Paulo, Brazil ing the restoration of the ecosystem function of seed dispersal (Tylianakis et al. 2010). © 2015 Society for Ecological Restoration doi: 10.1111/rec.12244 The Atlantic rainforest is a biodiversity hotspot with Supporting information at: high levels of endemism (Myers et al. 2000). Nowadays, http://onlinelibrary.wiley.com/doi/10.1111/rec.12244/suppinfo Restoration Ecology 1 Restoration of tropical seed dispersal networks Figure 1. The field site: (A) Brazil and São Paulo state; (B) 15-year-old restored area, in Santa Bárbara D’Oeste city; (C) 25-year-old restoredarea,in Iracemápolis city; (D) 57-year-old restored area, in Cosmópolis city. composition and structure following restoration, we studied Methods seed dispersal networks in three different tropical forest sites Study sites are riparian forest areas in the seasonal that were restored 15, 25, and 57 years ago, a timescale that is semi-deciduous forest domain (part of the Atlantic Forest rarely observed in restoration studies. We used this dataset to biome) in São Paulo state, Brazil. They were restored by address three questions: (1) How does restoration age affect replanting a high plant species diversity (70–140 species) 15, species richness and connectance? Older sites have been avail- 25, and 57 years ago. Both pioneer and nonpioneer species were able for colonization by species for a longer time, and therefore planted, initially with good weed control (Rodrigues et al. 2009, we expect a positive correlation between restoration age and 2011). Seedlings used in planting were chosen according to species richness. Given that connectance is negatively related availability from commercial sources and also from native seeds to network size (Allesina & Tang 2012), we predict a reduction collected from the surrounding landscapes. Some alien plants in the connectance of seed dispersal networks following time were used and others invaded (e.g. Cordia absynnica, Melia since restoration; (2) What are the effects of age on the structure azedarach, Callicarpa reevesii; see species list in Garcia et al. of seed dispersal communities? Network structure affects net- 2014). The 15-year-old area is 30 ha in size and 1,435 m from work stability (May 1972; Tylianakis et al. 2010), and network the nearest forest remnant of comparable size (22∘49′43.87′′S, metrics such as nestedness and modularity have been shown to 47∘25′57.71′′W). The 25-year-old area is 50 ha in size and increase community stability (Bascompte et al. 2006; Olesen 70 m from nearest fragment (22∘34′36.84′′S, 47∘30′ 29.92′′W), et al. 2007). Because restoration seeks to increase the stability and the 57-year site is 30 ha in size and 180 m from the nearest of restored communities, we predict that the older sites will be fragment (22∘40′18.84′′S, 47∘12′21.64′′W; WGS 84) (Garcia more nested and more modular; (3) Does restoration age affect et al. 2014) (Fig. 1). All areas are located in a highly degraded the level of specialization of the seed dispersal community? landscapes with sugarcane matrixes and low habitat cover. High specialization is associated with a greater diversity of resources in mutualistic networks, which in turn allows for higher consumer diversity and more coexisting species (Fründ Constructing Seed Dispersal Networks et al. 2010). We predict that, with restoration time, more niches Sites were sampled from January 2011 to December 2012 at will be available and, consequently, communities in older areas least once a month. At each site, we selected a plot 3 × 1,000 m will be more specialized. comprising almost entirely of 1.2 km of preestablished trails. 2 Restoration Ecology Restoration of tropical seed dispersal networks Within these plots, we collected the data to construct the seed generalist species that interact with each other and are respon- dispersal networks. Within each plot, fleshy fruited plants were sible for most of the interactions, (2) specialist species tend tagged and we observed fruit consumption by birds in those to have few interactions and interact preferably with generalist plants monthly; we observed every plant that fruited on the species, and (3) specialist species rarely interact with each other plots, although not all tagged plants fruited. We consider all (Bascompte et al. 2003, 2006). This architecture not only mini- plants with fleshy fruits as potential ornithochorous plants, anda mizes competition and enables more species to coexist (Bastolla species list for each site is provided in the Table S1, Supporting et al. 2009; Thébault & Fontaine 2010) but also implies an Information. We built qualitative
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