REPORT Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla Sabrina E. Russo1* and Carol K. Augspurger2 1 Department of Animal Biology, University of Illinois, 505 S. Goodwin Ave., Urbana, IL 61801, USA 2 Department of Plant Biology, University of Illinois, 505 S. Goodwin Ave., Urbana, IL 61801, USA *Correspondence and present address: Center for Tropical Forest Science ��� Arnold Arbor- etum Asia Program, Harvard University, 22 Divinity Avenue, Cambridge, MA 02138, USA. E-mail: srusso@oeb.harvard.edu Abstract The initial spatial pattern of seed deposition influences plant population and community structure, particularly when that pattern persists through recruitment. In a vertebrate- dispersed rain forest tree, Virola calophylla, we found that spatially aggregated seed deposition strongly influenced the spatial structure of later stages. Seed dispersion was clumped, and seed densities were highest underneath V. calophylla females and the sleeping sites of spider monkeys (Ateles paniscus), the key dispersal agent. Although these site types had the lowest per capita seed-to-seedling survival, they had the highest seedling/sapling densities. Conversely, seed and seedling/sapling densities were lowest, and seed survival was highest, at sites of diurnal seed dispersal by spider monkeys. Negative density-dependent and positive distance-dependent seed survival thinned seed clumps. Nonetheless, the clumped dispersion at sleeping and parental sites persisted to the seedling/sapling stage because differences in seed deposition were large enough to offset differences in seed survival among these site types. Keywords Ateles paniscus, dispersion, Myristicaceae, neotropical forest, Peru, recruitment, seed dispersal, seed survival, seedlings, Virola calophylla. Ecology Letters (2004) 7: 1058���1067 I N T R O DU C T I O N Seed dispersal results in colonization of potential recruit- ment sites and establishes the initial template of offspring dispersion. It therefore can strongly influence the spatial distribution of adult plants in a landscape (Howe & Smallwood 1982 Schupp & Fuentes 1995). The spatial distribution of individuals, in turn, mediates intra- and interspecific interactions, such as density-dependent mor- tality and competition, and the balance of these interactions affects species coexistence (Chesson 2000). Thus, under- standing the role of seed dispersal in the development of spatial pattern in plant populations is critical to explanations of plant community structure (Levin 1974 Hurtt & Pacala 1995 Chesson 2000). The development of spatial pattern in plant populations results from a set of processes governing the pattern of seed deposition and a set of post-dispersal processes that modify that pattern during recruitment (Schupp & Fuentes 1995 Schupp 1995). First, the spatial extent of seed dispersal restricts the suite of potential sites for recruitment (Howe & Smallwood 1982). However, there are few descriptions of seed dispersion at spatial scales large enough to encompass the variation in seed density generated by dispersal agents, particularly in forest communities. An increasing number of studies has revealed patterns of seed deposition in forests either by using seed traps and inverse modelling or by developing mechanistic models of the behaviour of dispersal agents to simulate seed dispersion (Nathan & Muller- Landau 2000). These studies suggest that seed deposition is often spatially aggregated, particularly for vertebrate- dispersed tree species (Schupp et al. 2002). Second, the spatial pattern of seed deposition and the recruitment consequences of that pattern affect the density and dispersion of plants in later life stages (Hubbell 1980 McCanny 1985). One mechanism that has figured prom- inently in explaining tree dispersion, particularly in tropical forests (Hubbell 1980 Augspurger 1983a Clark & Clark 1984 Condit et al. 1992), is survival that depends upon the density of seeds, seedlings, and/or saplings or their distance from a conspecific adult (Janzen 1970 Connell 1971). Such non-random survival resulting from natural enemies, such as seed predators and seedling pathogens, can thin clumps of seeds and seedlings and produce spatial patterns that differ from what would result simply from random thinning of the initial seed deposition Ecology Letters, (2004) 7: 1058���1067 doi: 10.1111/j.1461-0248.2004.00668.x ��2004 Blackwell Publishing Ltd/CNRS

pattern (Augspurger 1983a). Third, the availability and distribution of sites suitable for establishment, combined with the interactions between a plant���s regeneration requirements and its environment and other species, can also influence the spatial pattern of seedling and sapling recruitment (Grubb 1977). Dispersion of vertebrate-dispersed tree species, then, can be viewed in terms of the balance between dispersal processes that aggregate seeds and post-dispersal processes that alter the initial offspring dispersion pattern through non-random survival (Schupp & Fuentes 1995 Schupp 1995). However, the recruitment consequences of natural seed deposition patterns remain unquantified for all but a handful of the wide variety of plant���animal disperser systems (e.g. birds, Herrera et al. 1994 Wenny 2000 tapirs, Fragoso 1997 howler monkeys, Julliot 1997 rodents, Forget 1990, 1994, Forget et al. 1999). Despite recent advances (Houle 1992 Herrera et al. 1994 Nathan et al. 2000 Balcomb & Chapman 2003), the extent to which the spatial patterns of recruitment are determined by the initial seed deposition pattern remains a fundamental unanswered question in plant ecology. Thus, in order to understand the importance of seed dispersal for plant community ecology, we must describe its consequences for later life stages and link patterns of dispersion among multiple life stages (Levine & Murrell 2003). The objectives of this study were to investigate the development of spatial structure of a vertebrate-dispersed, neotropical nutmeg tree, Virola calophylla (Myristicaceae), and to determine whether dispersion shifts through time as individuals age. We evaluated how the spatial pattern of recruitment from the seed to the adult stage was modified from the initial template of seed deposition in V. calophylla growing in mature floodplain forest in Amazonian Peru. First, observations documented the spatial pattern of seed deposition. Second, natural and manipulative experiments quantified spatial variation in post-dispersal seed survival to the seedling stage. In particular, the strength of density- and distance-dependent mortality was estimated. Third, patterns of seed deposition and survival were related to densities of V. calophylla seedlings and saplings. Finally, the dispersion of juvenile and adult V. calophylla individuals was quantified and interpreted in light of the spatial structure of earlier life stages and the strength of density- and distance-dependent survival. Our results indicate that a clumped pattern of seed deposition was generated by the key dispersal agent, the spider monkey, Ateles paniscus (Platyrrhini). This clumped pattern was largely maintained through recruitment to the sapling stage, despite substantial density- and distance- dependent seed mortality, and was consistent with the clumped dispersion of adults. Thus, spatially aggregated seed dispersal had a strong, persistent effect on the spatial structure of this population of V. calophylla. M E T H O D S Study site This study was conducted from August 1999 to December 2001 at Cocha Cashu Biological Station (CCBS) in Manu�� National Park, Peru �� (18 812 km2, 11��54�� S, 71��18�� W, ele- vation c. 400 m). The average annual rainfall is c. 2000 mm, with most precipitation falling between October and April (Terborgh 1983). This study was conducted in c. 300 ha of mature floodplain forest at CCBS. This site has been described in detail in previous publications (Terborgh 1983 Gentry 1990). Dispersal system Species of Virola have been a model system for studying seed dispersal (e.g. Howe 1981 Howe et al. 1985 Forget & Milleron 1991). Virola calophylla is a dioecious, shade- tolerant, canopy tree in lowland moist forests of South America (Rodrigues 1980). At CCBS V. calophylla ripens fruit from early to mid-September to December. The fruit of V. calophylla is a bivalved, dark green capsule that opens upon ripening to expose a single seed with a bright red, oily aril. Most of the volume of the diaspore is comprised of the seed (length: 17.0 �� 1.8 mm, n �� 98 fresh mass: 1.4 �� 0.5 g, n �� 108 x �� SD). At CCBS seeds of V. calophylla are dispersed by at least 17 bird species and one primate, the spider monkey, Ateles paniscus (Russo 2003a). Based on 2 years of observations quantifying visitation and seed dispersal rates, spider monkeys dispersed 92% of dispersed seeds (Russo 2003a). They ingest up to 104 seeds in a visit and defecate them intact after gut passage times that range from c. 2.5 to 18 h (Milton 1981 S.E. Russo, unpublished data). They are highly frugivorous, forage primarily in the canopy and subcanopy, and have large home ranges (150���230 ha Symington 1987). Secondary dispersal of V. calophylla by rodents (Russo, in press) or dung beetles (Andresen 1994) appears to be minimal at CCBS. Non-dispersed and naturally and experimentally dispersed seeds A combination of observational and experimental methods was used to quantify seed deposition patterns and to compare seed survival and germination of non-dispersed seeds (seeds falling below the parent), seeds dispersed by spider monkeys, and experimentally dispersed seeds. To characterize seed production, seed-fall below, and seed dispersal from V. calophylla females, 10 female trees bearing fruit in the study area in 2000 were randomly selected. The area of the crown projection of each tree was estimated based on the area of an ellipse by measuring four radii of the Seed dispersal and plant recruitment 1059 ��2004 Blackwell Publishing Ltd/CNRS