Victoria Andrea Barrera Zambrano^1,2, Jenny Zambrano Moncada^1,3 & Pablo R. Stevenson^1,4

1. Centro de Investigaciones Ecológicas La Macarena, Departamento de Ciencias Biológicas, Universidad de los Andes, Carrera 1 Numero 18ª-10, Bogotá, Colombia, Tel 0571 3394949-2770;

2. barrera.andreav@gmail.com,

3. je-zambr@uniandes.edu.co; jennyzambrano@hotmail.com

4. pstevens@uniandes.edu.co

Abstract: Hunting may have drastic effects on some populations of frugivores and seed dispersal agents, which in turn may affect patterns of forest regeneration and plant diversity. However, when a species disappears, it is possible that the population of other species increases due to competition release, compensating or not, their ecological roles. The main aim of this study was to measure density compensation in primate communities, their possible effects on seedling and sapling diversity, and compensation of seed removal rates in two canopy trees (Apeiba aspera and Hymenaea oblongifolia). The study site was Amacayacu National Park (Colombian Amazon), where we carried out a census of mammal species using line transect methods in two forests with different levels of hunting pressure. Vegetation plots were used to quantify plant diversity for seedlings and saplings (4 m² and 25 m² respectively), and fruit traps were set up to estimate seed removal of A. aspera and H. oblongifolia. Large primates were less frequently encountered near human settlements, while small primates exhibited the opposite pattern, suggesting a density compensation effect. The diversity of regenerating plants was higher in the forest where large primates occur. Seed removal was higher in forests with large primates for A. aspera, but not for H. oblongifolia. Overall, the results support the hypothesis of density compensation on the primate community; however, there is no strong evidence of ecological compensation in terms of seed dispersal and regeneration in the species studied. Finally, the presence of large seed dispersers (e.g. Lagothrix lagothricha) was associated with higher plant diversity. Rev. Biol. Trop. 56 (3): 1531-1542. Epub 2008 September 30.

Central and western Amazonia tropical rain forests have been considered mega-diver-sity areas (Gentry 1988, Ter Steege et al. 2003), and several hypothesis have tried to explain this fact (Tuomisto et al. 1995, Wills et al. 1997, Schupp et al. 2002, Terborgh et al. 2002). Theories well supported by empirical data include negative density-dependent effects, low competition among young plants, and niche differentiation (Wright 2002). Negative density-dependent effects due to intra-specific competition and the attack of pathogens or predators, have been included in different models to predict changes on spatial patterns, regeneration, and diversity of plant species (Hubbell et al. 1999). Less attention has been focused in the role of inter-specific plant competition involving seed dispersal agents (Peres and van Roosmalen 2002).

Janzen (1970) and Connell (1971) suggested that the survival probability of the offspring below parental trees is low. Plants may experience negative density and distance-dependent effects, caused by pathogens and seed predators, as well as intra-specific competition. According to this theory, in the absence of dispersal mechanisms, some species such as large seeded animal dispersed plants would not be able to recruit in the long term and plant diversity would decrease (e.g., Nuñez and Howe 2007). On the other hand, it is possible that a reduction in the rate of seed dispersal may increase plant diversity when seeds of highly competitive species fail to reach adequate regeneration sites and therefore fail to outcompete inferior species (e.g. Tuomisto et al. 1995, Hubbell et al. 1999, Wright 2002).

However, there have been only few studies addressing the role of seed dispersal agents on plant regeneration and diversity patterns (Harms et al. 2000, Nuñez and Howe 2007). Despite that animals disperse a large proportion of the seeds in trees of tropical humid forests (Chapman 1995), it is difficult to predict the ecological effects caused by the reduction or extinction of some groups of dispersers.

Some plant species are known to have a limited number of seed dispersal agents. For example, large seeded endozoochorus plants rely on a few large frugivore species for dispersal (Janson 1983, Peres and van Roosmalen 2002, Stevenson 2007). Even in these plant species it is difficult to predict the effect of a population decrease in large dispersers due to the likelihood of concurrent compensation processes taking place.

Compensation was first defined as "a community level phenomenon where a decrease in the abundance of a species is counterbalanced by an increase in the density of potentially competing species" (Mac Arthur et al. 1972). Peres and Dolman (2000) presented evidence of density compensation in Neotropical primates in forests where hunting on large species was associated with population increase of medium sized monkeys. However, there are few studies addressing the effects of density compensation on ecological processes like frugivory, seed dispersal, and plant recruitment (Bleher and Bohning-Gaese 2001, Poulsen et al. 2002, Cordeiro and Howe 2003, Moran et al. 2004, Stevenson et al. 2005a). When large primates are heavily hunted and the population size of smaller primates increases, it is possible that some plant species will not reach an ecological compensation in terms of seed dispersal, because small animals might not fulfill the role of larger animals (e.g. Peres and Roosmalen 2002, Stevenson et al. 2005a, Nuñez and Howe 2007).

The main aims of this study were: first, to evaluate the existence of density compensation (in terms of population size) in primate communities in two sites with different levels of hunting pressure in Amacayacu National Park, Colombia (Van Leijsen and Vleut 2005). Second, to test the existence of a relationship between hunting of primates and seed removal. Third, to estimate the compensatory effects for seed removal and regeneration, in two canopy species, Apeiba aspera Aubl (Malvacea: Tilioidae) and Hymenaea oblongifolia Huber (Fabaceae: Caesalpinoidea), comparing two sites with different levels of hunting pressure. Small seeds of A. aspera are more likely to germinate in gaps, due to light requirements (Stevenson 2006), therefore we focused in particular on seed removal rates and observations on the recruitment of seedlings and saplings near and far from parental plants, as well as in canopy gaps. Finally, our main aim was to quantify the diversity of plants regenerating in areas of contrasting hunting pressure.

It is known that population densities of large primates in general are reduced in heavily hunted areas (Peres 1999a, Peres and Palacios 2007). Based on previous studies in the zone (Van Leijsen and Vleut 2005), we hypothesized that hunting pressure near human settlements would affect primate community composition in such a way that the density of large primates would be reduced, whereas the density of medium and small sized primates (lesshunted) (Redford and Robinson 1987) should increase due to density compensation (Peres and Dolman 2000, Peres and Palacios 2007). Whenever this density compensation occurs, it is also possible to expect compensation in ecological roles. This pattern may vary depending on life history traits of plant species, such as seed size. In particular, small seeded species (e.g. A. aspera) would be more likely to show compensation in seed removal rates than large seeded species (e.g. H. oblongifolia), since small seeds can be swallowed by medium and small primates species. Given that large ateline primates are important seed dispersers (Andresen 1999, Stevenson 2000, Russo et al. 2004, Dew 2005, Link and DiFiore 2006) there should be low seed dispersal rates in areas of high hunting pressure.

Finally, according to the dispersal limitation hypothesis (Hubbell et al. 1999), when seeds of highly competitive species fail to reach adequate regeneration sites and therefore fail to outcompete less competitive species, higher plant diversity is expected in places with high dispersal rates of competitive species. Therefore, assuming that large primates are efficient dispersers of this kind of seeds, it should be expected to find higher plant diversity in severely hunted places (i.e., without large primates) than in locations where large primates are common. In contrast, when negative density dependent effects in seedlings are very strong, no-recruitment may be expected for some plant species in the absence of large primate dispersers. Therefore, higher plant diversities would be encountered in areas with high seed dispersal rates (i.e. with large primates).

Study site: This study was undertaken during twelve months, between June – September 2003, June – November 2005 and February- March 2006, in Amacayacu National Park, in the Colombian Amazon (3º02’–3º47’S, 69º54’–70º25’W). Annual mean temperature is 26º C, average relative humidity 86%, and annual mean rainfall in the closest city is 3200 mm (Rudas et al. 2005). The study was carried out in three sites located on terra firme forests with similar climatic conditions, and with two comparative levels of hunting pressure. Two sites were situated 8 km away from the Indigenous communities, the other near the visiting centre of Amacayacu National Park, which is located adjacent to two human communities (San Martin de Amacayacu and Mocagua). There is a large history of human occupancy near the visitor’s centre, on the border of the Amazon River. Hunting occurs at the sites 8 km away from the centre, but it is less frequent than at sites nearby human populations. Communities generally hunt up to 10 km from their villages (Peres and Palacios 2007). Based on field data and interviews Van Leijsen and Vleut (2005) reported that hunting pressure and its frequency in the close vicinity of the community of Mocagua in the past was much more severe than nowadays, reducing or exterminating most of the larger body sized animals close to settlements.

Primates Census: We used line transects to quantify the abundance of primates and other diurnal mammals (Burnham et al. 1980, Buckland et al. 1993, Peres 1999b). Transects varied in length, with an average of 3.95 ± 1.31 km. Total sample length was 190.3 km in less hunted places and 90.8 km in the site near communities. The transects were walked at 1.5 km/hour, between 6 am – 10 am and 2 pm -5 pm, during 9 days/transect in average, in the sites far from communities, and 8 days/ transect in average, in the site near communities. For each encounter with mammals during censuses we noted perpendicular distance from first animal detected to trail, species identity, and approximate group size. Population density was calculated for each species using King´s method (Krebs 1999):

D = n / (2a)L,

Where the density (D) is a function of the number of animals (n) seen in the trail, total transect length (L), and the mean perpendicular distance (a). We used King´s method, because the number of encounters with some primate species was not enough to employ distance sampling approaches. For further analysis, primate species were grouped in three categories of size: 1. large (5 kg or more): Lagothrix lagotricha and Alouatta seniculus; 2. medium (1 -5 kg): Callicebus torquatus, Pithecia monachus and Cebus albifrons; and 3. small (<1 kg): Saguinus spp. and Saimiri sciureus.

Plant Diversity: Plots of 4 m² were placed to quantify seedlings and herbs (without DBH or DBH < 1cm) (Duncan and Chapman 2003). Plots of 25 m² were set up to quantify saplings (DBH between 1-5 cm) (Stevenson 2006). To evaluate plant diversity, 114 seedling plots and 111 sapling plots were placed in the proximity of human communities. In the distant site, 100 plots were set up for both seedlings and saplings. The plots were located at each side (randomly) of some of the transects used for primate censuses, every 25 m. Plant species or morpho-species were identified, and diversity estimated using species richness, number of species per stem, and Fisher’s diversity index.

Study Species: Seed removal and the escape and colonization hypotheses were evaluated for Apeiba aspera and Hymenaea oblongifolia. The species were chosen due to fruit characteristics and fruit availability (low availability of other fruits). Both species have a mammal dispersal syndrome, without bright color, relatively large, and protected with a hard husk (Janson 1983). The husk limits the access to pulp and seeds by frugivorous birds and their fruits are eaten mainly by capuchins, howler, and woolly monkeys (Stevenson et al. 2000). The study species had different seed size, being larger in H. oblongifolia (X = 1.4 seeds/fruit; 1.8-2.1 cm. length, 0.8-1.3 cm width) and smaller in A. aspera (X = 166.8 seeds/fruit; 0.2–0.3 cm length) (Stevenson et al. 2000).

Seed Removal: Fruit and seed traps.

To assess seed removal, five fruit traps (1m²) were set up at 1.5 m above ground level, under each of six trees of each species. Traps were checked every 15 or 30 days during the fruit crop to quantify and classify its contents (empty husks, whole fruits and seeds). Seed removal rates were estimated as the percentage of seeds going away from parental crowns, based on the total number of fruits produced by the tree, the mean number of seeds per fruit, and the number of seeds found in traps:

SR = 100-(Total number of seeds in traps*100/Total number of seeds produced)

Plant Regeneration Plots: In order to quantify regeneration of the two focal species, we used plots for seedlings and saplings (4 m² and 25 m² respectively) on six transects per tree. At each transect we set three stations, one at 2 m, one at 10 m and one at 50 m away from 20 trees of H. oblongifolia and 24 trees of A. aspera. Overall, we placed 540 plots around H. oblongifolia trees and 648 plots for A. aspera in forests near the indigenous communities, and the same distance away from them. Plots of the same size (4 m² and 25 m²) were used in natural gaps defined by a fallen tree. We quantified regeneration in gaps due to light requirements of A. aspera which is a pioneer species with very small seeds (Stevenson 2006). The gaps were a few years old (communication from local assistants). The sampling area used to quantify the regeneration in gaps was 200 m² for seedlings and 1250 m² for saplings (50 plots of each size near and far from human settlements).

Statistical Methods: A non- parametric test was used to compare primate densities, due to the lack of normal distributions (Kolmogrov– Smirnov normality test). A G test was performed using Poptools Software (Hood 2000), to assess the relationship between the number of encounters with primates of three different size categories and study site (near or far from human settlements). A comparison for diversity indexes was performed between study sites using either Mann Whitney or T tests. Seed removal results (average ± SD) for each species were subjected to normality test and then were compared using an ANOVA test on SPSS10.0 software.

Results

Primate Censuses: Large primate species were not seen in forests near indigenous communities. In forests far from the communities, they were observed at low densities (6.23 ± 5.15 individuals/km², Fig. 1). The opposite pattern was observed for small primates, which had a higher density in forests near indigenous communities than in forests further away (65.22 ± 6.88 vs 32.07 ± 16.9 individuals/km², Table 1). Differences on total density between places were non significant (Z = -0.74, p = 0.94), but differences between size categories were observed (X² = 44.9, p < 0.001) (Fig. 1A). A G-test on primate group encounter frequency between size categories showed similar results. The encounter rate of large and small primates was significantly associated to sites (near or far from indigenous communities) (G_w = 10.36, p = 0.006, Fig. 1B). Medium sized primates showed no contrasting patterns between sites (Table 1).

Seed Removal: Seed removal rates for A. aspera were higher in places with higher density of large primates (far: 0.48 ± 0.2; near: 0.11 ± 0.18, t = -3.48, p = 0.005) (Fig. 3A). In contrast, seed removal rates for H. oblongifolia were not significantly different between both forests (near: 0.36 ± 0.25 vs. far: 0.17 ± 0.19; t = 1.45, p = 0.18) (Fig. 3B).

A. aspera seedlings were found exclusively in gaps (Table 2) and sapling density in this species was higher at 50 m than at 2 m from parental tree (X_saplings = 0.008 ± 0.015, X² = 7.5, p = 0.02). The density of H. oblongifolia seedlings was higher at 2 m from parental tree and lower at 50 m (Table 2, (X² = 24.7, p < 0,001). In contrast, sapling density was higher at 50 m than at 2 m from parental tree (X² = 7.3, p = 0.03).

Acknowledgments

We thank the Amacaycu National Park staff and the indigenous communities of Mocagua, San Martin de Amacayacu, Zaragoza and Macedonia, where the field work was done and also the indigenous research group who collaborated with data collection. We thank "The Woolly Monkey Project" for its participation in this research and Angela Parrado for her collaboration during this investigation. We thank Daniel Cadena, Julian Palomino, and the CIEM students for their comments and contributions to the final version of this manuscript. The research was founded by Tropenbos Fundation and La Facultad de Ciencias and el Departamento de Biología de la Universidad de los Andes.

Resumen

La cacería ha tenido fuertes efectos en algunas poblaciones de frugívoros y dispersores de semillas, lo cual en consecuencia puede afectar los patrones de diversidad de plantas y regeneración del bosque. Sin embargo, es posible que extinciones locales promuevan el incremento de otras especies, que pueden o no compensar roles ecológicos. El principal objetivo de este estudio fue examinar la posibilidad de compensación por densidad en las comunidades de primates y sus posibles efectos sobre la diversidad de plántulas y juveniles, así como también la remoción de semillas de dos árboles (Apeiba aspera e Hymenaea oblongifolia). El trabajo fue realizado en el Parque Nacional Natural Amacayacu (Amazonas – Colombia). Hicimos censos de mamíferos usando transectos lineales en dos bosques con diferentes presiones de cacería. Además, levantamos parcelas de vegetación para plántulas y juveniles (4 m² y 25 m² respectivamente), y ubicamos trampas de frutos bajo al menos seis árboles de cada especie, en cada bosque, para estimar la remoción de semillas. Los encuentros con primates grandes fueron menos frecuentes en bosques cerca de las comunidades indígenas, mientras que para los primates pequeños el patrón fue contrario, sugiriendo un efecto de compensación por densidad. Por otra parte, la diversidad de plántulas y juveniles fue más alta en bosques donde la densidad de primates grandes es mayor. La remoción de semillas fue mayor en bosques con mayor densidad de primates grandes para A. aspera, pero para H. oblongifolia las diferencias entre bosques no fueron significativas. En general, los resultados de este estudio apoyan la hipótesis de compensación por densidad en la comunidad de primates, sin embargo, no hay evidencia fuerte de compensación ecológica en términos de dispersión de semillas y regeneración. Finalmente, la presencia de dispersores grandes (ej. Lagothrix lagothricha) estuvo asociada con una mayor diversidad de plantas.

Received 30-V-2007. Corrected 21-XII-2007. Accepted 31-III-2008.

References

Andresen, E. 1999. Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest. Biotropica 31: 145-158.         [ Links ]

Beckman, N. & H. C. Muller-Landau. 2007. Differential effects of hunting on pre-dispersal seed predation and primary and secondary seed removal of two Neotropical tree species. Biotropica 39: 328–339.         [ Links ]

Bleher, B. & K. Bohning-Gaese. 2001. Consequences of frugivore diversity for seed dispersal, seedling establishment and the spatial pattern of seedlings and trees. Oecologia 129:385-394.         [ Links ]

Buckland, S.T., D.A. Elston. 1993. Empirical models for the spatial distribution of wildlife. J. appl ecol. 30: 478-495.         [ Links ]

Burnham, K.P., D.R. Anderson & J.L. Laake.. 1980. Estimation of density from line transect sampling of biological populations. Wildlife Monographs 7-202.         [ Links ]

Chapman, C.A. 1995. Primate seed dispersal: coevolution and conservation implications. Evolutionary Anthropology 4: 74-82.         [ Links ]

Cordeiro, N.J. & H.F. Howe. 2003. Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. PNAS-USA 100: 1405214056.         [ Links ]

Connell, J.H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. p. 298-312 In P.J. den Boer & G.R. Gradwell, (eds). Dynamics of populations. Pudoc, Wageningen, Holland.         [ Links ]

Defler, T.R. 2001. Diversity and abundance of species in eastern Colombia. Memories of the XVIII th Congress of the International Primatological Society. Adelaide, Australia.         [ Links ]

Dew, J.L. 2005. Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth. Int. j. Primatol. 26: 1107-1135.         [ Links ]

Duncan, R.S. & C.A. Chapman. 2003. Consequences of plantation harvest during tropical forest restoration in Uganda. Forest Ecol. Manag. 173: 235-250.         [ Links ]

Muller-Landau, H.C. 2007. Predicting the long-term effects of hunting on plant species composition and diversity in tropical forests. Biotropica 39: 372–384.         [ Links ]

Garber, P.A. 1986. The ecology of seed dispersal in 2 species of callitrichid primates (saguinus mystax and saguinus fuscicollis). Am. J. primatol. 10: 155-170.         [ Links ]

Ganzhorn. J.U., P.P. Lowry II, E.G. Schatz, S. Sommer. 2001. The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx 35: 346-348.         [ Links ]

Gentry, A.H. 1988. Changes in Plant Community Diversity and Floristic Composition On Environmental and Geographical Gradients. Ann. Missouri Bot. Garden 75: 1-34.         [ Links ]

Guariguata, M.R. & M.A. Pinard. 1998. Ecological knowledge of regeneration from seed in neotropical forest trees: implications for natural forest management. Forest Ecol. Manag.112: 87-99.         [ Links ]

Guillotin, M., G. Dubost & D. Sabatier. 1994. Food Choice and Food Competition Among the 3 Major Primate Species of French-Guiana. J. Zool. 233: 551-579.         [ Links ]

Harms, K.E., S.J. Wright, O. Calderon, A. Hernandez & E.A. Herre. 2000. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404: 493-495.         [ Links ]

Howe, H.F. & J. Smallwood. 1982. Ecology of seed dispersal. Ann. Rev ecolog. Syst. 13: 201-218.         [ Links ]

Hubbell, S.P., R.B. Foster, S.T. O’brien, K.E. Harms, R. Condit, B. Wechsler, S.J. Wrightand S.L.de lao, 1999. Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283: 554-557.         [ Links ]

Janson, C.H. 1983. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219: 187-189.         [ Links ]

Janzen, D.H. 1970. Herbivores and the number of tree species in tropical forests. Am. nat. 104: 501-528.         [ Links ]

Krebs, C.J. 1999. Ecological Methodology. Addison-Welsey, San Francisoc, California, U.S.A.         [ Links ]

Link, A. & A. Di Fiore. 2006. Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. J. Trop. Ecol. 22: 235-246.         [ Links ]

Maldonado, A.M. 2007. The Woolly Monkey Project: Status and conservation of Primates in Amacayacu National Park, Colombian Amazon: A community based research project. Woolly Monkey Project:, Bogotá.         [ Links ]

McArthur, R.H. 1972. Density compensation in island faunas. Ecology 53: 330.         [ Links ]

Moran, C., C.P. Catterall, R.J. Green & M.F. Olsen. 2004. Functional variation among frugivorous birds: implications for rainforest seed dispersal in a fragmented subtropical landscape. Oecologia 141: 584-595.         [ Links ]

Nuñez-Iturri, G. & H. F. Howe. 2007. Bushmeat and the fate of trees with seeds dispersed by large primates in a lowland rainforest in western Amazonia. Biotropica 39: 348-354.         [ Links ]

Peres, C.A. 1999a. Effects of subsistence hunting and forest types on the structure of amazonian primate communities. p. 268-283 In, J.G. Fleagle, C.H. Janson & K.E. Reed, (eds.). Primate Communities. Cambridge University, Cambridge, United Kingdom.         [ Links ]

Peres, C. 1999b. General guidelines for standardized line-transect surveys of tropical forest primates. Neotrop. Primates 7:11-16.         [ Links ]

Peres, C.A. & P.M. Dolman. 2000. Density compensation in neotropical primate communities: evidence from 56 hunted and nonhunted amazonian forests of varying productivity. Oecologia 122: 175-189.         [ Links ]

Peres, C.A. & M. Van Roosmalen. 2002. Primate frugivory in two species-rich neotropical forests: implications for the demography of large-seeded plants in over-hunted areas. pp. 407-421 In Levey, D.J., W.R. Silva & M. Galetti. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CAB, London         [ Links ]

Peres, C.A. & E. Palacios. 2007. Basin-Wide effects of Game Harvest on Vertebrate Population Densities in Amazonian Forests: Implications for Animal-Mediated Seed Dispersal. Biotropica 39: 304-315.         [ Links ]

Poulsen, J.R., C.J. Clark, E.F. Connor & T.B. Smith. 2002. Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 83: 228-240.         [ Links ]

Redford, K.H. & J.G. Robinson. 1987. The game of choice -patterns of indian and colonist hunting in the neotropics. Am. Anthropol 89:650-667.         [ Links ]

Rudas, A., A. Prieto Cruz, C.M. Taylor & R. Ortiz. 2005. Flórula del Parque Nacional Natural Amacayacu, Amazonas, Colombia. Missouri Botanical Garden, Saint Louis, Missouri, USA         [ Links ]

Russo, S.E. & C.K. Augspurger. 2004. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol. Lett. 7: 1058-1067.         [ Links ]

Schupp, E., T. Milleron & S.E. Russo. 2002. Dissemination limitation and the origin and maintenance of species-rich tropical forests. p. 17-33 In D.J. Levey, W.R.

Silva & M. Galetti (eds.). Seed dispersal and frugivory: ecology, evolution, and conservation, New York, USA.

Silman, M.R., J.W. Terborgh & R.A. Kiltie. 2003. Population regulation of a dominant-rain forest tree by a major seed-predator. Ecology 84: 431-438.         [ Links ]

Stevenson, P.R. 2000. Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: dispersal distance, germination rates, and dispersal quantity. Am. J. primatol. 50: 275-289.         [ Links ]

Stevenson, P.R. 2002. Frugivory and seed dispersal by woolly monkeys at Tinigua National Park, Colombia. PhD Thesis. State University of New York at Stony Brook, New York, USA p. 411.         [ Links ]

Stevenson P.R. 2006. A test of the escape and colonization hypotheses for zoochorous tree species in a Western Amazonian forest. Plant Ecology DOI 10.1007/ s11258-006-9205-5.         [ Links ]

Stevenson, P.R. 2007. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. p. 340-362. In A. J. Dennis, E.W., Schupp, R. J. Green & D. W. Westcott (eds). Seed dispersal: theory and its application in a changing world. Wallingford, United Kingdom.         [ Links ]

Stevenson, P.R., Quiñones, M.J. & Ahumada, J. 2000. Influence of fruit availability on ecological overlap among four neotropical primates at Tinigua National Park, Colombia. Biotropica 32: 533-544.         [ Links ]

Stevenson, P.R., M. Pineda & T. Samper. 2005a. Influence of seed size on dispersal probabilities by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia. Oikos 110: 435-440.         [ Links ]

Stevenson, P.R., A. Link. & B.H. Ramirez. 2005b. Frugivory and seed fate in Bursera inversa (Burseraceae) at Tinigua Park, Colombia: implications for primate conservation. Biotropica 37: 431-438.         [ Links ]

Stoner, K.E., P. Riba-Hernández, K. Vulinec & J.E. Lambert. 2007. The role of mammals in tropical forest regeneration and some possible consequences of their elimination: An overview. Biotropica 39: 316-327.         [ Links ]

Terborgh, J. 1983. Five new world primates. A study on comparative ecology. Princeton University, Princeton New Jersey, USA p. 260.         [ Links ]

Terborgh J, N. Pitman M. Silman, H. Schicheter & V.P. Nuñez 2002. Maintenance of tree diversity in tropical forests. p. 1-17. In Seed dispersal and frugivory: Ecology, Evolution and Conservation . Levey DJ, Silva WR and Galetti M (eds), Oxford University, London, United Kingdom.         [ Links ]

Ter Steege, H., N. Pitman, D. Sabatier, H. Castellanos, P. Van der Hout, D.C. Daly, M. Silveira, O. Phillips, R. Vasquez, T. Van Andel, J. Duivenvoorden, A.A. De Oliveira, R. Ek, . Lilwah, R. Thomas, J. Van Essen, C. Baider, P. Maas, S. Mori, J. Terborgh, P.N. Vargas, H. Mogollon, & W. Morawetz. 2003. A spatial model of tree alpha-diversity and tree density for the Amazon. Biodiv. Conserv. 12: 2255-2277.         [ Links ]

Tuomisto, H., K. Ruokolainen, R. Kalliola, A. Linna, W. Danjoy & Z. Rodriguez 1995. Dissecting amazonian biodiversity. Science 269: 63-66.         [ Links ]

Van Leijsen Jeroen & Vleut Ivar. 2005. Impact of an indigenous community on the woolly monkey (lagothrix lagothrichia) and 7 other primate species in the amazonian rainforest, Colombia. MsC Thesis. Wageningen University, The Netherlands.         [ Links ]

Webb C.O. & D.R. Peart. 2001. High seed dispersal rates in faunally intact rain forest: theoretical and conservation implications. Ecology Letters 4: 491-499.         [ Links ]

Wills, C., R. Condit, R.B. Foster & S.P. Hubbell. 1997. Strong density- and diversity-related effects help to maintain tree species diversity in a neotropical forest. PNAS-USA 94: 1252-1257.         [ Links ]

Wright, J.S. 2002. Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130: 1-14.         [ Links ]