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Primate Seed Dispersal: Old and New Challenges

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Abstract

Primate seed dispersal plays crucial roles in many ecological processes at various levels of biological organization: from plant population genetics and demography to community assembly and ecosystem function. Although research on primate seed dispersal has advanced significantly in the last 20–30 years, many aspects are still poorly understood. Here, we discuss some new challenges that we need to address, as well as some old ones that still need our attention, highlighting examples from the Neotropics. Despite new analytical tools from network theory, research on primate seed dispersal rarely takes a community-wide approach, thus limiting our understanding of its evolutionary, ecological, and conservation implications. Of particular relevance for conservation are changes caused by landscape-scale processes (e.g., forest loss and fragmentation), but these effects need to be assessed using a landscape approach, which is currently absent in primate seed dispersal research. Agroecosystems can play a key role in maintaining primate seed dispersal in anthropogenic landscapes, but this topic remains poorly studied. Primate seed dispersal research will need to play a role in refaunation projects aimed at restoring plant–animal interactions. Old challenges that we still need to address include the long-term effects of primate declines on plant populations and communities, and the role of primate seed dispersal in the regeneration of degraded habitats. If we take advantage of all tools provided by modern science, from powerful methods of data analyses to molecular techniques, and combine them with strong multidisciplinary collaborations, the future of primate seed dispersal research will indeed be exciting.

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Data Availability

The database generated during our literature review is available from the corresponding author on reasonable request.

References

  • Albert, A., McConkey, K., Savini, T., & Huynen, M.-C. (2014). The value of disturbance-tolerant cercopithecine monkeys as seed dispersers in degraded habitats. Biological Conservation, 170, 300–310.

    Article  Google Scholar 

  • Albert, A., Savini, T., & Huynen, M.-C. (2013). The role of Macaca spp. (primates Cercopithecidae) in seed dispersal networks. The Raffles Bulletin of Zoology, 61, 423–434.

    Google Scholar 

  • Almeida-Rocha, J. M., Peres, C. A., & Oliveira, L. C. (2017). Primate responses to anthropogenic habitat disturbance: a pantropical meta-analysis. Biological Conservation, 215, 30–38.

    Article  Google Scholar 

  • Andresen, E. (2000). Ecological roles of mammals: The case of seed dispersal. In A. Entwistle & N. Dunstone (Eds.), Priorities for the conservation of mammalian diversity: Has the panda had its day? (pp. 11–26). Conservation Biology 3 Cambridge: Cambridge University Press.

  • Andresen, E., Arroyo-Rodríguez, V., & Escobar, F. (2018). Tropical biodiversity: The importance of biotic interactions for its origin, maintenance, function, and conservation. In W. Dáttilo & V. Rico-Gray (Eds.), Ecological networks in the tropics. (pp. 1–13). New York: Springer Science+Business Media.

  • Andresen, E., & Levey, D. J. (2004). Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia, 139, 45–54.

    Article  PubMed  Google Scholar 

  • Anzures-Dadda, A., Manson, R. H., Andresen, E., & Martínez, M. L. (2016). Possible implications of seed dispersal by the howler monkey for the early recruitment of a legume tree in small rain-forest fragments in Mexico. Journal of Tropical Ecology, 32, 340–343.

    Article  Google Scholar 

  • Arroyo-Rodríguez, V., Aguilar-Barajas, E., González-Zamora, A., Rocha-Ramirez, V., González-Rodríguez, A., & Oyama, K. (2017c). Parent–parent and parent–offspring distances in Spondias radlkoferi seeds suggest long-distance pollen and seed dispersal: Evidence from latrines of the spider monkey. Journal of Tropical Ecology, 33, 95–106.

    Article  Google Scholar 

  • Arroyo-Rodríguez, V., Andresen, E., Bravo, S. P., & Stevenson, P. R. (2015). Seed dispersal by howler monkeys: Current knowledge, conservation implications, and future directions. In M. M. Kowalewski, P. A. Garber, L. Cortes-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology and conservation. Developments in primatology: Progress and prospects (pp. 111–139). New York: Springer Science+Business Media.

    Google Scholar 

  • Arroyo-Rodríguez, V., & Dias, P. A. D. (2010). Effects of habitat fragmentation and disturbance on howler monkeys: a review. American Journal of Primatology, 72, 1–16.

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez, V., & Fahrig, L. (2014). Why is a landscape perspective important in studies of primates? American Journal of Primatology, 76, 901–909.

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez, V., Melo, F. P., Martínez-Ramos, M., Bongers, F., Chazdon, R. L., et al (2017a). Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biological Reviews, 92, 326–340.

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez, V., Pérez-Elissetche, G. K., Ordóñez-Gómez, J. D., González-Zamora, A., Chaves, Ó. M., et al (2017b). Spider monkeys in human-modified landscapes. Tropical Conservation Science, 10, 1–13.

    Article  Google Scholar 

  • Arroyo-Rodríguez, V., Rös, M., Escobar, F., Melo, F. P. L., Santos, B. A., Tabarelli, M., & Chazdon, R. (2013). Plant β-diversity in fragmented rainforests: testing floristic homogenization and differentiation hypotheses. Journal of Ecology, 101, 1449–1458.

    Article  Google Scholar 

  • Aslan, C. E., Aslan, A., Croll, D., Tershy, B., & Zavaleta, E. (2014). Building taxon substitution guidelines on a biological control foundation. Restoration Ecology, 22, 437–441.

    Article  Google Scholar 

  • Aslan, C. E., Bronstein, J. L., Rogers, H. S., Gedan, K. B., Brodie, J., Palmer, T. M., & Young, T. P. (2016). Leveraging nature's backup plans to incorporate interspecific interactions and resilience into restoration. Restoration Ecology, 24, 434–440.

    Article  Google Scholar 

  • Barnett, A. A., Boyle, S. A., Pinto, L. P., Lourenço, W. C., Almeida, T., Sousa Silva, W., Ronchi-Teles, B., Bezerra, B. M., Ross, C., MacLarnon, A., & Spironello, W. R. (2012). Primary seed dispersal by three Neotropical seed-predating primates (Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus). Journal of Tropical Ecology, 28, 543–555.

    Article  Google Scholar 

  • Bascompte, J., & Jordano, P. (2014). Mutualistic networks. Monographs in population biology 53. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Beck, B. B. (2017). A history of primate reintroduction. Retrieved from www.drbenjaminbeck.com.

  • Beier, P., & Noss, R. F. (1998). Do habitat corridors provide connectivity? Conservation Biology, 12, 1241–1252.

    Article  Google Scholar 

  • Bialozyt, R., Flinkerbusch, S., Niggemann, M., & Heymann, E. W. (2014). Predicting the seed shadows of a Neotropical tree species dispersed by primates using an agent-based model with internal decision making for movements. Ecological Modelling, 278, 74–84.

    Article  Google Scholar 

  • Blanco, V., & Waltert, M. (2013). Does the tropical agricultural matrix bear potential for primate conservation? A baseline study from western Uganda. Journal for Nature Conservation, 21, 383–393.

    Article  Google Scholar 

  • Brodie, J. F., & Aslan, C. E. (2012). Halting regime shifts in floristically intact tropical forests deprived of their frugivores. Restoration Ecology, 20, 153–157.

    Article  Google Scholar 

  • Bueno, R. S., Guevara, R. G., Ribeiro, M. C., Culot, L., Bufalo, F. S., & Galetti, M. (2013). Functional redundancy and complementarities of seed dispersal by the last neotropical megafrugivores. PLoS One, 8, e56252.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bufalo, F. S., Galetti, M., & Culot, L. (2016). Seed dispersal by primates and implications for the conservation of a biodiversity hotspot, the Atlantic forest of South America. International Journal of Primatology, 37, 333–349.

    Article  Google Scholar 

  • Calle-Rendón, B. R., Peck, M., Bennett, S. E., Morelos-Juarez, C., & Alfonso, F. (2016). Comparison of forest regeneration in two sites with different primate abundances in northwestern Ecuador. Revista de Biología Tropical, 64, 493–506.

    Article  PubMed  Google Scholar 

  • Campbell-Smith, G., Simanjorang, H. V. P., Leader-Williams, N., & Linkie, M. (2010). Local attitudes and perceptions toward crop-raiding by orangutans (Pongo abelii) and other nonhuman primates in northern Sumatra, Indonesia. American Journal of Primatology, 72, 866–876.

    Article  PubMed  Google Scholar 

  • Chanthorn, W., Wiegand, T., Getzin, S., Brockelman, W. Y., & Nathalang, A. (2017). Spatial patterns of local species richness reveal importance of frugivores for tropical forest diversity. Journal of Ecology. https://doi.org/10.1111/1365-2745.12886.

  • Chapman, C. A. (1989). Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21, 148–154.

    Article  Google Scholar 

  • Chapman, C. A. (1995). Primate seed dispersal: coevolution and conservation implications. Evolutionary Anthropology, 4, 74–82.

    Article  Google Scholar 

  • Chapman, C. A., & D. A. Onderdonk. (1998). Forests without primates: primate/plant codependency. American Journal of Primatology 45:127–142.

  • Chapman, C. A., & Russo, S. E. (2006). Primate seed dispersal: Linking behavioral ecology with forest community structure. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & K. Bearder (Eds.), Primates in perspective (pp. 510–525). Oxford: Oxford University Press.

    Google Scholar 

  • Chaves, O. M., Arroyo-Rodríguez, V., Martínez-Ramos, M., & Stoner, K. E. (2015). Primate extirpation from rainforest fragments does not appear to influence seedling recruitment. American Journal of Primatology, 77, 468–478.

    Article  PubMed  Google Scholar 

  • Chaves, O. M., Stoner, K. E., Arroyo-Rodríguez, V., & Estrada, A. (2011). Effectiveness of spider monkeys (Ateles geoffroyi vellerosus) as seed dispersers in continuous and fragmented rainforests in southern Mexico. International Journal of Primatology, 32, 177–192.

    Article  Google Scholar 

  • Clark, C. J., Poulsen, J. R., & Parker, V. T. (2001). The role of arboreal seed dispersal groups on the seed rain of a lowland tropical forest. Biotropica, 33, 606–620.

    Article  Google Scholar 

  • Cohen, E. B., Pearson, S. M., & Moore, F. R. (2014). Effects of landscape composition and configuration on migrating songbirds: inference from an individual-based model. Ecological Applications, 24, 169–180.

    Article  PubMed  Google Scholar 

  • Cordeiro, N. J., & Howe, H. F. (2001). Low recruitment of trees dispersed by animals in African forest fragments. Conservation Biology, 15, 1733–1741.

    Article  Google Scholar 

  • Corlett, R. (2007). Pollination or seed dispersal: Which should we worry about most? In A. J. Dennis, E. W. Schupp, R. J. Green, & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 523–543). Wallingford: CABI.

    Chapter  Google Scholar 

  • Corlett, R. T. (2002). Frugivory and seed dispersal in degraded tropical east Asian landscapes. In D. J. Levey, W. R. Silva, & M. Galetti (Eds.), Seed dispersal and frugivory: Ecology, evolution and conservation (pp. 451–465). Wallingford: CABI.

    Google Scholar 

  • Corlett, R. T. (2017). Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: An update. Global Ecology and Conservation, 11, 1–22.

    Article  Google Scholar 

  • Correia, M., Timóteo, S., Rodríguez-Echeverría, S., Mazars-Simon, A., & Heleno, R. (2017). Refaunation and the reinstatement of the seed-dispersal function in Gorongosa national park. Conservation Biology, 31, 76–85.

    Article  PubMed  Google Scholar 

  • Culot, L., Bello, C., Batista, J. L. F., do Couto, H. T. Z., & Galetti, M. (2017). Synergistic effects of seed disperser and predator loss on recruitment success and long-term consequences for carbon stocks in tropical rainforests. Scientific Reports, 7, 7662.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Culot, L., Huynen, M. C., & Heymann, E. W. (2015). Partitioning the relative contribution of one-phase and two-phase seed dispersal when evaluating seed dispersal effectiveness. Methods in Ecology and Evolution, 6, 178–186.

    Article  Google Scholar 

  • Culot, L., Lazo, F. J. J. M., Huynen, M.-C., Poncin, P., & Heymann, E. W. (2010). Seasonal variation in seed dispersal by tamarins alters seed rain in a secondary rain forest. International Journal of Primatology, 31, 553–569.

    Article  PubMed  PubMed Central  Google Scholar 

  • de A. Moura, A. C., Cavalcanti, L., Leite-Filho, E., Mesquita, D. O., & McConkey, K. R. (2015). Can green iguanas compensate for vanishing seed dispersers in the Atlantic forest fragments of north-east Brazil? Journal of Zoology, 295, 189–196.

    Article  Google Scholar 

  • de Luna, G. A., García-Morera, Y., & Link, A. (2016). Behavior and ecology of the white-footed tamarin (Saguinus leucopus) in a fragmented landscape of Colombia: Small bodied primates and seed dispersal in Neotropical forests. Tropical Conservation Science, 9, 788–808.

    Article  Google Scholar 

  • Dias, P. A. D., & Rangel-Negrín, A. (2015). Diets of howler monkeys. In M. M. Kowalewski, P. A. Garber, L. Cortes-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology and conservation. Developments in primatology: Progress and prospects (pp. 21–56). New York: Springer.

    Google Scholar 

  • Donatti, C. I., Guimarães, P. R., Galetti, M., Pizo, M. A., Marquitti, F., & Dirzo, R. (2011). Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecology Letters, 14, 773–781.

    Article  PubMed  Google Scholar 

  • Effiom, E. O., Birkhofer, K., Smith, H. G., & Olsson, O. (2014). Changes of community composition at multiple trophic levels due to hunting in Nigerian tropical forests. Ecography, 37, 367–377.

    Article  Google Scholar 

  • Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., et al (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3, e1600946.

    Article  PubMed  PubMed Central  Google Scholar 

  • Estrada, A., Raboy, B. E., & Oliveira, L. C. (2012). Agroecosystems and primate conservation in the tropics: A review. American Journal of Primatology, 74, 696–711.

    Article  PubMed  Google Scholar 

  • Fahrig, L. (2002). Effect of habitat fragmentation on the extinction threshold: a synthesis. Ecological Applications, 12, 346–353.

    Google Scholar 

  • Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology and Systematics, 34, 487–515.

    Article  Google Scholar 

  • Fahrig, L. (2013). Rethinking patch size and isolation effects: the habitat amount hypothesis. Journal of Biogeography, 40, 1649–1663.

    Article  Google Scholar 

  • Fahrig, L. (2017). Ecological responses to habitat fragmentation per se. Annual Review of Ecology, Evolution and Systematics, 48, 1–25.

    Article  Google Scholar 

  • Fahrig, L., Baudry, J., Brotons, L., Burel, F. G., Crist, T. O., Fuller, R. J., Sirami, C., Siriwardena, G. M., & Martin, J. L. (2011). Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecology Letters, 14, 101–112.

    Article  PubMed  Google Scholar 

  • Fleming, T. H., & Kress, W. J. (2013). The ornaments of life: Coevolution and conservation in the tropics. Chicago: University of Chicago Press.

    Book  Google Scholar 

  • Fuzessy, L. F., Cornelissen, T. G., Janson, C., & Silveira, F. A. (2016). How do primates affect seed germination? A meta-analysis of gut passage effects on neotropical plants. Oikos, 125, 1069–1080.

    Article  Google Scholar 

  • Fuzessy, L. F., Janson, C. H., & Silveira, F. A. (2017). How far do Neotropical primates disperse seeds? American Journal of Primatology, 79, e22659.

    Article  Google Scholar 

  • Galetti, M., Pires, A. S., Brancalion, P. H. S., & Fernandez, F. A. S. (2017). Reversing defaunation by trophic rewilding in empty forests. Biotropica, 49, 5–8.

    Article  Google Scholar 

  • Garber, P. A., & Lambert, J. E. (1998). Introduction to primate seed dispersal. American Journal of Primatology, 45, 3–8.

    Article  PubMed  CAS  Google Scholar 

  • Gautier-Hion, A., Duplantier, J.-M., Quris, R., Feer, F., Sourd, C., et al (1985). Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 65, 324–337.

    Article  PubMed  CAS  Google Scholar 

  • Gelmi-Candusso, T. A., Heymann, E. W., & Heer, K. (2017). Effects of zoochory on the spatial genetic structure of plant populations. Molecular Ecology, 26, 5896–5910. https://doi.org/10.1111/mec.14351.

    Article  PubMed  Google Scholar 

  • González-Zamora, A., Arroyo-Rodríguez, V., Escobar, F., Rös, M., Oyama, K., Ibarra-Manríquez, G., Stoner, K. E., & Chapman, C. A. (2014). Contagious deposition of seeds in spider monkeys’ sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS One, 9(2), e89346.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haila, Y. (2002). A conceptual genealogy of fragmentation research: from island biogeography to landscape ecology. Ecological Applications, 12, 321–334.

    Google Scholar 

  • Hawes, J. E., & Peres, C. A. (2014). Ecological correlates of trophic status and frugivory in neotropical primates. Oikos, 123, 365–377.

    Article  Google Scholar 

  • Herrera, C. M. (2002). Seed dispersal by vertebrates. In C. M. Herrera & O. Pellmyr (Eds.), Plant–animal interactions: An evolutionary approach (pp. 185–208). Oxford: Blackwell.

    Google Scholar 

  • Heymann, E. W., Culot, L., Knogge, C., Noriega Piña, T. E., Tirado Herrera, E. R., Klapproth, M., & Zinner, D. (2017). Long-term consistency in spatial patterns of primate seed dispersal. Ecology and Evolution, 7, 1435–1441.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hockings, K. J., Yamakoshi, G., & Matsuzawa, T. (2017). Dispersal of a human-cultivated crop by wild chimpanzees (Pan troglodytes verus) in a forest–farm matrix. International Journal of Primatology, 38, 172–193.

    Article  Google Scholar 

  • Holbrook, K. M., & Loiselle, B. A. (2009). Dispersal in a Neotropical tree, Virola flexuosa (Myristicaceae): Does hunting of large vertebrates limit seed removal? Ecology, 90, 1449–1455.

    Article  PubMed  CAS  Google Scholar 

  • Holzschuh, A., Steffan-Dewenter, I., & Tscharntke, T. (2010). How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids? Journal of Applied Ecology, 79, 491–500.

    Article  Google Scholar 

  • Howe, H. F. (1984). Implications of seed dispersal by animals for tropical reserve management. Biological Conservation, 30, 261–281.

    Article  Google Scholar 

  • Jackson, H. B., & Fahrig, L. (2015). Are ecologists conducting research at the optimal scale? Global Ecology and Biogeography, 24, 52–63.

    Article  Google Scholar 

  • Jordano, P. (2014). Fruits and frugivory. In R. S. Gallagher (Ed.), Seeds: The ecology of regeneration in plant communities (pp. 18–61). Wallingford: CABI.

    Chapter  Google Scholar 

  • Jordano, P. (2016). Sampling networks of ecological interactions. Functional Ecology, 12, 1883–1893.

    Article  Google Scholar 

  • Karubian, J., Ottewell, K., Link, A., & Di Fiore, A. (2015). Genetic consequences of seed dispersal to sleeping trees by white-bellied spider monkeys. Acta Oecologica, 68, 50–58.

    Article  Google Scholar 

  • Kunz, B. K., & Linsenmair, E. K. (2010). Fruit removal and seed predation in two African trees (Lannea acida and Lannea welwitschii, Anacardiaceae). West Africa Journal of Applied Ecology, 17, 87–95.

    Google Scholar 

  • Kurten, E. L. (2013). Cascading effects of contemporaneous defaunation on tropical forest communities. Biological Conservation, 163, 22–32.

    Article  Google Scholar 

  • Lambert, J. E. (2001). Red-tailed guenons (Cercopithecus ascanius) and Strychnos mitis: evidence for plant benefits beyond seed dispersal. International Journal of Primatology, 22, 189–201.

    Article  Google Scholar 

  • Lambert, J. E. (2010). Primate frugivory and seed dispersal: Implications for the conservation of biodiversity. Evolutionary Anthropology, 19, 165–166.

    Article  Google Scholar 

  • Lambert, J. E., & Chapman, C. A. (2005). The fate of primate-dispersed seeds: Deposition pattern, dispersal distance and implications for conservation. In P.-M. Forget, J. Lambert, P. Hulme, & S. B. Vander Wall (Eds.), Seed fate: Predation, dispersal and seedling establishment (pp. 137–150). Wallingford: CABI.

    Chapter  Google Scholar 

  • Lambert, J. E., & Garber, P. A. (1998). Evolutionary and ecological implications of primate seed dispersal. American Journal of Primatology, 45, 9–28.

    Article  PubMed  CAS  Google Scholar 

  • Lambert, J. E., & Kaplin, B. A. (2001). New horizons in the ecology of primate seed dispersal. Evolutionary Anthropology, 10, 77–78.

    Article  Google Scholar 

  • Levi, T., & Peres, C. A. (2013). Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biological Conservation, 163, 99–106.

    Article  Google Scholar 

  • López-del-Toro, P., Andresen, E., Barraza, L., & Estrada, A. (2009). Attitudes and knowledge of shade-coffee farmers towards vertebrates and their ecological functions. Tropical Conservation Science, 2, 299–318.

    Article  Google Scholar 

  • Lugon, A. P., Boutefeu, M., Bovy, E., Vaz-de-Mello, F. Z., Huynen, M.-C., Galetti, M., & Culot, L. (2017). Persistence of the effect of frugivore identity on post-dispersal seed fate: consequences for the assessment of functional redundancy. Biotropica, 49, 293–302.

    Article  Google Scholar 

  • Markl, J. S., Schleuning, M., Forget, P.-M., Jordano, P., Lambert, J., et al (2012). Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conservation Biology, 26, 1072–1081.

    Article  PubMed  Google Scholar 

  • Martins, M. M. (2006). Comparative seed dispersal effectiveness of sympatric Alouatta guariba and Brachyteles arachnoides in southeastern Brazil. Biotropica, 38, 57–63.

    Google Scholar 

  • McConkey, K. R., & Brockelman, W. Y. (2011). Nonredundancy in the dispersal network of a generalist tropical forest tree. Ecology, 92, 1492–1502.

    Article  PubMed  Google Scholar 

  • McConkey, K. R., Brockelman, W. Y., & Saralamba, C. (2014). Mammalian frugivores with different foraging behavior can show similar seed dispersal effectiveness. Biotropica, 46, 647–651.

    Article  Google Scholar 

  • McConkey, K. R., & O'Farrill, G. (2016). Loss of seed dispersal before the loss of seed dispersers. Biological Conservation, 201, 38–49.

    Article  Google Scholar 

  • McConkey, K. R., Prasad, S., Corlett, R. T., Campos-Arceiz, A., Brodie, J. F., Rogers, H., & Santamaria, L. (2012). Seed dispersal in changing landscapes. Biological Conservation, 146, 1–13.

    Article  Google Scholar 

  • Menke, S., Böhning-Gaese, K., & Schleuning, M. (2012). Plant–frugivore networks are less specialized and more robust at forest–farmland edges than in the interior of a tropical forest. Oikos, 121, 1553–1566.

    Article  Google Scholar 

  • Muñoz-Lazo, F. J. J., Culot, L., Huynen, M.-C., & Heymann, E. W. (2011). Effect of resting patterns of tamarins (Saguinus fuscicollis and Saguinus mystax) on the spatial distribution of seeds and seedling recruitment. International Journal of Primatology, 32, 223–237.

    Article  PubMed  Google Scholar 

  • Norconk, M. A., Grafton, B. W., & Conklin-Brittain, N. L. (1998). Seed dispersal by neotropical seed predators. American Journal of Primatology, 45, 103–126.

    Article  PubMed  CAS  Google Scholar 

  • Norden, N., & Stevenson, P. R. (2015). Influence of frugivore activity on the species abundance of seedlings and saplings in a lowland tropical forest in Colombia. Journal of Tropical Ecology, 31, 291–303.

    Article  Google Scholar 

  • Nuñez-Iturri, G., Olsson, O., & Howe, H. F. (2008). Hunting reduces recruitment of primate-dispersed trees in Amazonian Peru. Biological Conservation, 141, 1536–1546.

    Article  Google Scholar 

  • Oliveira, A. C. M., & Ferrari, S. F. (2000). Seed dispersal by black-handed tamarins, Saguinus midas niger (Callitrichinae, Primates): Implications for the regeneration of degraded forest habitats in eastern Amazonia. Journal of Tropical Ecology, 16, 709–716.

    Article  Google Scholar 

  • Ordóñez-Gómez, J. D., Arroyo-Rodríguez, V., Nicasio-Arzeta, S., & Cristóbal-Azkarate, J. (2015). Which is the appropriate scale to assess the impact of landscape spatial configuration on the diet and behavior of spider monkeys? American Journal of Primatology, 77, 56–65.

    Article  PubMed  Google Scholar 

  • Pacheco, L. F., & Simonetti, J. A. (2000). Genetic structure of a mimosoid tree deprived of its seed disperser, spider monkey. Conservation Biology, 14, 1766–1775.

    Article  Google Scholar 

  • Peres, C. A., & Dolman, P. M. (2000). Density compensation in neotropical primate communities: evidence from 56 hunted and nonhunted Amazonian forest of varying productivity. Oecologia, 122, 175–189.

    Article  PubMed  CAS  Google Scholar 

  • Peres, C. A., Emilio, T., Schietti, J., Desmoulière, S. J. M., & Levi, T. (2016). Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proceedings of the National Academy of Sciences of the USA, 113, 892–897.

    Article  PubMed  CAS  Google Scholar 

  • Perfecto, I., & Vandermeer, J. (2008). Biodiversity conservation in tropical agroecosystems. Annals of the New York Academy of Sciences, 1134, 173–200.

    Article  PubMed  Google Scholar 

  • Phalan, B., Onial, M., Balmford, A., & Green, R. E. (2011). Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science, 333, 1289–1291.

    Article  PubMed  CAS  Google Scholar 

  • Phiphatsuwannachai, S., Westcott, D. A., McKeown, A., & Savini, T. (2017). Inter-group variability in seed dispersal by white-handed gibbons in mosaic forest. Biotropica, 50, 106–115. https://doi.org/10.1111/btp.12499.

    Article  Google Scholar 

  • Pizo, M. A. (2007). Frugivory by birds in degraded areas of Brazil. In A. J. Dennis, E. W. Schupp, R. J. Green, & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 615–627). Wallingford: CABI.

  • Poulsen, J. R., Clark, C. J., Connor, E. F., & Smith, T. B. (2002). Differential resource use by primates and hornbills: Implications for seed dispersal. Ecology, 83, 228–240.

    Article  Google Scholar 

  • Redford, K. H. (1992). The empty forest. Bioscience, 42, 412–422.

    Article  Google Scholar 

  • Rocha, L. C., & Fortes, V. B. (2015). Perceptions and attitudes of rural residents towards capuchin monkeys, in an area of influence of the Dona Francisca hydroelectric power plant, south Brazil. Ambiente & Sociedade, 18, 19–34.

    Article  Google Scholar 

  • Russo, S. E., Campbell, C. J., Dew, J. L., Stevenson, P. R., & Suarez, S. A. (2005). A multi-forest comparison of dietary preferences and seed dispersal by Ateles spp. International Journal of Primatology, 26, 1017–1037.

    Article  Google Scholar 

  • Russo, S. E., & Chapman, C. (2011). Primate seed dispersal: Linking behavioral ecology with forest community structure. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (pp. 523–534). Oxford: Oxford University Press.

    Google Scholar 

  • Schleuning, M., Blüthgen, N., Flörchinger, M., Braun, J., Schaefer, H. M., & Böhning-Gaese, K. (2011). Specialization and interaction strength in a tropical plant–frugivore network differ among forest strata. Ecology, 92, 26–36.

    Article  PubMed  Google Scholar 

  • Schupp, E. W., Jordano, P., & Gómez, J. M. (2010). Seed dispersal effectiveness revisited: a conceptual review. New Phytologist, 188, 333–353.

    Article  PubMed  Google Scholar 

  • Seddon, P. J., Griffiths, C. J., Soorae, P. S., & Armstrong, D. P. (2014). Reversing defaunation: restoring species in a changing world. Science, 345, 406–412.

    Article  PubMed  CAS  Google Scholar 

  • Sengupta, A., McConkey, K. R., & Radhakrishna, S. (2015). Primates, provisioning and plants: impacts of human cultural behaviours on primate ecological functions. PLoS One, 10, e0140961.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stevenson, P. R. (2007). Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In A. J. Dennis, E. W. Schupp, R. J. Green, & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 340–362). Wallingford: CABI.

    Chapter  Google Scholar 

  • Stevenson, P. R. (2011). The abundance of large Ateline monkeys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica, 43, 512–519.

    Article  Google Scholar 

  • Stevenson, P. R., Link, A., González-Caro, S., & Torres-Jiménez, M. F. (2015). Frugivory in canopy plants in a western Amazonian forest: dispersal systems, phylogenetic ensembles and keystone plants. PLoS One, 10, e0140751.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stevenson, P. R., Link, A., Onshuus, A., Quiroz, A. J., & Velasco, M. (2014). Estimation of seed shadows generated by Andean woolly monkeys (Lagothrix lagothricha lugens). International Journal of Primatology, 35, 1021–1036.

    Article  Google Scholar 

  • Terakawa, M., Isagi, Y., Matsui, K., & Yumoto, T. (2009). Microsatellite analysis of the maternal origin of Myrica rubra seeds in the feces of Japanese macaques. Ecological Research, 24, 663–670.

    Article  CAS  Google Scholar 

  • Terborgh, J. (1986). Community aspects of frugivory in tropical forests. In A. Estrada & T. H. Fleming (Eds.), Frugivores and seed dispersal (pp. 371–384). Dordrecht: Dr. W. Junk Publishers.

    Chapter  Google Scholar 

  • Traveset, A., Heleno, R., & Nogales, M. (2014). The ecology of seed dispersal. In R. S. Gallagher (Ed.), Seeds: The ecology of regeneration in plant communities (pp. 62–93). Wallingford: CABI.

    Chapter  Google Scholar 

  • Traveset, A., Robertson, A. W., & Rodríguez-Pérez, J. (2007). A review on the role of endozoochory in seed germination. In A. J. Dennis, E. W. Schupp, R. J. Green, & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 78–103). Wallingford: CABI.

    Chapter  Google Scholar 

  • Tscharntke, T., Tylianakis, J. M., Rand, T. A., Didham, R. K., Fahrig, L., Batáry, P., Bengtsson, J., Clough, Y., Crist, T. O., Dormann, C. F., Ewers, R. M., Fründ, J., Holt, R. D., Holzschuh, A., Klein, A. M., Kleijn, D., Kremen, C., Landis, D. A., Laurance, W., Lindenmayer, D., Scherber, C., Sodhi, N., Steffan-Dewenter, I., Thies, C., van der Putten, W. H., & Westphal, C. (2012). Landscape moderation of biodiversity patterns and processes-eight hypotheses. Biological Reviews, 87, 661–685.

    Article  PubMed  Google Scholar 

  • Tylianakis, J. M., Laliberté, E., Nielsen, A., & Bascompte, J. (2010). Conservation of species interaction networks. Biological Conservation, 143, 2270–2279.

    Article  Google Scholar 

  • Valenta, K., & Fedigan, L. M. (2009). Effects of gut passage, feces, and seed handling on latency and rate of germination in seeds consumed by capuchins (Cebus capucinus). American Journal of Physical Anthropology, 138, 486–492.

    Article  PubMed  Google Scholar 

  • Valiente-Banuet, A., Aizen, M. A., Alcántara, J. M., Arroyo, J., Cocucci, A., Galetti, M., García, M. B., García, D., Gómez, J. M., Jordano, P., Medel, R., Navarro, L., Obeso, J. R., Oviedo, R., Ramírez, N., Rey, P. J., Traveset, A., Verdú, M., & Zamora, R. (2015). Beyond species loss: the extinction of ecological interactions in a changing world. Functional Ecology, 29, 299–307.

    Article  Google Scholar 

  • Villard, M. A., & Metzger, J. P. (2014). Beyond the fragmentation debate: a conceptual model to predict when habitat configuration really matters. Journal of Applied Ecology, 51, 309–318.

    Article  Google Scholar 

  • Williams-Guillén, K., McCann, C., Martínez Sánchez, J., & Koontz, F. (2006). Resource availability and habitat use by mantled howling monkeys in a Nicaraguan coffee plantation: can agroforests serve as core habitat for a forest mammal? Animal Conservation, 9, 331–338.

    Article  Google Scholar 

  • Zárate, D. A., Andresen, E., Estrada, A., & Serio-Silva, J. C. (2014). Black howler monkey (Alouatta pigra) activity, foraging and seed dispersal patterns in shaded cocoa plantations versus rainforest in southern Mexico. American Journal of Primatology, 76, 890–899.

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Guest Editor Laurance Culot, Editor-in-Chief Joanna M. Setchell, and two anonymous reviewers for thoughtful comments that improved this manuscript.

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  1. Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, CP 58190, Morelia, Michoacán, Mexico

    Ellen Andresen & Víctor Arroyo-Rodríguez

  2. Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, CP 62209, Cuernavaca, Morelos, Mexico

    Michelle Ramos-Robles

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  1. Ellen Andresen
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Andresen, E., Arroyo-Rodríguez, V. & Ramos-Robles, M. Primate Seed Dispersal: Old and New Challenges. Int J Primatol 39, 443–465 (2018). https://doi.org/10.1007/s10764-018-0024-z

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