Skip to main content

Macaques as Seed Dispersal Agents in Asian Forests: A Review

Abstract

The role of primates in seed dispersal is well recognized. Macaques (Macaca spp.) are major primate seed dispersers in Asia, and recent studies have revealed their role as seed dispersal agents in this region. Here, we review present knowledge of the traits that define the role of macaques as seed dispersers. The size of seeds in fruit influences whether macaques swallow (0.5–17.1 mm; median: 3.0), spit (1–37 mm; median: 7.6), or drop (8.2–57.7 mm; median: 20.5) them. Dispersal distances via defecation are several hundreds of meters (median: 259 m, range: 0–1300 m), shorter than those achieved by some mammals and birds in tropical and temperate regions. However, macaques disperse seeds by defecation at comparable distances to omnivorous carnivores, and further than passerines. Seed dispersal distance by spitting is much shorter (median: 20 m, range: 0–405 m) than by defecation. Among Asian primates, seed dispersal distances resulting from macaque defecation are shorter than those for gibbons and longer than those for langurs. The effects of seed ingestion on the percentage and speed of germination vary among both plant and macaque species. The degree of frugivory, fruit/seed handling methods, seed dispersal distance, microhabitats of dispersed seeds, and effects of dispersal on seed germination vary seasonally and interannually, and long-term studies of the ecological role of macaques are needed. Researchers have begun to assess the effectiveness of seed dispersal by macaques, secondary dispersal of seeds originally dispersed by macaques, and the effects of provisioning on seed dispersal. Future studies should also test the effects of social factors (such as age and rank), which have received little attention in studies of seed dispersal.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Albert, A., Hambuckers, A., Culot, L., Savini, T., & Huynen, M. (2013a). Frugivory and seed dispersal by northern pigtailed macaques (Macaca leonina), in Thailand. International Journal of Primatology, 34, 170–193.

    Article  Google Scholar 

  • Albert, A., McConkey, K., Savini, T., & Huynen, M. (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. (2013b). The role of Macaca spp. (Primates: Cercopithecidae) in seed dispersal networks. The Ruffles Bulletin of Zoology, 61, 423–434.

    Google Scholar 

  • Ali, R. (1986). Feeding ecology of the bonnet macaque at the Mundanthurai sanctuary, Tamilnadu. Journal of Bombay Natural History Society, 83, 98–110.

    Google Scholar 

  • Andresen, E. (2002). Primary seed dispersal by red howler monkeys and the effect of defecation patterns on the fate of dispersed seeds. Biotropica, 34, 261–272.

  • Andresen, E., Arroyo-Rodríguez, V., & Ramos-Robles, M. (2018). Primate seed dispersal: Old and new challenges. International Journal of Primatology.

  • Andresen, E., & Feer, F. (2005). The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests. In P. M. Forget, J. E. Lambert, P. E. Hulme, & S. B. Vander Wall (Eds.), Seed fate (pp. 331–349). Cambridge: CAB International.

  • Augspurger, C. K. (1984). Seedling survival of tropical tree species: Interactions of dispersal distance, light-gaps, and pathogens. Ecology, 65, 1705–1712.

    Article  Google Scholar 

  • Caldecott, J. O. (1986). An ecological and behavioural study of the pig-tailed macaque. Basel: Karger.

    Google Scholar 

  • Campos-Arceiz, A., & Blake, S. (2011). Megagardeners of the forest and the role of elephants in seed dispersal. Acta Oecologica, 37, 542–553.

    Article  Google Scholar 

  • Campos-Arceiz, A., Larrinaga, A. R., Weerasinghe, U. R., Takatsuki, S., Pastorini, J., Leimgruber, P., Fernando, P., & Santamaría, L. (2008). Behavior rather than diet mediates season differences in seed dispersed by Asian elephants. Ecology, 89, 2684–2691.

    PubMed  Article  Google Scholar 

  • Campos-Arceiz, A., Traeholt, C., Jaffar, R., Santamaria, L., & Corlett, R. T. (2012). Asian tapirs are no elephants when it comes to seed dispersal. Biotropica, 44, 220–227.

    Article  Google Scholar 

  • Chang, N. C., Su, H. H., & Lee, L. L. (2016). Effects of dietary fiber on gut retention time in captive Macaca cyclopis, Macaca fascicularis, Hylobates lar, and Pongo pygmaeus and the germination of ingested seeds. International Journal of Primatology, 37, 671–687.

    Article  Google Scholar 

  • Chapman, C. A., & Russo, S. E. (2007). Primate seed dispersal: Linking behavioral ecology with forest community structure. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 510–525). Oxford: Oxford University Press.

    Google Scholar 

  • Chen, C. E. (1999). The influence of Formosan macaques (Macaca cyclopis) on seed dispersal in Fushan Experimental Forest. Master thesis: National Taiwan University.

  • Chen, C.E. (2002). Seed dispersal by Formosan macaques (Macaca cyclopis) in the Fusan Experimental Forest of Taiwan. PhD dissertation: National Taiwan University.

  • Corlett, R. T. (2009). Seed dispersal distances and plant migration potential in tropical East Asia. Biotropica, 41, 592–598.

    Article  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 

  • Corlett, R. T., & Lucas, P. W. (1990). Alternative seed-handling strategies in primates: Seed-spitting by long-tailed macaques (Macaca fascicularis). Oecologia, 82, 166–171.

    PubMed  Article  CAS  Google Scholar 

  • Dalling, J. W. (2005). The fate of seed bank: Factors influencing seed survival for light-demanding species in moist tropical forests. In P. M. Forget, J. E. Lambert, P. E. Hulme, & S. B. Vander Wall (Eds.), Seed fate (pp. 31–44). Cambridge: CAB International.

    Google Scholar 

  • Dittus, W. P. J. (1977). The socioecological basis for the conservation of the toque monkey (Macaca sinica) of Sri Lanka (Ceylon). In Prince Rainer III (Ed.), Primate conservation (pp. 237–265). New York: Academic Press.

  • Enari, H., Koike, S., & Sakamaki, H. (2011). Assessing the diversity of dung beetle assemblages utilizing Japanese monkeys feces in cool-temperate forests. Journal of Forest Research, 16, 456–464.

    Article  Google Scholar 

  • Enari, H., Koike, S., & Sakamaki, H. (2013). Influences of different large mammalian fauna on dung beetle diversity in beech forests. Journal of Insect Science, 13(54), 1–13.

    Article  Google Scholar 

  • Enari H., & Sakamaki-Enari, H. (2014). Synergistic effects of primates and dung beetles on soil seed accumulation in snow regions. Ecological Research, 29, 653–660.

  • Erinjery, J. J., Kavana, T. S., & Singh, M. (2015). Food resources, distribution and seasonal variations in ranging in lion-tailed macaques, Macaca silenus in the western Ghats, India. Primates, 56, 45–54.

    PubMed  Article  Google Scholar 

  • Estrada, A., & Coates-Estrada, R. (1991). Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal: Ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology, 7, 459–474.

    Article  Google Scholar 

  • Fukui, A. (1995). The role of the brown-eared bulbul Hypsypetes amaurotis as a seed dispersal agent. Researches on Population Ecology, 37, 211–218.

    Article  Google Scholar 

  • Fukui, A. (1996). Retention time of seeds in bird guts: Costs and benefits for fruiting plants and frugivorous birds. Plant Species Biology, 11, 141–147.

    Article  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 

  • Go, M. (2010). Seasonal changes in food resource distribution and feeding sites selected by Japanese macaques on Koshima islet, Japan. Primates, 51, 149–158.

    PubMed  Article  Google Scholar 

  • González-Varo, J. P., López-Bao, J. V., & Guitián, J. (2013). Functional diversity among seed dispersal kernels generated by carnivorous mammals. Journal of Animal Ecology, 82, 562–571.

    PubMed  Article  Google Scholar 

  • Gross-Camp, N. D., Mulindahabi, F., & Kaplin, B. A. (2009). Comparing the dispersal of large-seeded tree species by frugivore assemblages in tropical montane forest in Africa. Biotropica, 41, 442–451.

    Article  Google Scholar 

  • Hamada, A., & Hanya, G. (2016). Frugivore assemblage of Ficus superba in a warm-temperate forest in Yakushima, Japan. Ecological Research, 31, 903–911.

    Article  Google Scholar 

  • Hanya, G. (2004). Diet of a Japanese macaque troop in the coniferous forest of Yakushima. International Journal of Primatology, 25, 55–71.

    Article  Google Scholar 

  • Hanya, G. (2005). Comparisons of dispersal success between the species fruiting prior to and those at the peak of migrant frugivore abundance. Plant Ecology, 181, 167–177.

    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 

  • Hladik, C. M., & Hladik, A. (1972). Disponibilités alimentaires et domaines vitaux des primate á Ceylan. La Terre et la Vie, 2, 149–215.

    Google Scholar 

  • Howe, H. F. (1989). Scatter- and clump-dispersal and seedling demography: Hypothesis and implications. Oecologia, 79, 417–426.

    PubMed  Article  CAS  Google Scholar 

  • Howe, H. F., & Smallwood, J. (1982). Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201–228.

    Article  Google Scholar 

  • Hsu, C. I. (2014). Comparison of seed dispersal by Taiwanese macaques (Macaca cyclopis) in Kenting and Ershui. Master’s thesis, National Pingtung University of Science and Technology.

  • Huang, C.L. (2005) Effects of dispersal via cheek pouches of Formosan macaques (Macaca cyclopis) on seed shadow and seed fate of three Lauraceae species at Fushan Experimental Forest. PhD dissertation: National Taiwan University.

  • Huang, Z., Huang, C., Wei, H., Tang, H., Krzton, A., Ma, G., & Zhou, Q. (2015). Factors influencing positional behavior and habitat use of sympatric macaques in the limestone habitat of Nonggang, China. International Journal of Primatology, 36, 95–112.

    Article  Google Scholar 

  • Ilham, K., Rizaldi, Nurdin, J., & Tsuji, Y. (2017). Status of urban populations of the long-tailed macaque (Macaca fascicularis) in West Sumatra, Indonesia. Primates, 58, 1–11.

  • José-Domínguez, J. M., Asensio, N., García, C. J. G., Huynen, M. C., & Savini, T. (2015). Exploring the multiple functions of sleeping sites in northern pig-tailed macaques (Macaca leonina). International Journal of Primatology, 36, 948–966.

    Article  Google Scholar 

  • Kaplin, B. A., & Moermond, T. C. (1998). Variation in seed handling by two species of forest monkeys in Rwanda. American Journal of Primatology, 45, 83–101.

    PubMed  Article  CAS  Google Scholar 

  • Kinzey, W. G., & Norconk, M. A. (1993). Physical and chemical properties of fruit and seeds eaten by Pithecia and Chiropotes in Surinam and Venezuela. International Journal of Primatology, 14, 207–227.

    Article  Google Scholar 

  • Kitamura, S. (2011). Frugivory and seed dispersal by hornbills (Bucerotidae) in tropical forests. Acta Oecologica, 37, 531–541.

    Article  Google Scholar 

  • Kitamura, S., Yumoto, T., Poonswad, P., Chuailua, P., Plongmai, K., Maruhashi, T., & Noma, N. (2002). Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecologia, 133, 559–572.

    PubMed  Article  Google Scholar 

  • Koganezawa, M., & Imaki, H. (1999). The effects of food sources on Japanese monkey home range size and location, and population dynamics. Primates, 40, 177–185.

    PubMed  Article  CAS  Google Scholar 

  • Koike, S., Masaki, T., Nemoto, Y., Kozakai, C., Yamazaki, K., Kasai, S., Nakajima, A., & Kaji, K. (2011). Estimate of the seed shadow created by the Asiatic black bear Ursus thibetanus and its characteristics as a seed disperser in Japanese cool-temperate forest. Oikos, 120, 280–290.

    Article  Google Scholar 

  • Krishnamani, R. (1994). Diet composition of the bonnet macaque (Macaca radiata) in a tropical dry evergreen forest of southern India. Tropical Biodiversity, 2, 285–302.

    Google Scholar 

  • Kumar, R. S., Mishra, C., & Sinha, A. (2007). the Arunachal macaque Macaca munzala: A preliminary study. Current Science, 93, 532–539.

    Google Scholar 

  • Kuussaari, M., Bommarco, R., Heikkinen, R. K., Helm, A., Krauss, J., Lindborg, R., Öckinger, E., Pärtel, M., Pino, J., Rodà, F., Stefanescu, C., Teder, T., Zobel, M., & Steffan-Dewenter, I. (2009). Extinction debt: A challenge for biodiversity conservation. Trends in Ecology & Evolution, 24, 564–571.

    Article  Google Scholar 

  • Lambert, J. E. (1999). Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. American Journal of Physical Anthropology, 109, 365–386.

    PubMed  Article  CAS  Google Scholar 

  • Leighton, M. (1993). Modeling dietary selectivity by Bornean orangutans: Evidence for integration of multiple criteria in fruit selection. International Journal of Primatology, 14, 257–313.

    Article  Google Scholar 

  • Lin, P. J. (2000). Fruit and seed consumption by frugivores on the Lauraceae trees (Lindera communis, Litsea acuminata, Machilus thungbergii, M. mushaensis, M. zuihoensis) at Fushan experimental forest. Master’s thesis, National Dong Hwa University, Taiwan.

  • Liu, T. H., Lin, Y. C., Wei, C. H., & Su, H. H. (2012). Seed distributions and density of Bischofia javanica produced by Taiwanese macaques (Macaca cyclopis) in Kenting. Tunghai Science, 14, 46–65.

    Google Scholar 

  • Lucas, P. W., & Corlett, R. T. (1991). Relationship between the diet of Macaca fascicularis and forest phenology. Folia Primatologica, 57, 201–215.

    Article  Google Scholar 

  • Lucas, P. W., & Corlett, R. T. (1998). Seed dispersal by long-tailed macaques. American Journal of Primatology, 45, 29–44.

    PubMed  Article  CAS  Google Scholar 

  • MacKinnon, J., & MacKinnon, K. S. (1981). Niche differentiation in a primate community. In D. J. Chivers (Ed.), Malayan forest primates (pp. 167–190). New York: Plenum Publishing.

  • McConkey, K. R. (2018). Seed dispersal by primates in Asian habitats: From species, to communities, to conservation. International Journal of Primatology.

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

    PubMed  Article  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., Brockelman, W. Y., Saralamba, C., & Nathalang, A. (2015). Effectiveness of primate seed dispersers for an “oversized” fruit, Garcinia benthamii. Ecology, 96, 2737–2747.

    PubMed  Article  Google Scholar 

  • McConkey, K. R., & Chivers, D. J. (2007). Influence of gibbon ranging patterns on seed dispersal distance and deposition site in a Bornean forest. Journal of Tropical Ecology, 23, 269–275.

    Article  Google Scholar 

  • Mehlman, P. T. (1988). Food resources of the wild barbary macaque (Macaca sylvanus) in high-altitude fir forest, Ghomaran Rif, Morocco. Journal of Zoology, 214, 469–490.

    Article  Google Scholar 

  • Mehlman, P. T. (1989). Comparative density, demography, and ranging behavior of barbary macaques (Macaca sylvanus) in marginal and prime conifer habitats. International Journal of Primatology, 10, 269–292.

    Article  Google Scholar 

  • Ménard, N., & Vallet, D. (1996). Demography and ecology of barbary macaques (Macaca sylvanus) in two different habitats. In J. E. Fa & D. G. Lindburg (Eds.), Evolution and ecology of macaque societies (pp. 106–131). Cambridge: Cambridge University Press.

    Google Scholar 

  • Mendiratta, U., Kumar, A., Mishra, C., & Sinha, A. (2009). Winter ecology of the Arunachal macaque Macaca munzala in Pangchen Valley, western Arunachal Pradesh, northeastern India. American Journal of Primatology, 71, 939–947.

    PubMed  Article  Google Scholar 

  • Moles, A. T., Ackerly, D. D., Tweddle, J. C., Dickie, J. B., Smith, R., Leishman, M. R., Mayfield, M. M., Pitman, A., Wood, J. T., & Westoby, M. (2007). Global patterns in seed size. Global Ecology and Biogeography, 16, 109–116.

    Article  Google Scholar 

  • Moles, A. T., Wright, I. J., Pitman, A. J., Murray, B. R., & Westoby, M. (2009). Is there a latitudinal gradient in seed production? Ecography, 32, 78–82.

    Article  Google Scholar 

  • Murray, P. (1975). The role of cheek pouches in cercopithecine monkey adaptive strategy. In R. H. Tuttle (Ed.), Primate functional morphology and evolution (pp. 151–194). Hague: Mouton.

  • Nakamoto, A., Kinjo, K., & Izawa, M. (2009). The role of Orii’s flying-fox (Pteropus dasymallus inopinatus) as a pollinator and a seed disperser on Okinawa-Jima Island, the Ryukyu archipelago, Japan. Ecological Research, 24, 405–414.

    Article  Google Scholar 

  • Nakashima, Y., Inoue, E., Inoue-Murayama, M., & Sukor, J. R. A. (2010). Functional uniqueness of a small carnivore as seed dispersal agents: A case study of the common palm civets in the Tabin wildlife reserve, Sabah, Malaysia. Oecologia, 164, 721–730.

    PubMed  Article  Google Scholar 

  • Nakashima, Y., Lagan, P., & Kitayama, K. (2008). A study of fruit–frugivore interactions in two species of durian (Durio, Bombacaceae) in Sabah, Malaysia. Biotropica, 40, 255–258.

    Article  Google Scholar 

  • Nakashima, Y., & Sukor, J. A. (2010). Importance of common palm civets (Paradoxurus hermaphroditus) as a long-distance disperser for large-seeded plants in degraded forests. Tropics, 18, 221–228.

    Article  Google Scholar 

  • Nishikawa, M., & Mochida, K. (2010). Coprophagy-related interspecific nocturnal interactions between Japanese macaques (Macaca fuscata yakui) and sika deer (Cervus nippon yakushimae). Primates, 51, 95–99.

    PubMed  Article  Google Scholar 

  • Noma, N., & Yumoto, T. (1997). Fruiting phenology of animal-dispersed plants in response to winter migration of frugivores in a warm temperate forest on Yakushima Island, Japan. Ecological Research, 12, 119–129.

    Article  Google Scholar 

  • O’Brien, T. G., & Kinnaird, M. F. (1997). Behavior, diet, and movements of the Sulawesi crested black macaque (Macaca nigra). International Journal of Primatology, 18, 321–351.

    Article  Google Scholar 

  • Otani, T. (2001). Measuring fig foraging frequency of the Yakushima macaque by using automatic cameras. Ecological Research, 16, 49–54.

    Article  Google Scholar 

  • Otani, T. (2003). Seed dispersal and predation of fleshy-fruited plants by Japanese macaques in the cool temperate zone of northern Japan. Mammal Study, 28, 153–156.

    Article  Google Scholar 

  • Otani, T. (2004). Effects of macaque ingestion on seed destruction and germination of a fleshy-fruited tree, Eurya emarginata. Ecological Research, 19, 495–501.

    Article  Google Scholar 

  • Otani, T. (2005). Characteristics of middle-size mammals as a seed disperser of fleshy-fruited plants. Nagoya University Forest Science, 24, 7–43.

    Google Scholar 

  • Otani, T. (2010). Seed dispersal by Japanese macaques. In N. Nakagawa, M. Nakamichi, & H. Sugiura (Eds.), The Japanese macaques (pp. 129–142). Tokyo: Springer.

    Chapter  Google Scholar 

  • Otani, T., & Shibata, E. (2000). Seed dispersal and predation by Yakushima macaques, Macaca fuscata yakui, in a warm temperate forest of Yakushima Island, southern Japan. Ecological Research, 15, 133–144.

    Article  Google Scholar 

  • Phua, P. B., & Corlett, R. T. (1989). Seed dispersal by the lesser-short-nosed fruit bat (Cynopterus brachyotis, Pteropodidae, Megachiroptera). Malayan Nature Journal, 42, 251–256.

    Google Scholar 

  • Pombo, A. R., Waltert, M., Mansjoer, S. S., Mardiastuti, A., & Mühlenberg, M. (2004). Home range, diet and behaviour of the Tonkean macaque (Macaca tonkeana) in Lore Lindu National Park, Sulawesi. In G. Gerold, & M. Fremerey (Eds.), Land use, nature conservation and the stability of rainforest margins in Southeast Asia (pp. 313–325). Berlin: Springer.

  • Priston, N. E. C., & McLennan, M. R. (2013). Managing humans, managing macaques: Human–macaque conflict in Asia and Africa. In S. Radhakrishna, M. A. Huffman, & A. Sinha (Eds.), The macaque connection: Cooperation and conflict between humans and macaques. Developments in Primatology: Progress and Prospects 43 (pp. 225–250). Heidelberg: Springer-Verlag.

    Google Scholar 

  • Razafindratsima, O. H., Jones, T. A., & Dunham, A. E. (2013). Patterns of movement and seed dispersal by three lemur species. American Journal of Primatology, 76, 84–96.

    PubMed  Article  Google Scholar 

  • Razafindratsima, O. H., Sato, H., Tsuji, Y., & Culot, L. (2018). Advances and frontiers in primate seed dispersal. International Journal of Primatology.

  • Reiter, J., Curio, E., Tacud, B., Urbina, H., & Geronimo, F. (2006). Tracking bat-dispersed seeds using fluorescent pigment. Biotropica, 38, 64–68.

    Google Scholar 

  • Richard, A. F., Goldstein, S. J., & Dewar, R. E. (1989). Weed macaques: The evolutionary implications of macaques feeding ecology. International Journal of Primatology, 10, 569–594.

    Article  Google Scholar 

  • Richter, C., Taufiq, A., Hodges, K., Ostner, J., & Schülke, O. (2013). Ecology of an endemic primate species (Macaca siberu) on Siberut Island, Indonesia. Springer Plus, 2, 137.

    PubMed  Article  Google Scholar 

  • Riley, E. P. (2007). Flexibility in diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration. International Journal of Primatology, 28, 107–133.

    Article  Google Scholar 

  • Rodman, P. S. (1978). Diets, densities, and distributions of Bornean primates. In G. G. Montogomery (Ed.), The ecology of arboreal folivores (pp. 465–478). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Sakamoto, Y., & Takatsuki, S. (2015). Seeds recovered from the droppings at latrines of the raccoon dog (Nyctereutes procyonoides viverrinus): The possibility of seed dispersal. Zoological Science, 32, 157–162.

    PubMed  Article  Google Scholar 

  • Santhosh, K., Kumara, H. N., Velankar, A. D., & Sinha, A. (2015). Ranging behavior and resource use by lion-tailed macaques (Macaca silenus) in selectively logged forests. International Journal of Primatology, 36, 288–310.

    Article  Google Scholar 

  • Saraswat, R., Sinha, A., & Radhakrishna, S. (2015). A god becomes a pest? Human-rhesus macaque interactions in Himachal Pradesh, northern India. European Journal of Wildlife Research, 61, 435–443.

    Article  Google Scholar 

  • Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 107(108), 15–29.

    Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Sekar, N., Lee, C. L., & Sukumar, R. (2015). In the elephant's seed shadow: The prospects of domestic bovids as replacement dispersers of three tropical Asian trees. Ecology, 96, 2093–2105.

    PubMed  Article  Google Scholar 

  • Sekar, N., & Sukumar, R. (2015). The Asian elephant is amongst the top three frugivores of two tree species with easily edible fruit. Journal of Tropical Ecology, 31, 385–394.

    Article  Google Scholar 

  • Sengupta, A., McConkey, K. R., & Radhakrishna, S. (2014). Seed dispersal by rhesus macaques Macaca mulatta in northern India. American Journal of Primatology, 76, 1175–1184.

    PubMed  Article  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.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Sengupta, A., & Radhakrishna, S. (2016). Fruit trait preference in rhesus macaques (Macaca mulatta) and its implications for seed dispersal. International Journal of Primatologica, 36, 982–996.

    Google Scholar 

  • Sha, J. C. M., & Hanya, G. (2013). Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis). American Journal of Primatology, 75, 581–592.

    PubMed  Article  Google Scholar 

  • Sprague, D. S., Suzuki, S., Takahashi, H., & Sato, S. (1998). Male life history in natural populations of Japanese macaques: Migration, dominance rank, and troop participation of males in two habitats. Primates, 39, 351–363.

    Article  Google Scholar 

  • Su, H. H., & Lee, L. L. (2001). Food habits of Formosan rock macaques (Macaca cyclopis) in Jentse, northeastern Taiwan, assessed by fecal analysis and behavioral observation. International Journal of Primatology, 22, 359–377.

    Article  Google Scholar 

  • Sugiura, H., Shimooka, Y., & Tsuji, Y. (2011). Variation in spatial cohesiveness in a group of Japanese macaques (Macaca fuscata). International Journal of Primatology, 32, 1348–1366.

    Article  Google Scholar 

  • Takasaki, H. (1981). Troop size, habitat quality, and home range area in Japanese macaques. Behavioral Ecology and Sociobiology, 9, 277–281.

    Article  Google Scholar 

  • Terakawa, M., Isagi, Y., Matsui, K., & Yumoto, T. (2008). 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 

  • Terakawa, M., Matsui, K., Hamada, T., Noma, N., & Yumoto, T. (2009). Reduced seed dispersal effectiveness in the large-seeded tree Myrica rubra in the absence of the Japanese macaque on Tanegashima Island, Japan. Japanese Journal of Conservation Ecology, 13, 161–167.

    Google Scholar 

  • Thierry, B. (2007). The macaques: A double-layered social organization. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp.224–239). Oxford: Oxford University Press.

  • Traveset, A. (1998). Effect of seed passage through vertebrate frugivores' guts on germination: A review. Perspectives in Plant Ecology, Evolution and Systematics, 1(2), 151–190.

    Article  Google Scholar 

  • Tsuji, Y. (2011). Seed dispersal by Japanese macaques (Macaca fuscata) in western Tokyo, Japan: A preliminary report. Mammal Study, 36, 165–168.

    Article  Google Scholar 

  • Tsuji, Y. (2014). Inter-annual variation in characteristics of endozoochory by wild Japanese macaques. PLoS One, 9, e108155.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Tsuji, Y., Hanya, G., & Grueter, C. C. (2013). Feeding strategies of primates in temperate and alpine forests: A comparison of Asian macaques and colobines. Primates, 54, 201–215.

    PubMed  Article  Google Scholar 

  • Tsuji, Y., Ito, T. Y., Wada, K., & Watanabe, K. (2015). Spatial patterns in the diet of the Japanese macaque Macaca fuscata and their environmental determinants. Mammal Review, 45, 227–238.

    Article  Google Scholar 

  • Tsuji, Y., & Morimoto, M. (2016). Endozoochorous seed dispersal by Japanese macaques (Macaca fuscata): Effects of temporal variation in ranging and seed characteristics on seed shadows. American Journal of Primatology, 78, 185–191.

    PubMed  Article  Google Scholar 

  • Tsuji, Y., Morimoto, M., & Matsubayashi, K. (2010). Effects of the physical characteristics of seeds on gastrointestinal passage time in captive Japanese macaques. Journal of Zoology, 280, 171–176.

    Article  Google Scholar 

  • Tsuji, Y., Ningsih, J. I. D. P., Kitamura, S., Widayati, K. A., & Suryobroto, B. (2017). Neglected seed dispersers: Endozoochory by Javan lutungs (Trachypithecus auratus) in Indonesia. Biotropica, 49, 539–545.

    Article  Google Scholar 

  • Tsuji, Y., Okumura, T., Kitahara, M., & Jiang, Z. (2016). Estimated seed shadow generated by Japanese martens (Martes melampus): Comparison with forest-dwelling animals in Japan. Zoological Science, 33, 352–357.

    PubMed  Article  Google Scholar 

  • Tsuji, Y., Sato, K., & Sato, Y. (2011). The role of Japanese macaques (Macaca fuscata) as endozoochorous seed dispersers on Kinkazan Island, northern Japan. Mammalian Biology, 76, 525–533.

    Article  Google Scholar 

  • Tsuji, Y., & Sugiyama, Y. (2014). Female emigration in Japanese macaques, Macaca fuscata: Ecological and social backgrounds and its biogeographical implications. Mammalia, 78, 281–290.

    Article  Google Scholar 

  • Tsuji, Y., & Takatsuki, S. (2004). Food habits and home range use of Japanese macaques on an island inhabited by deer. Ecological Research, 19, 381–388.

    Article  Google Scholar 

  • Tsuji, Y., & Takatsuki, S. (2012). Inter-annual variation in nut abundance is related to agonistic interactions of foraging female Japanese macaques (Macaca fuscata). International Journal of Primatology, 33, 489–512.

    Article  Google Scholar 

  • Tsujino, R., & Yumoto, T. (2009). Topography-specific seed dispersal by Japanese macaques in a lowland forest on Yakushima Island, Japan. Journal of Animal Ecology, 78, 119–125.

    PubMed  Article  Google Scholar 

  • Umpathy, A. G., & Kumar, A. (2000). Impacts of the habitat fragmentation on time budget and feeding ecology of lion-tailed macaque (Macaca silenus) in rain forest fragments of Anamalai Hills, South India. Primate Reports, 58, 67–82.

    Google Scholar 

  • Unger, P. S. (1996). Feeding heights and niche separation in sympatric Sumatran monkeys and apes. Folia Primatologica, 67, 163–168.

    Article  Google Scholar 

  • van Noordwijk, M. A., & van Schaik, C. P. (1985). Male migration and rank acquisition in wild long-tailed macaques (Macaca fascicularis). Animal Behaviour, 33, 849–861.

    Article  Google Scholar 

  • van Noordwijk, M. A., & van Schaik, C. P. (1987). Competition among female long-tailed macaques, Macaca fascicularis. Animal Behavior, 35, 577–589.

    Article  Google Scholar 

  • Whitten, A. J. (1982). Diet and feeding behavior of Kloss gibbons on Siberut Island, Indonesia. Folia Primatologica, 37, 177–208.

    Article  CAS  Google Scholar 

  • Willson, M. F., Irvine, A. K., & Walsh, N. G. (1989). Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica, 21, 133–147.

    Article  Google Scholar 

  • Yagihashi, T., Hayashida, M., & Miyamoto, T. (1998). Effects of bird ingestion on seed germination of Sorbus commixta. Oecologia, 114, 209–212.

    PubMed  Article  Google Scholar 

  • Yumoto, T., Noma, N., & Maruhashi, T. (1998). Cheek-pouch dispersal of seeds by Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan. Primates, 39, 325–338.

    Article  Google Scholar 

  • Zhao, Q., Deng, Z., & Xu, J. (1991). Natural foods and their ecological implications for Macaca thibetana at mount Emei, China. Folia Primatologica, 57, 1–15.

    Article  CAS  Google Scholar 

  • Zhou, Q., Wei, H., Huang, Z., & Huang, C. (2011). Diet of the Assamese macaque Macaca assamensis in limestone habitats of Nonggang, China. Current Zoology, 57, 18–25.

    Article  Google Scholar 

Download references

Acknowledgments

This study was based on the symposium “Advances and Frontiers in Primate Seed Dispersal” held at the XXIIIth International Primatological Congress in Chicago. We thank Drs. Hiroki Sato, Onja H. Razafindratsima, and Laurence Culot for contributing to the edition of the special issue. The manuscript benefited from the comments of Drs. Kim McConkey, Joanna M. Setchell, Michael A. Huffman, and an anonymous reviewer.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yamato Tsuji.

Additional information

Handling Editor: Joanna M. Setchell

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tsuji, Y., Su, HH. Macaques as Seed Dispersal Agents in Asian Forests: A Review. Int J Primatol 39, 356–376 (2018). https://doi.org/10.1007/s10764-018-0045-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-018-0045-7

Keywords

  • Asia
  • Endozoochory
  • Long-term study
  • Macaca
  • Seed dispersal effectiveness