Reviews

Seed dispersal by primates

  • Chen Yuan ,
  • Wang Zheng ,
  • Xiang Zuofu
Expand
  • 1 College of Life Science and Technology, Central South University of Forestry and Technology, Changsha 410004
    2 College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037

Received date: 2016-06-02

  Accepted date: 2017-01-11

  Online published: 2017-04-07

Abstract

Seed dispersal facilitates the recruitment of plants, which has profound influences upon the spatial distribution of forest plants and the maintenance of biodiversity. Recently, the role of primates in the process of seed dispersal has been increasingly studied. Primates play an important and special role in plant recruitment and vegetation regeneration in the form of feeding on fruits and dispersing seeds. The selection of different fruits is not only closely related to the quality of fruits and the feeding competition of sympatric animals, but also varies greatly with morphological, physiological, and behavioral features of different primates. According to the processes of fruit treatment, the patterns of seed dispersal by primates can be classified as endozoochory, epizoochory, and synzoochory. These patterns have different effects on the distance of seed dispersal, seed germination, and the establishment of seedlings. The most effective pattern is endozoochory, characterized by long-distance dispersal and high rates of seed germination and seedling establishment. Seed dispersal by many primate species helps to restore degraded habitats. Studies on the ecological processes of seed dispersal by primates and determined factors would be conducive to determine the role of primates in the forest ecological system, the contribution of primates to vegetation regeneration, and to provide theoretical evidence for forest ecosystem management and biodiversity conservation.

Cite this article

Chen Yuan , Wang Zheng , Xiang Zuofu . Seed dispersal by primates[J]. Biodiversity Science, 2017 , 25(3) : 325 -331 . DOI: 10.17520/biods.2016148

References

1 Agetsuma N, Noma N (1995) Rapid shifting of foraging pattern by Yakushima macaques (Macaca fuscata yakui) in response to heavy fruiting of Myrica rubra. International Journal of Primatology, 16, 247-260.
2 Albert A, Savini T, Huynen MC (2013) The role of Macaca spp. (Primates: Cercopithecidae) in seed dispersal networks. The Raffles Bulletin of Zoology, 61, 423-434.
3 Albert A, McConkey K, Savini T, Huynen MC (2014) The value of disturbance-tolerant cercopithecine monkeys as seed dispersers in degraded habitats. Biological Conservation, 170, 300-310.
4 Andresen E (1999) Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest. Biotropica, 31, 145-158.
5 Arroyo-Rodríguez V, Andresen E, Bravo SP, Stevenson PR (2015) Seed dispersal by howler monkeys: current knowledge, conservation implications, and future directions. In: Howler Monkeys (eds Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D), pp. 111-139. Springer, New York.
6 Barnett AA, Boyle SA, Pinto LP, Lourenço WC, Almeida T, Silva WS, Ronchi-Teles B, Bezerra BM, Ross C, Maclarnon A, Spironello WR (2012) Primary seed dispersal by three neotropical seed-predating primates (Cacajao melano- cephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus). Journal of Tropical Ecology, 28, 543-555.
7 Beaune D, Bretagnolle F, Bollache L, Bourson C, Hohmann G, Fruth B (2013) Ecological services performed by the bonobo (Pan paniscus): seed dispersal effectiveness in tropical forest. Journal of Tropical Ecology, 29, 367-380.
8 Beaune D (2015) What would happen to the trees and lianas if apes disappeared? Oryx, 49, 442-446.
9 Bicca-Marques JC (2003) How do howler monkeys cope with habitat fragmentation? In: Primates in Fragments: Ecology and Conservation (ed. Marsh LK), pp. 283-303. Springer, New Mexico.
10 Bravo SP (2009) Implications of behavior and gut passage for seed dispersal quality: the case of black and gold howler monkeys. Biotropica, 41, 751-758.
11 Bueno RS, Guevara R, Ribeiro MC, Culot L, Bufalo FS, Galetti M (2013) Functional redundancy and complementarities of seed dispersal by the last neotropical megafrugivores. PLoS ONE, 8, e56252.
12 Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. American Journal of Botany, 87, 1217-1227.
13 Carbone C, Cowlishaw G, Isaac NJB, Rowcliffe JM (2005) How far do animals go? Determinants of day range in mammals. The American Naturalist, 165, 290-297.
14 Cardoso NA, Pendu YL, Lapenta MJ, Raboy BE (2011) Frugivory patterns and seed dispersal by golden-headed lion tamarins (Leontopithecus chrysomelas) in Una Biological Reserve, Bahia, Brazil. Mammalia, 75, 327-337.
15 Chapman CA (1989) Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21, 148-154.
16 Chapman CA, Chapman LJ (1995) Survival without dispersers: seedling recruitment under parents. Conservation Biology, 9, 675-678.
17 Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Dynamics of Populations, 298, 298-312.
18 Corlett RT, Lucas PW (1990) Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis). Oecologia, 82, 166-171.
19 Dew JL, Wright P (1998) Frugivory and seed dispersal by four species of primates in Madagascar’s eastern rain forest. Biotropica, 30, 425-437.
20 Estrada A, Coates-Estrada R (1984) Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxtlas, Mexico. American Journal of Primatology, 6, 77-91.
21 Fan PF, Huang B, Jiang XL (2008) Seed dispersal by black gibbons (Nomascus concolor) in the Wuliang Mountains, Central Yunnan. Acta Theriologica Sinica, 28, 232-236.(in Chinese with English abstract)
21 [范朋飞, 黄蓓, 蒋学龙 (2008) 云南无量山黑长臂猿对植物种子的传播作用. 兽类学报 28, 232-236.]
22 Feeley K (2004) The role of clumped defecation in the spatial distribution of soil nutrients and the availability of nutrients for plant uptake. Journal of Tropical Ecology, 20, 1-4.
23 Fleming TH, Kress WJ (2011) A brief history of fruits and frugivores. Acta Oecologica, 37, 521-530.
24 Fuzessy LF, Cornelissen TG, Janson C, Silveira FAO (2016) How do primates affect seed germination? A meta-analysis of gut passage effects on neotropical plants. Oikos, 125, 1069-1080.
25 Garber PA, Paciulli LM (1997) Experimental field study of spatial memory and learning in wild capuchin monkeys (Cebus capucinus). Folia Primatologica, 68, 236-253.
26 Garber PA, Lambert JE (1998) Primates as seed dispersers: ecological processes and directions for future research. American Journal of Primatology, 45, 3-8.
27 González-Zamora A, Arroyo-Rodríguez V, Escobar F, Rős M, Oyama K, Ibarra-Manríquez G, Stoner KE, Chapman CA (2014) Contagious deposition of seeds in spider monkeys’ sleeping trees limits effective seed dispersal in fragmented landscapes. PLoS ONE, 9, e89346.
28 Hallwachs W (1986) Agoutis (Dasyprocta punctata): the inheritors of guapinol (Hymenaea courbaril: Leguminosae). In: Frugivores and Seed Dispersal (eds Estrada A, Theodore H), pp. 285-304. Springer, Dordrecht.
29 Hemingway CA (1996) Morphology and phenology of seeds and whole fruit eaten by Milne-Edwards’ sifaka, Propith- ecus diadema edwardsi, in Ranomafana National Park, Madagascar. International Journal of Primatology, 17, 637-659.
30 Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201-228.
31 Jansen PA, Bartholomeus M, Bongers F, Elzinga JA, Ouden JD, Wieren SEV (2002) The role of seed size in dispersal by a scatter-hoarding rodent. In: Seed Dispersal and Frugivory: Ecology, Evolution and Conservation (eds Levey DJ, Silva WR, Galetti M), pp. 209-225. CABI Publishing, Wallingford.
32 Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science, 219, 187-189.
33 Janzen DH (1970) Herbivores and the number of tree species in tropical forests. The American Naturalist, 104, 501-528.
34 Julliot C (1997) Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. Journal of Ecology, 85, 431-440.
35 Kaplin BA, Moermond TC (1998) Variation in seed handling by two species of forest monkeys in Rwanda. American Journal of Primatology, 45, 83-101.
36 Koné I, Lambert JE, Refisch J, Bakayoko A (2008) Primate seed dispersal and its potential role in maintaining useful tree species in the Taï region, Côte-d’Ivoire: implications for the conservation of forest fragments. Tropical Conservation Science, 1, 293-306.
37 Lambert JE (1998) Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology: Issues, News,and Reviews, 7, 8-20.
38 Lambert JE (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.
39 Lambert JE (2002) Exploring the link between animal frugivory and plant strategies: the case of primate fruit processing and post-dispersal seed fate. In: Seed Dispersal and Frugivory: Ecology, Evolution and Conservation (eds Levey DJ, Silva WR, Galetti M), pp. 365-379. CABI Publishing, Wallingford.
40 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.
41 Levey DJ, Silva WR, Galetti M (2002) Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. CABI Publishing, Wallingford.
42 Linden B, Linden J, Fischer F, Linsenmair KE (2015) Seed dispersal by South Africa’s only forest-dwelling guenon, the samango monkey (Cercopithecus mitis). South African Journal of Wildlife Research, 45, 88-99.
43 Link A, Fiore AD (2006) Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. Journal of Tropical Ecology, 22, 235-246.
44 Lord JM, Markey AS, Marshall J (2002) Have frugivores influenced the evolution of fruit traits in New Zealand. In: Seed Dispersal and Frugivory: Ecology, Evolution and Conservation (eds Levey DJ, Silva WR, Galetti M), pp. 55-68. CABI Publishing, Wallingford.
45 Lu CH (2001) Effect of rodents on seed dispersal. Chinese Journal of Ecology, 20, 56-58.(in Chinese with English abstract)
45 [鲁长虎 (2001) 啮齿类对植物种子的传播作用. 生态学杂志 20, 56-58.]
46 Maisels F (1993) Gut passage rate in guenons and mangabeys: another indicator of a flexible feeding niche? Folia Primatologica, 61, 35-37.
47 Martins MM (2006) Comparative seed dispersal effectiveness of sympatric Alouatta guariba and Brachyteles arachnoides in southeastern Brazil. Biotropica, 38, 57-63.
48 McCanny SJ (1985) Alternatives in parent-offspring relationships in plants. Oikos, 45, 148-149.
49 McConkey KR, Aldy F, Ario A, Chivers DJ (2002) Selection of fruit by gibbons (Hylobates muelleri × agilis) in the rain forests of central Borneo. International Journal of Primatology, 23, 123-145.
50 Mourthé ÍMC, Strier KB, Boubli JP (2008) Seed predation of Mabea fistulifera (Euphorbiaceae) by northern muriquis (Brachyteles hypoxanthus). Neotropical Primates, 15, 40-45.
51 Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution, 15, 278-285.
52 Nguyen HH, Bai B, Li N, Pan Y, Lu CH (2013) Fruit diet, se- lectivity and seed dispersal of Hatinh langur (Trachypith- ecus francoisi hatinhensis). Acta Ecologica Sinica, 33, 110-119.(in Chinese with English abstract)
52 [阮海河, 白冰, 李宁, 潘扬, 鲁长虎 (2013) 河静黑叶猴果实性食物组成、选择及其对种子的扩散作用. 生态学报 33, 110-119.]
53 Norconk MA, Veres M (2011) Physical properties of fruit and seeds ingested by primate seed predators with emphasis on sakis and bearded sakis. The Anatomical Record, 294, 2092-2111.
54 Otani T (2010) Seed dispersal by Japanese macaques. In: The Japanese Macaques (eds Nakagawa N, Nakamichi M, Sugiura H), pp. 129-142. Springer, Tokyo.
55 Petre CA, Tagg N, Beudels-Jamar RC, Haurez B, Doucet JL (2015) Western lowland gorilla seed dispersal: are seeds adapted to long gut retention times? Acta Oecologica, 67, 59-65.
56 Poulsen JR, Clark CJ, Smith TB (2001) Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon. Journal of Tropical Ecology, 17, 787-808.
57 Righini N, Serio-Silva JC, Rico-Gray V, Martínez-Mota R (2004) Effect of different primate species on germination of Ficus (Urostigma) seeds. Zoo Biology, 23, 273-278.
58 Robertson AW, Trass A, Ladley JJ, Kelly D (2006) Assessing the benefits of frugivory for seed germination: the importance of the deinhibition effect. Functional Ecology, 20, 58-66.
59 Rudran R (1978) Socioecology of the blue monkeys (Cercopithecus mitis stuhlmanni) of the Kibale forest, Uganda. Smithsonian Institution Press, Washington DC.
60 Russo SE, Chapman CA (2011) Primate seed dispersal: linking behavioral ecology with forest community structure. Primates in Perspective, 2, 523-534.
61 Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologist, 188, 333-353.
62 Sengupta A, McConkey KR, Radhakrishna S (2014) Seed dispersal by rhesus macaques Macaca mulatta in northern India. American Journal of Primatology, 76, 1175-1184.
63 Sengupta A, Radhakrishna S (2015) Fruit trait preference in rhesus macaques (Macaca mulatta) and its implications for seed dispersal. International Journal of Primatology, 36, 999-1013.
64 Stevenson PR, Castellanos MC, Pizarro JC, Garavito M (2002) Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. International Journal of Primatology, 23, 1187-1204.
65 Stevenson PR (2011) The abundance of large ateline monkeys is positively associated with the diversity of plants regenerating in neotropical forests. Biotropica, 43, 512-519.
66 Stevenson PR, Link A, Onshuus A, Quiroz AJ, Velasco M (2014) Estimation of seed shadows generated by Andean woolly monkeys (Lagothrix lagothricha lugens). International Journal of Primatology, 35, 1021-1036.
67 Tabarelli M, Peres CA (2002) Abiotic and vertebrate seed dispersal in the Brazilian Atlantic forest: implications for forest regeneration. Biological Conservation, 106, 165-176.
68 Traveset A (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives in Plant Ecology, Evolution and Systematics, 1, 151-190.
69 Traveset A, Verdú M (2002) A meta-analysis of the effect of gut treatment on seed germination. In: Seed Dispersal and Frugivory: Ecology, Evolution and Conservation (eds Levey DJ, Silva WR, Galetti M), pp. 339-350. CABI Publishing, Wallingford.
70 Traveset A, Robertson AW, Rodríguez-Pérez J (2007) A review on the role of endozoochory on seed germination. In: Seed Dispersal: Theory and Its Application in a Changing World (ed. Dennis AJ), pp. 78-103. CABI Publishing, Wallingford.
71 Tsuji Y, Yangozene K, Sakamaki T (2010) Estimation of seed dispersal distance by the bonobo, Pan paniscus, in a tropical forest in Democratic Republic of Congo. Journal of Tropical Ecology, 26, 115-118.
72 Tutin CEG, Williamson EA, Rogers ME, Fernandez M (1991) A case study of a plant-animal relationship: Cola lizae and lowland gorillas in the Lopé Reserve, Gabon. Journal of Tropical Ecology, 7, 181-199.
73 Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends in Ecology and Evolution, 17, 379-386.
74 Wehncke EV, Dominguez CA (2007) Seed dispersal ecology of non-restricted frugivores, capuchin monkeys in three neotropical forests. Journal of Tropical Ecology, 23, 519-528.
Outlines

/

〈 〉