Plant Ecology

, Volume 219, Issue 4, pp 417–427 | Cite as

First evidence of epizoochorous seed dispersal by golden snub-nosed monkeys (Rhinopithecus roxellana) in temperate forest

  • Yuan Chen
  • Haochun Chen
  • Youji Zhang
  • Hui Yao
  • Wanji Yang
  • Yucheng Zhao
  • Xiangdong Ruan
  • Zuofu Xiang


Although many primates are identified as effective endozoochorous seed dispersers in forest ecosystems, epizoochorous seed dispersal by primates has generally been overlooked. In this study, we report epizoochorous seed dispersal in a group of free-ranging golden snub-nosed monkeys (Rhinopithecus roxellana) residing in the temperate forests of central China by identifying seeds carried by 12 well-habituated individuals. The results showed a total of 1920 seeds (five families, seven genera) belonging to eight plant species attached to the monkeys’ fur; the three most abundant species were Geum aleppicum (54% of the total), Torilis japonica (17%), and Agrimonia pilosa (14%). The majority of seeds (95.3%) that attached to the monkeys’ fur had special morphologies such as hairs, hooks, or awns. We also found that the quantity of seeds attached to the fur was not significantly different by age-sex class, even though adult males have very long fur. Our study provides the first empirical evidence of epizoochorous seed dispersal by primates and suggests the role of primates in seed dispersal may be greater than previously assumed.


External dispersal Snub-nosed monkey Seed traits Individual difference Temperate forest Plant recruitment 



This study was supported by the National Key Technology R & D Program of China (2013BAD03-02), and the National Natural Science Foundation of China (31670397). We thank the staff at the administrative bureau of Shennongjia National Park in Hubei province for their support. We are grateful to Ms. Fan Zhang and Mr. Jinlong Luo for assistance with seed identification. We also thank Dr. Cheng Guo and two anonymous reviewers for constructive comments on the manuscript.

Compliance with ethical standards

Ethical approval

The research adhered to the American Society of Primatologists’ principles for the ethical treatment of primates. Prior to conducting this study, approval was obtained from Shennongjia National Park (snp-081201) and Institutional Animal Care and Use Committee of Central South University of Forestry and Technology (csuft-090120).


  1. Albert A, Savini T, Huynen MC (2013) The role of Macaca spp. (Primates: Cercopithecidae) in seed dispersal networks. Raffles B Zool 61:423–434Google Scholar
  2. Albert A, Mårell A, Picard M, Baltzinger C (2015) Using basic plant traits to predict ungulate seed dispersal potential. Ecography 38:440–449. CrossRefGoogle Scholar
  3. Barton RA, Whiten A, Strum SC, Byrne RW, Simpson AJ (1992) Habitat use and resource availability in baboons. Anim Behav 43:831–844. CrossRefGoogle Scholar
  4. Benthien O, Bober J, Castens J, Stolter C (2016) Seed dispersal capacity of sheep and goats in a near-coastal dry grassland habitat. Basic Appl Ecol 17:508–515. CrossRefGoogle Scholar
  5. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Corlett RT, Lucas PW (1990) Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis). Oecologia 82:166–171. CrossRefPubMedGoogle Scholar
  7. Couvreur M, Cosyns E, Hermy M, Hoffmann M (2005) Complementarity of epi- and endozoochory of plant seeds by free ranging donkeys. Ecography 28:37–48. CrossRefGoogle Scholar
  8. Couvreur M, Verheyen K, Vellend M, Lamoot I, Cosyns E, Hoffmann M, Hermy M (2008) Epizoochory by large herbivores: merging data with models. Basic Appl Ecol 9:204–212. CrossRefGoogle Scholar
  9. Davison GWH (1982) Convergence with terrestrial cercopithecines by the monkey Rhinopithecus roxellana. Folia Primatol 37:209–215. CrossRefPubMedGoogle Scholar
  10. Dovrat G, Perevolotsky A, Ne’eman G (2012) Wild boars as seed dispersal agents of exotic plants from agricultural lands to conservation areas. J Arid Environ 78:49–54. CrossRefGoogle Scholar
  11. Fischer SF, Poschlod P, Beinlich B (1996) Experimental studies on the dispersal of plants and animals on sheep in calcareous grasslands. J Appl Ecol 33:1206–1222. CrossRefGoogle Scholar
  12. Habeck CW, Schultz AK (2015) Community-level impacts of white-tailed deer on understorey plants in North American forests: a meta-analysis. AoB Plants 7:plv119. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Heinken T, Raudnitschka D (2002) Do wild ungulates contribute to the dispersal of vascular plants in central European forests by epizoochory? A case study in NE Germany. Eur J For Res 121:179–194. Google Scholar
  14. Hernández Á, Zaldívar P (2013) Epizoochory in a hedgerow habitat: seasonal variation and selective diaspore adhesion. Ecol Res 28:283–295. CrossRefGoogle Scholar
  15. Kaplin BA, Moermond TC (1998) Variation in seed handling by two species of forest monkeys in Rwanda. Am J Primatol 45:83–101. CrossRefPubMedGoogle Scholar
  16. Kiviniemi K, Telenius A (1998) Experiments on adhesive dispersal by wood mouse: seed shadows and dispersal distances of 13 plant species from cultivated areas in southern Sweden. Ecography 21:108–116. CrossRefGoogle Scholar
  17. Kuijper DPJ, Cromsigt JPGM, Jędrzejewska B, Miścicki S, Churski M, Jędrzejewski W, Kweczlich I (2010) Bottom-up versus top-down control of tree regeneration in the Białowieża Primeval Forest, Poland. J Ecol 98:888–899. CrossRefGoogle Scholar
  18. Li Y (2001) The seasonal diet of the Sichuan snub-nosed monkey (Pygathrix roxellana) in Shennongjia Nature Reserve, China. Folia Primatol 72:40–43. CrossRefPubMedGoogle Scholar
  19. Li Y (2002) The seasonal daily travel in a group of Sichuan snub-nosed monkey (Pygathrix roxellana) in Shennongjia Nature Reserve, China. Primates 43:271–276. CrossRefGoogle Scholar
  20. Li Y (2006) Seasonal variation of diet and food availability in a group of Sichuan snub-nosed monkeys in Shennongjia Nature Reserve, China. Am J Primatol 68:217–233. CrossRefGoogle Scholar
  21. Li B, Pan R, Oxnard CE (2002) Extinction of snub-nosed monkeys in China during the past 400 years. Int J Primatol 23:1227–1244. CrossRefGoogle Scholar
  22. Li Y, Xu L, Ma Y, Yang J, Yang Y (2003) The species richness of nonvolant mammals in Shennongjia Nature Reserve, Hubei Province, China: distribution patterns along elevational gradient. Biodivers Sci 11:1–9. Google Scholar
  23. Li GL, Cong J, Lu H, Xue YD, Su XJ, Yang JY, Li DQ (2012) Numerical classification and ordination of forest communities in habitat of Sichuan snub-nosed monkey in Hubei Shennongjia National Nature Reserve. Acta Ecol Sin 32:7501–7511. CrossRefGoogle Scholar
  24. Li J, Cong J, Liu X, Zhou Y, Wang XL, Li GL, Li DQ (2015) Effect of tourist roads on mammal activity in Shennongjia National Nature Reserve based on the trap technique of infrared cameras. Chin J Ecol 34:2195–2200. Google Scholar
  25. Liu X, Stanford CB, Yang J, Yao H, Li Y (2013) Foods eaten by the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China, in relation to nutritional chemistry. Am J Primatol 75:860–871. CrossRefPubMedGoogle Scholar
  26. Liu Z, Liu G, Roos C, Wang Z, Xiang Z, Zhu P, Wang B, Ren B, Shi F, Pan H, Li M (2015) Implications of genetics and current protected areas for conservation of 5 endangered primates in China. Conserv Biol 29:1508–1517. CrossRefPubMedGoogle Scholar
  27. Manzano P, Malo JE (2006) Extreme long-distance seed dispersal via sheep. Front Ecol Environ 4:244–248. CrossRefGoogle Scholar
  28. Milotić T, Suyoto HN, Provoost S, Hoffmann M (2017) Herbivore-induced expansion of Helianthemum nummularium in grassland–scrub mosaic vegetation: circumstantial evidence for zoochory and indirect grazing impact. Plant Ecol. Google Scholar
  29. Righini N, Serio-Silva JC, Rico-Gray V, Martínez-Mota R (2004) Effect of different primate species on germination of Ficus (Urostigma) seeds. Zoo Biol 23:273–278. CrossRefGoogle Scholar
  30. Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353. CrossRefPubMedGoogle Scholar
  31. Sengupta A, McConkey KR, Radhakrishna S (2014) Seed dispersal by rhesus macaques Macaca mulatta in northern India. Am J Primatol 76:1175–1184. CrossRefPubMedGoogle Scholar
  32. Sorensen AE (1986) Seed dispersal by adhesion. Ann Rev Ecol Syst 17:443–463. CrossRefGoogle Scholar
  33. 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. Int J Primatol 23:1187–1204. CrossRefGoogle Scholar
  34. Su YJ, Ren RM, Yan KH, Li JJ, Zhou Y, Zhu Z, Hu Y (1998) Preliminary survey of the home range and ranging behavior of golden monkeys (Rhinopithecus roxellana) in Shennongjia National Natural Reserve, Hubei, China. In: Jablonski NG (ed) The natural history of the Doucs and Snub-nosed monkeys. World Scientific, Singapore, pp 255–268CrossRefGoogle Scholar
  35. Vild O, Hédl R, Kopecký M, Szabó P, Suchánková S, Zouhar V (2016) The paradox of long-term ungulate impact: increase of plant species richness in a temperate forest. Appl Veg Sci. Google Scholar
  36. Will H, Maussner S, Tackenberg O (2007) Experimental studies of diaspore attachment to animal coats: predicting epizoochorous dispersal potential. Oecologia 153:331–339. CrossRefPubMedGoogle Scholar
  37. Wu Z, Raven PH (1998) Flora of China: illustrations. Missouri Botanical Garden Press, MissouriGoogle Scholar
  38. Xiang ZF, Yang BH, Yu Y, Yao H, Grueter CC, Garber PA, Li M (2014) Males collectively defend their one-male units against bachelor males in a multi-level primate society. Am J Primatol 76:609–617. CrossRefPubMedGoogle Scholar
  39. Yao H, Liu X, Stanford C, Yang J, Huang T, Wu F, Li Y (2011) Male dispersal in a provisioned multilevel group of Rhinopithecus roxellana in Shennongjia Nature Reserve, China. Am J Primatol 73:1280–1288. CrossRefPubMedGoogle Scholar
  40. Yu Y, Xiang ZF, Yao H, Grueter CC, Li M (2013) Female snub-nosed monkeys exchange grooming for sex and infant handling. PLoS ONE 8:e74822. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Zhang P, Hu K, Yang B, Yang D (2016) Snub-nosed monkeys (Rhinopithecus spp.): conservation challenges in the face of environmental uncertainty. Sci Bull 5:345–348. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Evolutionary Ecology and Conservation BiologyCentral South University of Forestry and TechnologyChangshaChina
  2. 2.Shennongjia National ParkHubeiChina
  3. 3.National Forest Inventory and Design InstituteBeijingChina

Personalised recommendations