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Primates

, Volume 56, Issue 4, pp 351–363 | Cite as

Effects of food availability and climate on activity patterns of western black-crested gibbons in an isolated forest fragment in southern Yunnan, China

  • Qingyong NiEmail author
  • Meng Xie
  • Cyril C. Grueter
  • Xuelong Jiang
  • Huailiang Xu
  • Yongfang Yao
  • Mingwang Zhang
  • Yan Li
  • Jiandong Yang
Original Article

Abstract

The critically endangered western black-crested gibbon (Nomascus concolor) is distributed in isolated habitat fragments in northern Vietnam, northwestern Laos, and southwestern China. To assess the behavioral adaptation of this species to forest fragments and its response to seasonal variation in food availability and climate, we present activity patterns of a group inhabiting an isolated forest based on two year-long studies in southern Yunnan, China. Annually, the gibbons spent nearly half of their active time resting, followed by moving and feeding. In both study periods, the time allocated to activities varied significantly between months, and was affected by food availability and climate factors. The group delayed retirement when tree fruit was abundant, and they decreased time spent moving and playing during periods of low fruit availability. In the cold months, the gibbons decreased time spent moving, and they decreased active time and resting time when rainfall was high. The results suggest that the group may seek to maximize net energy intake like energy maximizers when high quality food is most available, and adopt an energy-conserving strategy during periods of lower food availability and temperature. The gibbons showed similar diurnal variation in activity patterns to a group inhabiting a continuous forest at Dazhaizi, Mt. Wuliang, central Yunnan. However, they had a longer active period, and devoted more time to resting but less time to feeding. The individuals also spent lower percentages of time engaged in social behavior than those at Dazhaizi. These differences may be due to their smaller home range and unusual group composition caused by habitat fragmentation.

Keywords

Time budget Nomascus concolor Seasonal variation Temperature and rainfall Habitat fragmentation 

Notes

Acknowledgments

This study was supported by the National Natural Science Foundation of China (31301892, 31070349). We thank the Forestry Bureau of Honghe Prefecture and local governments at Bajiaohe and Yingpan Township. We also thank our field assistants, Mr. Liang Zongli, Mr. Huang Yao and Mr. Deng Ruo for their kind help. We are grateful to Dr. Warren Brockelman, Dr. Thad Q. Bartlett and one anonymous reviewer for constructive comments on the manuscript.

References

  1. Achard F, Eva HD, Stibig HJ, Mayaux P, Gallego J, Richards T, Malingreau JP (2002) Determination of deforestation rates of the world’s humid tropical forests. Science 297:999–1002CrossRefPubMedGoogle Scholar
  2. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  3. Arroyo-Rodríguez V, Dias PAD (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1–16CrossRefPubMedGoogle Scholar
  4. Arroyo-Rodríguez V, Mandujano S (2006) Forest fragmentation modifies habitat quality for Alouatta palliata. Int J Primatol 27:1079–1096CrossRefGoogle Scholar
  5. Bartlett TQ (2007) The Hylobatidae: small apes of Asia. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 274–289Google Scholar
  6. Barton RA, Whiten A, Strum SC, Byrne RW, Simpson AJ (1992) Habitat use and resource availability in baboons. Anim Behav 43:822–831CrossRefGoogle Scholar
  7. Boyle SA, Smith AT (2010) Behavioral modifications in northern bearded saki monkeys (Chiropotes satanas chiropotes) in forest fragments of central Amazonia. Primates 51:43–51CrossRefPubMedGoogle Scholar
  8. Brockelman WY, Nathalang A, Greenberg DB, Suwanvecho U (2014) Evolution of small-group territoriality in gibbons. Springer, Primates and Cetaceans, pp 213–230Google Scholar
  9. Bronikowski AM, Altmann J (1996) Foraging in a variable environment: weather patterns and the behavioral ecology of baboons. Behav Ecol Sociobiol 39:11–25CrossRefGoogle Scholar
  10. Chapman CA, Peres CA (2001) Primate conservation in the new millennium: the role of scientists. Evol Anthropol 10:16–33CrossRefGoogle Scholar
  11. Chaves ÓM, Stoner KE, Arroyo-Rodríguez V (2011) Seasonal differences in activity patterns of Geoffroyi’s spider monkeys (Ateles geoffroyi) living in continuous and fragmented forests in southern Mexico. Int J Primatol 32:960–973CrossRefGoogle Scholar
  12. Chivers DJ (1974) The siamang in Malaya: a field study of a primate in a tropical rain forest. In: Kuhn H, Luckett WP, Noback CR, Schultz AH, Starck D, Szalay FS (eds) Contributions to primatology. Karger, Basel, 4:1–335Google Scholar
  13. Defler TR (1995) The time budget of a group of wild woolly monkeys (Lagothrix lagotricha). Int J Primatol 16:107–120CrossRefGoogle Scholar
  14. Doran D (1997) Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. Int J Primatol 18:183–206CrossRefGoogle Scholar
  15. Dunbar RIM (1988) Primate social systems. Chapman & Hall, LondonCrossRefGoogle Scholar
  16. Dunbar RIM (1992) A model of the gelada socio-ecological system. Primates 33:69–83CrossRefGoogle Scholar
  17. Dunbar RIM, Korstjens AH, Lehmann J (2009) Time as an ecological constraint. Biol Rev 84:413–429CrossRefPubMedGoogle Scholar
  18. Estrada A, Juan-Solano S, Martinez TO, Coates-Estrada R (1999) Feeding and general activity patterns of a howler monkey (Alouatta palliata) troop living in a forest fragment at Los Tuxtlas, Mexico. Am J Primatol 48:167–183CrossRefPubMedGoogle Scholar
  19. Fan PF (2007) The ecology and behavior of black crested gibbon (Nomascus concolor jingdongensis) at Dazhaizi, Wuliang Mountain, Central Yunnan, China Ph.D. thesis. Beijing: Graduate School of Chinese Academy of SciencesGoogle Scholar
  20. Fan PF, Jiang XL (2008) Effects of food and topography on ranging behavior of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang Mountain, Yunnan, China. Am J Primatol 70:871–878CrossRefPubMedGoogle Scholar
  21. Fan PF, Ni QY, Sun GZ, Huang B, Jiang XL (2008) Seasonal variations in the activity budget of Nomascus concolor jingdongensis at Mt. Wuliang, Central Yunnan, China: effects of diet and temperature. Int J Primatol 29:1047–1057CrossRefGoogle Scholar
  22. Fan PF, Jiang XL, Tian CC (2009a) The critically endangered black crested gibbon Nomascus concolor on Wuliang Mountain, Yunnan, China: the role of forest types in the species’ conservation. Oryx 43:1–6CrossRefGoogle Scholar
  23. Fan PF, Ni QY, Sun GZ, Huang B, Jiang XL (2009b) Gibbon under seasonal stress: the diet of the black crested gibbon (Nomascus concolor) on Mt. Wuliang, Central Yunnan China. Primates 50:37–44CrossRefPubMedGoogle Scholar
  24. Fan PF, Fei HL, Ma CY (2012) Behavioral responses of cao vit gibbon (Nomascus nasutus) to variations in food abundance and temperature in Bangliang, Jingxi, China. Am J Primatol 74:632–641CrossRefPubMedGoogle Scholar
  25. Fan PF, Ai HS, Fei HL, Zhang D, Yuan SD (2013) Seasonal variation of diet and time budget of eastern hoolock gibbons (Hoolock leuconedys) living in a northern montane forest. Primates 54:137–146CrossRefPubMedGoogle Scholar
  26. Gittins S (1982) Feeding and ranging in the agile gibbon. Folia Primatol 38:39–71CrossRefPubMedGoogle Scholar
  27. Grueter CC, Li DY, Ren BP, Wei FW, Xiang ZF, van Schaik CP (2009) Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. Am J Phys Anthropol 140:700–715CrossRefPubMedGoogle Scholar
  28. Grueter CC, Li DY, Ren BP, Li M (2013) Overwintering strategy of Yunnan snub-nosed monkeys: adjustments in activity scheduling and foraging patterns. Primates 54:125–135CrossRefPubMedGoogle Scholar
  29. Hanya G (2004) Seasonal variations in the activity budget of Japanese macaques in the coniferous forest of Yakushima: effects of food and temperature. Am J Primatol 63:165–177CrossRefPubMedGoogle Scholar
  30. Harrison MJS (1985) Time budget of the green monkey, Cercopithecus sabaeus: some optimal strategies. Int J Primatol 6:351–376CrossRefGoogle Scholar
  31. Hill R, Barrett L, Gaynor D, Weingrill T, Dixon P, Payne H, Henzi S (2003) Day length, latitude and behavioural (in)flexibility in baboons (Papio cynocephalus ursinus). Behav Ecol Sociobiol 53:278–286Google Scholar
  32. Hixon MA (1980) Food production and competitor density as the determinants of feeding territory size. Am Nat 115:510–530CrossRefGoogle Scholar
  33. Hixon MA (1982) Energy maximizers and time minimizers: theory and reality. Am Nat 119:596–599CrossRefGoogle Scholar
  34. Huang B (2011) The ecological and behavioural adaption of black-crested gibbon (Nomascus concolor) to the habitat at Dazhaizi, Wuliang Mountain, central Yunnan, China Ph.D. thesis. Beijing, China: Graduate School of Chinese Academy of SciencesGoogle Scholar
  35. Iwamoto T, Dunbar R (1983) Thermoregulation, habitat quality and the behavioural ecology of gelada baboons. J Anim Ecol 53:357–366CrossRefGoogle Scholar
  36. Kapos V, Wandelli E, Camargo J, Ganade G (1997) Edge-related changes in environment and plant responses due to forest fragmentation in central Amazonia. Trop For Remn Ecol Manag Conserv Fragm Commun Univ Chic Press Chic 101:33–44Google Scholar
  37. Kurup G, Kumar A (1993) Time budget and activity patterns of the lion-tailed macaque (Macaca silenus). Int J Primatol 14:27–39CrossRefGoogle Scholar
  38. Laurance WF, Laurance SG, Ferreira LV, Rankin-de Merona JM, Gascon C, Lovejoy TE (1997) Biomass collapse in Amazonian forest fragments. Science 278:1117–1118CrossRefGoogle Scholar
  39. Laurance WF, Ferreira LV, Merona JM, Laurance SG, Hutchings RW, Lovejoy TE (1998) Effects of forest fragmentation on recruitment patterns in Amazonian tree communities. Conserv Biol 12:460–464CrossRefGoogle Scholar
  40. Leighton DR (1987) Gibbons: Territoriality and monogamy. In: Smuts B, Cheney D, Seyfarth R, Wrangham R, Struhsaker T (eds) Primate Societies. Chicago University Press, Chicago, pp 135–145Google Scholar
  41. Majolo B, McFarland R, Young C, Qarro M (2013) The effect of climatic factors on the activity budgets of Barbary macaques (Macaca sylvanus). Int J Primatol 34:500–514CrossRefGoogle Scholar
  42. Menon S, Poirier FE (1996) Lion-tailed macaques (Macaca silenus) in a disturbed forest fragment: activity patterns and time budget. Int J Primatol 17:969–985CrossRefGoogle Scholar
  43. Ni QY, Jiang XL (2009) Crested gibbons in southeastern Yunnan, China: status and conservation. Gibbon J 5:36–43Google Scholar
  44. Ni QY, Huang B, Liang ZL, Wang XW, Jiang XL (2014) Dietary variability in the western black crested gibbon (Nomascus concolor) inhabiting an isolated and disturbed forest fragment in southern Yunnan, China. Am J Primatol 76:217–229CrossRefPubMedGoogle Scholar
  45. Norberg RA (1977) An ecological theory on foraging time and energetics and choice of optimal food-searching method. J Anim Ecol 46:511–529CrossRefGoogle Scholar
  46. Onderdonk DA, Chapman CA (2000) Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21:587–611CrossRefGoogle Scholar
  47. Passamani M (1998) Activity budget of Geoffroyʼs marmoset (Callithrix geoffroyi) in an Atlantic forest in southeastern Brazil. Am J Primatol 46:333–340CrossRefPubMedGoogle Scholar
  48. Pavelka MS, Knopff KH (2004) Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: does degree of frugivory influence activity level? Primates 45:105–111CrossRefPubMedGoogle Scholar
  49. Raemaekers J (1978) Changes through the day in the food choice of wild gibbons. Folia Primatol 30:194–205CrossRefPubMedGoogle Scholar
  50. Raemaekers J (1979) Ecology of sympatric gibbons. Folia Primatol 31:227–245CrossRefPubMedGoogle Scholar
  51. Raemaekers J (1980) Causes of variation between months in the distance traveled daily by gibbons. Folia Primatol 34:46–60CrossRefPubMedGoogle Scholar
  52. Reichard U (1998) Sleeping sites, sleeping places, and presleep behavior of gibbons (Hylobates lar). Am J Primatol 46:35–62CrossRefPubMedGoogle Scholar
  53. Sayers K, Norconk MA (2008) Himalayan Semnopithecus entellus at Langtang National Park, Nepal: diet, activity patterns, and resources. Int J Primatol 29:509–530CrossRefGoogle Scholar
  54. Schoener TW (1971) Theory of feeding strategies. Ann Rev Ecol Syst 2:369–404CrossRefGoogle Scholar
  55. Schwarzkopf L, Rylands AB (1989) Primate species richness in relation to habitat structure in Amazonian rainforest fragments. Biol Conserv 48:1–12CrossRefGoogle Scholar
  56. Silva SS, Ferrari SF (2009) Behavior patterns of southern bearded sakis (Chiropotes satanas) in the fragmented landscape of eastern Brazilian Amazonia. Am J Primatol 71:1–7CrossRefPubMedGoogle Scholar
  57. Van Doorn AC, O’Riain MJ, Swedell L (2010) The effects of extreme seasonality of climate and day length on the activity budget and diet of semi-commensal chacma baboons (Papio ursinus) in the Cape Peninsula of South Africa. Am J Primato 72:104–112Google Scholar
  58. Vasey N (2005) Activity budgets and activity rhythms in red ruffed lemurs (Varecia rubra) on the Masoala Peninsula, Madagascar: seasonality and reproductive energetics. Am J Primatol 66:23–44CrossRefPubMedGoogle Scholar
  59. Wong SN, Sicotte P (2007) Activity budget and ranging patterns of Colobus vellerosus in forest fragments in central Ghana. Folia Primatol 78:245–254CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2015

Authors and Affiliations

  • Qingyong Ni
    • 1
    Email author
  • Meng Xie
    • 2
  • Cyril C. Grueter
    • 3
  • Xuelong Jiang
    • 4
  • Huailiang Xu
    • 1
  • Yongfang Yao
    • 1
  • Mingwang Zhang
    • 1
  • Yan Li
    • 1
  • Jiandong Yang
    • 1
  1. 1.College of Animal Sciences and TechnologySichuan Agricultural UniversityChengduPeople’s Republic of China
  2. 2.College of Life SciencesSichuan Agricultural UniversityYaanPeople’s Republic of China
  3. 3.School of Anatomy, Physiology and Human BiologyThe University of Western AustraliaCrawleyAustralia
  4. 4.State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of ZoologyChinese Academy of SciencesKunmingPeople’s Republic of China

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