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Daily feeding rhythm in proboscis monkeys: a preliminary comparison with other non-human primates

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Abstract

In non-human primates, the daily feeding rhythm, i.e., temporal fluctuation in feeding activity across the day, has been described but has rarely received much analytical interpretation, though it may play a crucial part in understanding the adaptive significance of primate foraging strategies. This study is the first to describe the detailed daily feeding rhythm in proboscis monkeys (Nasalis larvatus) based on data collected from both riverbank and inland habitats. From May 2005 to May 2006, data on feeding behavior in a group of proboscis monkeys consisting of an alpha-male, six adult females and immatures was collected via continuous focal animal sampling technique in a forest along the Menanggul River, Sabah, Malaysia. In both the male and females, the highest peak of feeding activity was in the late afternoon at 15:00–17:00, i.e., shortly before sleeping. The differences in the feeding rhythm among the seasons appeared to reflect the time spent eating fruit and/or the availability of fruit; clearer feeding peaks were detected when the monkeys spent a relevant amount of time eating fruit, but no clear peak was detected when fruit eating was less frequent. The daily feeding rhythm was not strongly influenced by daily temperature fluctuations. When comparing the daily feeding rhythm of proboscis monkeys to that of other primates, one of the most common temporal patterns detected across primates was a feeding peak in the late afternoon, although it was impossible to demonstrate this statistically because of methodological differences among studies.

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References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  PubMed  CAS  Google Scholar 

  • Altmann SA (1998) Foraging for survival: yearling baboons in Africa. University of Chicago Press, Chicago

    Google Scholar 

  • Bennett EL (1986) Environmental correlates of ranging behaviour in the banded langur, Presbytis melalopho. Folia Primatol 47:26–38

    Article  PubMed  CAS  Google Scholar 

  • Bennett EL, Sebastian AC (1988) Social organization and ecology of proboscis monkeys (Nasalis larvatus) in mixed coastal forest in Sarawak. Int J Primatol 9:233–255

    Article  Google Scholar 

  • Boonratana R (1993) The ecology and behaviour of the proboscis monkey (Nasalis larvatus) in the lower Kinabatangan. Mahidol University, Thailand

    Google Scholar 

  • Boonratana R (2003) Feeding ecology of proboscis monkeys (Nasalis larvatus) in the lower Kinabatangan, Sabah, Malaysia. Sabah Parks Nat J 6:1–6

    Google Scholar 

  • Carlson BA, Rothman JM, Mitani JC (2013) Diurnal variation in nutrients and chimpanzee foraging behavior. Am J Primatol 75:342–349

    Article  PubMed  Google Scholar 

  • Caton JM (1999) Digestive strategy of the Asian colobine genus Trachypithecus. Primates 40:311–325

    Article  Google Scholar 

  • Chapman CA, Chapman LJ (1991) The foraging itinerary of spider monkeys: when to eat leaves? Folia Primatol 56:162–166

    Article  Google Scholar 

  • Chivers DJ (1977) The feeding behaviour of siamang (Symphalangus syndactylus). In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 355–382

    Google Scholar 

  • Chivers D (1994) Functional anatomy of the gastrointestinal tract. In: Davies A, Oates J (eds) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 205–227

    Google Scholar 

  • Clarke KR, Green RH (1988) Statistical design and analysis for a ‘biological effects’ study. Mar Ecol Prog Ser 46:213–226

    Article  Google Scholar 

  • Clutton-Brock TH (1974) Activity patterns of red colobus (Colobus badius tephrosceles). Folia Primatol 21:161–187

    Article  PubMed  CAS  Google Scholar 

  • Clutton-Brock TH (1977) Some aspects of intraspecific variation in feeding and ranging behaviour in primates. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys, and apes. Academic Press, London, pp 539–556

    Google Scholar 

  • Curtis DJ, Zaramody A, Martin RD (1999) Cathemerality in the mongoose lemur, Eulemur mongoz. Am J Primatol 47:279–298

    Article  PubMed  CAS  Google Scholar 

  • Dalgaard P (2002) Introductory statistics with R. Springer, New York

    Google Scholar 

  • Dasilva GL (1992) The western black-and-white colobus as a low-energy strategist: activity budgets, energy expenditure and energy intake. J Anim Ecol 61:79

    Article  Google Scholar 

  • Davies AG, Bennett EL, Waterman PG (1988) Food selection by two South-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biol J Linn Soc 34:33–56

    Article  Google Scholar 

  • Dela JDS (2007) Seasonal food use strategies of Semnopithecus vetulus nestor, at Panadura and Piliyandala, Sri Lanka. Int J Primatol 28:607–626

    Article  Google Scholar 

  • Dierenfeld ES, Koontz FW, Goldstein RS (1992) Feed intake, digestion and passage of the proboscis monkey (Nasalis larvatus) in captivity. Primates 33:399–405

    Article  Google Scholar 

  • Ding W, Zhao Q-K (2004) Rhinopithecus bieti at Tacheng, Yunnan: diet and daytime activities. Int J Primatol 25:583–598

    Article  Google Scholar 

  • Dunbar RIM (1977) Feeding ecology of gelada baboons: a preliminary report. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 251–273

    Google Scholar 

  • Fan P-F, Ni Q-Y, Sun G-Z, Huang B, Jiang X-L (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 29:1047–1057

    Article  Google Scholar 

  • Fashing PJ (2001) Activity and ranging patterns of guerezas in the Kakamega Forest: intergroup variation and implications for intragroup feeding competition. Int J Primatol 22:549–577

    Article  Google Scholar 

  • Gittins SP (1982) Feeding and ranging in the agile gibbon. Folia Primatol (Basel) 38:39–71

    Article  CAS  Google Scholar 

  • Glander KE (1978) Howling monkey’s feeding behaviour and plant secondary compounds: a study of strategies. In: Montgomery GC (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, pp 561–573

    Google Scholar 

  • 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 63:165–177

    Article  PubMed  Google Scholar 

  • Hanya G, Bernard H (2012) Fallback foods of red leaf monkeys (Presbytis rubicunda) in Danum Valley, Borneo. Int J Primatol 33:322–337

    Article  Google Scholar 

  • Hanya G, Kiyono M, Takafumi H, Tsujino R, Agetsuma N (2007) Mature leaf selection of Japanese macaques: effects of availability and chemical content. J Zool 273:140–147

    Article  Google Scholar 

  • Harrison MJS (1985) Time budget of the green monkey, Cercopithecus sabaeus: some optimal strategies. Int J Primatol 6:351–376

    Article  Google Scholar 

  • Kinzey WG (1977) Diet and feeding behaviour of Cellicebus torquatus. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 127–152

    Google Scholar 

  • Kirkpatrick RC, Zou RJ, Dierenfeld ES, Zhou HW (2001) Digestion of selected foods by Yunnan snub-nosed monkey Rhinopithecus bieti (Colobinae). Am J Phys Anthropol 114:156–162

    Article  PubMed  CAS  Google Scholar 

  • Koenig A, Borries C, Chalise MK, Winkler P (1997) Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). J Zool 243:215–235

    Article  Google Scholar 

  • Kosheleff VP, Anderson CNK (2009) Temperature’s influence on the activity budget, terrestriality, and sun exposure of chimpanzees in the Budongo Forest, Uganda. Am J Phys Anthropol 139:172–181

    Article  PubMed  Google Scholar 

  • Kruskal JB, Wish M (1978) Multidimensional scaling. Sage Beverly Hills, CA

    Google Scholar 

  • Marsh CW (1981) Time budget of Tana River red colobus. Folia Primatol 35:30–50

    Article  PubMed  CAS  Google Scholar 

  • Martin P, Bateson P (1993) Measuring behaviour: an introductory guide, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Maruhashi T (1980) Feeding behavior and diet of the Japanese monkey (Macaca fuscata yakui) on Yakushima Island, Japan. Primates 21:141–160

    Article  Google Scholar 

  • Maruhashi T (1981) Activity patterns of a troop of Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan. Primates 22:1–14

    Article  Google Scholar 

  • Matsuda I, Tuuga A, Higashi S (2009a) The feeding ecology and activity budget of proboscis monkeys. Am J Primatol 71:478–492

    Article  PubMed  Google Scholar 

  • Matsuda I, Tuuga A, Higashi S (2009b) Ranging behavior of proboscis monkeys in a riverine forest with special reference to ranging in inland forest. Int J Primatol 30:313–325

    Article  Google Scholar 

  • Matsuda I, Tuuga A, Higashi S (2010) Effects of water level on sleeping-site selection and inter-group association in proboscis monkeys: why do they sleep alone inland on flooded days? Ecol Res 25:475–482

    Article  Google Scholar 

  • Matsuda I, Tuuga A, Bernard H, Furuichi T (2012) Inter-individual relationships in proboscis monkeys: a preliminary comparison with other non-human primates. Primates 53:13–23

    Article  PubMed  Google Scholar 

  • Matsuda I, Tuuga A, Bernard H, Sugau J, Hanya G (2013) Leaf selection by two Bornean colobine monkeys in relation to plant chemistry and abundance. Sci Rep 3:1873

    PubMed Central  PubMed  CAS  Google Scholar 

  • McKey D, Waterman PG (1982) Ranging behaviour of a group of black colobus (Colobus satanas) in the Douala-Edea Reserve, Cameroon. Folia Primatol 39:264–304

    Article  PubMed  CAS  Google Scholar 

  • Milton K (1979) Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat 114:362–378

    Article  CAS  Google Scholar 

  • Murai T (2004) Social behaviors of all-male proboscis monkeys when joined by females. Ecol Res 19:451–454

    Article  Google Scholar 

  • Murai T, Mohamed M, Bernard H, Mahedi PA, Saburi R, Higashi S (2007) Female transfer between one-male groups of proboscis monkey (Nasalis larvatus). Primates 48:117–121

    Article  PubMed  Google Scholar 

  • Nakagawa N (1989) Activity budget and diet of patas monkeys in Kala Maloue National Park, Cameroon: a preliminary report. Primates 30:27–34

    Article  Google Scholar 

  • Newton P (1992) Feeding and ranging patterns of forest Hanuman langurs (Presbytis entellus). Int J Primatol 13:245–285

    Article  Google Scholar 

  • Oates JF (1977) The guereza and its food. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, New York, pp 276–319

    Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH (2010) Vegan: community ecology package, R package version 1.8–7 edn

  • Pollock JI (1977) The ecology and sociology of feeding in Indri indri. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 37–69

    Google Scholar 

  • Post DG (1981) Activity patterns of yellow baboons (Papio cynocephalus) in the Amboseli National Park, Kenya. Anim Behav 29:357–374

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • R-Development-Core-Team (2013) R: a language and environment for statistical computing. Foundation for statistical computing, Vienna

  • Robinson JG (1984) Diurnal variation in foraging and diet in the wedge-capped capuchin Cebus olivaceu. Folia Primatol 43:216–228

    Article  Google Scholar 

  • Robinson JG (1986) Seasonal variation in use of time and space by the wedge-capped capuchin monkeys, Cebus olivaceus: implications for foraging theory. Smithsonian Institution Press, Washington DC

    Google Scholar 

  • Rodman PS (1977) Feeding behaviour of orang-utans of the Kutai Nature Reserve, East Kalimantan. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 383–413

    Google Scholar 

  • Roper KM et al (2014) Vocal acoustics in the endangered proboscis monkey (Nasalis larvatus). Am J Primatol 76:192–201

    Article  PubMed  CAS  Google Scholar 

  • Salter RE, MacKenzie NA, Nightingale N, Aken KM, Chai PKP (1985) Habitat use, ranging behaviour, and food habits of the proboscis monkey, Nasalis larvatus (van Wurmb), in Sarawak. Primates 26:436–451

    Article  Google Scholar 

  • Schmidt-Nielsen D (1984) Animal physiology, 3rd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Schwarm A, Ortmann S, Wolf C, Streich WJ, Clauss M (2009) Passage marker excretion in red kangaroo (Macropus rufus), collared peccary (Pecari tajacu) and colobine monkeys (Colobus angolensis, C. polykomos, Trachypithecus johnii). J Exp Zool Part A 311:647–661

    Article  Google Scholar 

  • Sha JC, Hanya G (2013) Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis). Am J Primatol 75:581–592

    Article  PubMed  Google Scholar 

  • Sha JCM, Bernard H, Nathan S (2008) Status and conservation of proboscis monkeys (Nasalis larvatus) in Sabah, East Malaysia. Primate Conserv 23:107–120

    Article  Google Scholar 

  • Snaith TV, Chapman CA (2007) Primate group size and interpreting socioecological models: do folivores really play by different rules? Evol Anthropol 16:94–106

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry third edition. W. H. Freeman and Company, New York

  • Stanford CB (1991a) The capped langur in Bangladesh: behavioral ecology and reproductive tactics. S Karger Pub, New York

    Google Scholar 

  • Stanford CB (1991b) The diet of the capped langur (Presbytis pileata) in a moist deciduous forest in Bangladesh. Int J Primatol 12:199–216

    Article  Google Scholar 

  • Struhsaker TT (1975) Red colobus monkey, George B. Schaller edn. University of Chicago Press, Chicago

  • Struhsaker TT (1978) Food habits of five monkey species in the Kibale Forest, Uganda. In: Chivers DJ, Herbert J (eds) Recent advances in primatology, vol 1. Academic Press, New York, pp 225–248

    Google Scholar 

  • Sussman RW (1977) Feeding behaviour of Lemur catta and Lemur fulvus. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 1–36

    Google Scholar 

  • Tsuji Y, Kazahari N, Kitahara M, Takatsuki S (2008) A more detailed seasonal division of the energy balance and the protein balance of Japanese macaques (Macaca fuscata) on Kinkazan Island, northern Japan. Primates 49:157–160

    Article  PubMed  Google Scholar 

  • van Nijboer J, Clauss M, van de Put K, van der Kuilen J, Woutersee H, Beynen AC (2007) Influence of two different diets on fluid and particle retention time Javan langur (Trachypithecus auratus auratus). Der Zoologische Garten 77:36–46

    Article  Google Scholar 

  • 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 66:23–44

    Article  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York

    Book  Google Scholar 

  • Waser PM (1977) Feeding, ranging and group size in the mangabey Cercocebus albigena. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 183–222

    Google Scholar 

  • Waterman PG (1984) Food acquisition and processing as a function of plant chemistry. In: Chivers DJ, Wood BA, Bilsborough A (eds) Food acquisition and processing in primates. Plenum Press, New York, pp 177–211

    Chapter  Google Scholar 

  • Wrangham RW (1977) Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 503–538

    Google Scholar 

  • Yeager CP (1989) Feeding ecology of the proboscis monkey (Nasalis larvatus). Int J Primatol 10:497–530

    Article  Google Scholar 

  • Yeager CP (1991) Possible antipredator behavior associated with river crossings by proboscis monkeys (Nasalis larvatus). Am J Primatol 24:61–66

    Article  Google Scholar 

  • Zhou Q, Wei F, Huang C, Li M, Ren B, Luo B (2007) Seasonal variation in the activity patterns and time budgets of Trachypithecus francoisi in the Nonggang Nature Reserve, China. Int J Primatol 28:657–671

    Article  Google Scholar 

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Acknowledgments

We thank the Economic Planning Unit of the Malaysian Government, the Sabah Wildlife Department, the Sabah Forestry Department, the Kinabatangan Orangutan Conservation Project and our research assistants for support. The Economy Planning Unit of Malaysia permitted our study. I. Matsuda truly appreciates Y. Matsuda for supporting his field work. Advice and support has been generously supplied by S. Higashi, K. Watanabe, J. Yamagiwa, T. Furuichi, G. Hanya, H. Takemoto, Y. Tsuji, A. MacIntosh, C. C. Grueter, C. Tan, P. J. Fashing, and R. Boonratana. This study was partly financed by HOPE and Human Evolution Project of KUPRI and JSPS Grant-in-Aid for Challenging Exploratory Research (24657170) to I. Matsuda and for Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation, to KUPRI. The study includes data collected and analyzed using protocols approved by the Economic Planning Unit, Prime Minister’s Department, Putrajaya, Malaysia and the Sabah Wildlife Department, Sabah, Malaysia, and such protocols adhere to the legal requirements of Malaysia.

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Authors and Affiliations

  1. Primate Research Institute, Kyoto University, Inuyama, Aichi, 484-8506, Japan

    Ikki Matsuda

  2. Environmental Research and Management Center, Hiroshima University, Higashi-hiroshima, Japan

    Yoshihiro Akiyama

  3. Sabah Wildlife Department, Kota Kinabalu, Sabah, Malaysia

    Augustine Tuuga

  4. Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia

    Henry Bernard

  5. Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland

    Marcus Clauss

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  1. Ikki Matsuda
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Correspondence to Ikki Matsuda.

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Matsuda, I., Akiyama, Y., Tuuga, A. et al. Daily feeding rhythm in proboscis monkeys: a preliminary comparison with other non-human primates. Primates 55, 313–326 (2014). https://doi.org/10.1007/s10329-014-0407-5

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