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Development and behavior of wild infant-juvenile East Bornean orangutans (Pongo pygmaeus morio) in Danum Valley

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  • Research and Conservation of Orangutans (Pongo sp.) in Malaysia
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An Erratum to this article was published on 06 January 2017

Abstract

Orangutans have a long period of immaturity and the longest inter-birth interval (IBI) of all mammals, which can explained by their solitary life style, preventing the mother from rearing two offspring simultaneously (solitary life hypothesis). We collected data on mother-offspring dyads living in a primary lowland forest in Danum Valley, East Borneo in an effort to examine the developmental and behavioral patterns of the subspecies Pongo pygmaeus morio. We analyzed developmental changes in mother-offspring distance, contact, and activity budgets in orangutans ranging from 1 to 7 years of age. The results indicated decreased resting and playing with increasing age, whereas feeding, traveling and social play all increased significantly. Mothers’ feeding and traveling time were good predictors of their offspring’s feeding and traveling activities. Mother-offspring contact lasted longer in resting contexts; contact during traveling was almost non-existent after 4 years of age. Comparisons with previously published data on the Sumatran species Pongo abelli revealed no fundamental differences in these behavioral measures. However, a shorter association time with the mother after behavioral independence is documented for this East Bornean population in comparison to Sumatran populations. These results are best explained by the solitary life hypothesis, in agreement with previous studies. We suggest that environmental constraints in Bornean forests, as well as a lower population density, should be considered when interpreting the differences between Sumatran and Bornean orangutans in both the period of association with mother and the IBI.

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References

  • Altmann J (1980) Baboon mothers and infants. University of Chicago Press, Chicago

    Google Scholar 

  • Ancrenaz M, Gimenez O, Ambu L, Ancrenaz K, Andau P, Goossens B, Sawang A, Tuuga A, Lackman-Ancrenaz I (2004) Aerial surveys give new estimates for orangutans in Sabah, Malaysia. PLoS Biol 3:e3. doi:10.1371/journal.pbio.0030003

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashton PS, Givinish TJ, Appanah S (1988) Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting. Am Nat 132:44–66

    Article  Google Scholar 

  • Bercovitch FB, Berard JD (1993) Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32:103–109

    Article  Google Scholar 

  • Biro D, Inoue-Nakamura N, Tonooka R, Yamakoshi G, Sousa C, Matsuzawa T (2003) Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments. Anim Cogn 6:213–223. doi:10.1007/s10071-003-0183-x

    Article  PubMed  Google Scholar 

  • Byers JA, Walker C (1995) Refining the motor training hypothesis for the evolution of play. Am Nat 146:25–40

    Article  Google Scholar 

  • Chappell J, Phillips AC, van Noordwijk MA, Mitra Setia T, Thrope SKS (2015) The Ontogeny of gap crossing behaviour in Bornean orangutans (Pongo pygmaeus wurmbii). PLoS One 10:e0130291. doi:10.1371/journal.pone.0130291

    Article  PubMed  PubMed Central  Google Scholar 

  • Delgado RA, Van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9:201–218

    Article  Google Scholar 

  • Doran DM (1997) Ontogeny of locomotion in mountain gorillas and chimpanzees. J Hum Evol 32:323–344

    Article  CAS  PubMed  Google Scholar 

  • Douglas B, Martin M, Ben B (2012) lme4: linear mixed-effects models using S4 classes. RStudio, Boston

    Google Scholar 

  • Fagen R (1993) Primate juvenile and primate play. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. Oxford University Press, Oxford, pp 182–196

    Google Scholar 

  • Fairbanks LA (1988) Vervet monkey grandmothers: effects on mother-infant relationships. Behaviour 104:176–188

    Article  Google Scholar 

  • French JA (1981) Individual differences in play in Macaca fuscata: the role of maternal status and proximity. Int J Primatol 2:237–246

    Article  Google Scholar 

  • Furuichi T, Idani G, Ihobe H, Kuroda S, Kitamura K, Mori A, Enomoto T, Okayasu N, Hashimoto C, Kano T (1998) Population dynamics of wild bonobos (Pan paniscus) at Wamba. Int J Primatol 19:1029–1043

    Article  Google Scholar 

  • Galdikas BMF (1995) Social and reproductive behavior of wild adolescent female orangutans. In: Nadler RD, Galdikas BFM, Sheeran LK, Rosen N (eds) The neglected ape. Springer, New York, pp 163–182

    Chapter  Google Scholar 

  • Galdikas BMF, Wood JW (1990) Birth spacing patterns in humans and apes. Am J Phys Anthropol 83:185–191

    Article  CAS  PubMed  Google Scholar 

  • Harrison ME, Vogel ER, Morrogh-Bernard HC, van Noordwijk MA (2009) Methods for calculating activity budgets compared: a case study using orangutans. Am J Primatol 71:353–358

    Article  PubMed  Google Scholar 

  • Hazebroek HP, Adlin TZ, Sinum W (2012) Danum Valley: the rain forest. Natural History Publications, Kota Kinabalu

    Google Scholar 

  • Hinde RA, Atkinson S (1970) Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys. Anim Behav 18:169–176

    Article  Google Scholar 

  • Hiraiwa-Hasegawa M (1990a) Maternal investment before weaning. In: Nishida T (ed) The chimpanzees of the Mahale mountains: sexual and life history strategies. University of Tokyo Press, Tokyo, pp 257–266

    Google Scholar 

  • Hiraiwa-Hasegawa M (1990b) The role of food sharing between mother and infant in the ontogeny of feeding behavior. In: Nishida T (ed) The chimpanzees of Mahale mountains: sexual and life history strategies. Tokyo University Press, Tokyo, pp 267–275

    Google Scholar 

  • Hiraiwa-Hasegawa M (1990c) A note on the ontogeny of feeding. In: Nishida T (ed) The chimpanzees of Mahale mountains: sexual and life history strategies. Tokyo University Press, Tokyo, pp 277–283

    Google Scholar 

  • Husson SJ, Wich SA, Marshall AJ, Dennis RD, Ancrenaz M, Brassey R, Gumal M, Hearn AJ, Meijaard E, Simorangkir T, Singleton I (2009) Orangutan distribution, density, abundance and impacts of disturbance. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 77–96

    Google Scholar 

  • Janson CH, van Schaik CP (1993) Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. Oxford University Press, Oxford, pp 57–74

    Google Scholar 

  • Jaeggi AV, van Noordwijk MA, van Schaik CP (2008) Begging for information: mother-offspring food sharing among wild Bornean orangutans. Am J Primatol 70:533–541

    Article  PubMed  Google Scholar 

  • Jaeggi AV, Dunkel LP, van Noordwijk MA, Wich SA, Sura AAL, van Schaik CP (2010) Social learning of diet and foraging skills by wild immature Bornean orangutans: implications for culture. Am J Primatol 72:62–71

    Article  PubMed  Google Scholar 

  • Jones WT, Waser PM, Elliott LF, Link NE, Bush BB (1988) Philopatry, Ddispersal, and habitat saturation in the banner-tailed kanagaroo rat, Dipodomys Spectabilis. Ecology 69:1466. doi:10.2307/1941643

    Article  Google Scholar 

  • Kanamori T, Kuze N, Bernard H, Malim PT, Kohshima S (2010) Feeding ecology of Bornean orangutans (Pongo pygmaeus morio) in Danum Valley, Sabah, Malaysia: a 3-year record including two mast fruitings. Am J Primatol 72:820–840

    Article  PubMed  Google Scholar 

  • Kanamori T, Kuze N, Bernard H, Malim PT, Kohshima S (2012) Fatality of a wild Bornean orangutan (Pongo pygmaeus morio): behavior and death of a wounded juvenile in Danum Valley, North Borneo. Primates 53:221–226

    Article  PubMed  Google Scholar 

  • Kanamori T, Kuze N, Bernard H, Malim TP, Kohshima S (2016) Fluctuations of population density in Bornean orangutans (Pongo pygmaeus morio) related to fruit availability in Danum Valley, Sabah, Malaysia: a 10-year record including five mast fruitings. Primates (in Press)

  • Kaplan H, Hill K, Lancaster J, Hurtado AM (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9:156–185

    Article  Google Scholar 

  • Kelley J, Schwartz GT (2010) Dental development and life history in living African and Asian apes. Proc Natl Acad Sci USA 107:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Knott CD (1998) Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19:1061–1079

    Article  Google Scholar 

  • Knott CD (2001) Female reproductive ecology of the apes: implications for human evolution. In: Ellison PT (ed) Reproductive ecology and human evolution. Walter de Gruyter, Hawthorne, pp 429–463

    Google Scholar 

  • Knott CD, Thompson ME, Wich SA (2009) The ecology of female reproduction in wild orangutans. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 171–188

    Google Scholar 

  • Kokko H, Lundberg P (2001) Dispersal, migration, and offspring retention in saturated habitats. Am Nat 157:188–202

    Article  CAS  PubMed  Google Scholar 

  • Kuze N, Malim TP, Kohshima S (2005) Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus): possible signals in visual communication. Am J Primatol 65:353–376

    Article  PubMed  Google Scholar 

  • Maestripieri D, Ross SR (2004) Sex differences in play among western lowland gorilla (Gorilla gorilla gorilla) infants: implications for adult behavior and social structure. Am J Phys Anthropol 123:52–61. doi:10.1002/ajpa.10295

    Article  PubMed  Google Scholar 

  • Manduell KL, Harrison ME, Thorpe SKS (2012) Forest structure and support availability influence orangutan locomotion in Sumatra and Borneo: habitat effects on orangutan locomotion. Am J Primatol 74:1128–1142. doi:10.1002/ajp.22072

    Article  PubMed  Google Scholar 

  • Marshall AJ, Ancrenaz M, Brearley FQ, Fredriksson GM, Ghaffar N, Heydon MJ (2009) The effects of forest phenology and floristics on populations of Bornean and Sumatran orangutans. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 97–118

    Google Scholar 

  • Martin PR, Bateson PP (1993) Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Mitra Setia T, Delgado RA, Utami Atmoko SS, Singleton I, van Schaik CP (2009) Social organization and male–female relationships. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 245–253

    Google Scholar 

  • Morrogh-Bernard HC, Husson SJ, Knott CD, Wich SA, van Schaik CP, van Noordwijk MA, Lackman-Ancrenaz I, Marshall AJ, Kanamori T, Kuze N, Bin Sakong R (2009) Orangutan activity budgets and diet. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 119–134

    Google Scholar 

  • Pagel MD, Harvey PH (1993) Evolution of the juvenile period in mammals. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, pp 28–37

    Google Scholar 

  • Pontzer H, Raichlen DA, Shumaker RW, Ocobock C, Wich SA (2010) Metabolic adaptation for low energy throughput in orangutans. Proc Natl Acad Sci USA 107:14048–14052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pusey AE (1983) Mother-offspring relationships in chimpanzees after weaning. Anim Behav 31:363–377

    Article  Google Scholar 

  • Pusey AE (1990) Behavioural changes at adolescence in chimpanzees. Behaviour 115:203–246

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • R Studio (2015) R Studio: integrated development environment for R. R Studio, Boston, MA

    Google Scholar 

  • Robbins AM, Robbins MM, Gerald-Steklis N, Steklis HD (2006) Age-related patterns of reproductive success among female mountain gorillas. Am J Phys Anthropol 131:511–521. doi:10.1002/ajpa.20474

    Article  PubMed  Google Scholar 

  • Robbins AM, Stoinski T, Fawcett K, Robbins MM (2011) Lifetime reproductive success of female mountain gorillas. Am J Phys Anthropol 146:582–593. doi:10.1002/ajpa.21605

    Article  PubMed  Google Scholar 

  • Robson SL, Wood B (2008) Hominin life history: reconstruction and evolution. J Anat 212:294–425

    Article  Google Scholar 

  • Ross C (2001) Park or ride? Evolution of infant carrying in primates. Int J Primatol 22:749–771

    Article  Google Scholar 

  • Ross C, Jones KE (1999) Socioecology and the evolution of primate reproductive rates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 73–110

    Chapter  Google Scholar 

  • Russon AE (2006) Acquisition of complex foraging skills in juvenile and adolescent orangutans (Pongo pygmaeus): developmental influences. Aquat Mamm 32:500–510. doi:10.1578/AM.32.4.2006.500

    Article  Google Scholar 

  • Shimada M (2013) Dynamics of the temporal structures of playing clusters and cliques among wild chimpanzees in Mahale Mountains National Park. Primates 54:245–257

    Article  PubMed  Google Scholar 

  • Shimada M, Sueur C (2014) The importance of social play network for infant or juvenile wild chimpanzees at Mahale Mountains National Park, Tanzania: social play networks in wild chimpanzees. Am J Primatol 76:1025–1036. doi:10.1002/ajp.22289

    Article  PubMed  Google Scholar 

  • Singleton I, Knott CD, Morrogh-Bernard HC, Wich SA, van Schaik CP (2009) Ranging behavior of orangutan females and social organization. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 205–212

    Google Scholar 

  • Spinka M, Newberry NC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168

    Article  CAS  PubMed  Google Scholar 

  • Stacey PB (1979) Habitat saturation and communal breeding in the acorn woodpecker. Animal Behav 27:1153–1166

    Article  Google Scholar 

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  • Stoinski TS, Perdue B, Breuer T, Hoff MP (2013) Variability in the developmental life history of the genus Gorilla: gorilla developmental life history. Am J Phys Anthropol 152(2):165–172

    PubMed  Google Scholar 

  • Thompson ME (2013) Reproductive ecology of female chimpanzees: chimpanzee reproductive ecology. Am J Primatol 75:222–237. doi:10.1002/ajp.22084

    Article  PubMed  Google Scholar 

  • Thompson ME, Jones JH, Pusey AE, Brewe-Marsden S, Goodall J, Marsden D, Tetsuro M, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW (2007) Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 17:2150–2156. doi:10.1016/j.cub.2007.11.033

    Article  CAS  PubMed Central  Google Scholar 

  • van Adrichem GGJ, Utami SS, Wich SA, van Hoff JARAM, Sterck HM (2006) The development of wild immature Sumatran orangutans (Pongo abelii) at Ketambe. Primates 47:300–309

    Article  PubMed  Google Scholar 

  • van de Rijt-Plooij HHC, Plooij FX (1987) Growing independence, conflict and learning in mother–infant relations in free-ranging chimpanzees. Behaviour 101:1–86

    Article  Google Scholar 

  • van Noordwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79–94

    Article  PubMed  Google Scholar 

  • van Noordwijk MA, Sauren SEB, Nuzuar AA, Morrogh-Bernard HC, Utami Atmoko SS (2009) Development of independence: Sumatran and Bornean orangutans compared. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 189–203

    Google Scholar 

  • van Noordwijk MA, Arora N, Willems EP, Dunkel LP, Amda RN, Mardianah N, Ackermann C, Krützen M, van Schaik CP (2012) Female philopatry and its social benefits among Bornean orangutans. Behav Ecol Sociobiol 66:823–834

    Article  Google Scholar 

  • van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144

    Article  Google Scholar 

  • van Schaik CP (1999) The socioecology of fission–fusion sociality in orangutans. Primates 40:69–86

    Article  PubMed  Google Scholar 

  • van Schaik CP, Deaner RO (2003) Life history and cognitive evolution in primates. In: de Waal FBM, Tyack PL (eds) Animal social complexity. Harvard University Press, Cambridge, pp 5–25

    Google Scholar 

  • van Schaik CP, Pfannes KR (2005) Tropical climates and phenology: a primate perspective. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, New York, pp 23–44

    Chapter  Google Scholar 

  • van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377

    Article  Google Scholar 

  • Watts DP (1991) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–225

    Article  Google Scholar 

  • Watts DP, Pusey AE (1993) Behavior of juvenile and adolescent great apes. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, pp 148–167

    Google Scholar 

  • Wich SA, van Schaik CP (2000) The impact of El Niño on mast fruiting in Sumatra and elsewhere in Malesia. J Trop Ecol 16:563–577

    Article  Google Scholar 

  • Wich SA, Utami-Atmoko SS, Setia TM, Rijksen HD, Schürmann C, van Hoff JARAM, van Schaik CP (2004) Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol 47:385–398. doi:10.1016/j.jhevol.2004.08.006

    Article  CAS  PubMed  Google Scholar 

  • Wich SA, De Vries H, Ancrenaz M, Perkins L, Shumaker RW, Suzuki A, van Schaik CP (2009) Orangutan life history variation. In: Wich SA, Atmoko SSU, Tantang MS, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 65–75

    Google Scholar 

  • Wich SA, Vogel ER, Larsen MD, Fredriksson G, Leighton M, Yeager CP, Brealey FQ, van Schaik CP, Marshall AJ (2011) Forest fruit production is higher on Sumatra than on Borneo. PLoS One 6:e21278. doi:10.1371/journal.pone.0021278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10

    Google Scholar 

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Acknowledgments

We would like to thank to our local collaborator Mr Peter Malim, as well as the Sabah Biodiversity Centre and Danum Valley Management Committee for granting permission to conduct the research. We are also grateful to research assistants Eddy Boy, Poleh Bin Inging and Kirmizi Bin Rosliu for their help during the fieldwork, and to the staff of Borneo Rainforest Lodge for assistance provided during our stay there. Furthermore, we would like to thank Dr Fred Bercovitch, Dr Mike Huffman, Dr Anne Russon and anonymous reviewers for valuable comments on the manuscript. Our study was supported by a Grant-in-Aid for Specially Promoted Research from the Ministry of Education, Science, Sports and Culture, Japan (no. 24000001) to T. M.; a scholarship to R. S. M. (ITP-HOPE project; ITP-25-016), a Japan Society for the Promotion of Science Research Fellowship for Young Scientists to N. K.; T. K. was financially supported by Mitsui.

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Authors and Affiliations

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

    Renata S. Mendonça, Tomoko Kanamori, Misato Hayashi & Tetsuro Matsuzawa

  2. National Museum of Nature and Science, Tokyo, Japan

    Noko Kuze

  3. Japan Society for the Promotion of Science, Tokyo, Japan

    Noko Kuze

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

    Henry Bernard

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  1. Renata S. Mendonça
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  2. Tomoko Kanamori
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  4. Misato Hayashi
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  6. Tetsuro Matsuzawa
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Correspondence to Renata S. Mendonça.

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An erratum to this article is available at http://dx.doi.org/10.1007/s10329-016-0595-2.

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Mendonça, R.S., Kanamori, T., Kuze, N. et al. Development and behavior of wild infant-juvenile East Bornean orangutans (Pongo pygmaeus morio) in Danum Valley. Primates 58, 211–224 (2017). https://doi.org/10.1007/s10329-016-0567-6

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