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
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
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
Bercovitch FB, Berard JD (1993) Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32:103–109
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
Byers JA, Walker C (1995) Refining the motor training hypothesis for the evolution of play. Am Nat 146:25–40
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
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
Doran DM (1997) Ontogeny of locomotion in mountain gorillas and chimpanzees. J Hum Evol 32:323–344
Douglas B, Martin M, Ben B (2012) lme4: linear mixed-effects models using S4 classes. RStudio, Boston
Fagen R (1993) Primate juvenile and primate play. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. Oxford University Press, Oxford, pp 182–196
Fairbanks LA (1988) Vervet monkey grandmothers: effects on mother-infant relationships. Behaviour 104:176–188
French JA (1981) Individual differences in play in Macaca fuscata: the role of maternal status and proximity. Int J Primatol 2:237–246
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
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
Galdikas BMF, Wood JW (1990) Birth spacing patterns in humans and apes. Am J Phys Anthropol 83:185–191
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
Hazebroek HP, Adlin TZ, Sinum W (2012) Danum Valley: the rain forest. Natural History Publications, Kota Kinabalu
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
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
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
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
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
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
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
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
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
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
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
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
Kelley J, Schwartz GT (2010) Dental development and life history in living African and Asian apes. Proc Natl Acad Sci USA 107:1035–1040
Knott CD (1998) Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19:1061–1079
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
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
Kokko H, Lundberg P (2001) Dispersal, migration, and offspring retention in saturated habitats. Am Nat 157:188–202
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
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
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
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
Martin PR, Bateson PP (1993) Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge
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
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
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
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
Pusey AE (1983) Mother-offspring relationships in chimpanzees after weaning. Anim Behav 31:363–377
Pusey AE (1990) Behavioural changes at adolescence in chimpanzees. Behaviour 115:203–246
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
R Studio (2015) R Studio: integrated development environment for R. R Studio, Boston, MA
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
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
Robson SL, Wood B (2008) Hominin life history: reconstruction and evolution. J Anat 212:294–425
Ross C (2001) Park or ride? Evolution of infant carrying in primates. Int J Primatol 22:749–771
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
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
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
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
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
Spinka M, Newberry NC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168
Stacey PB (1979) Habitat saturation and communal breeding in the acorn woodpecker. Animal Behav 27:1153–1166
Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309
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
Thompson ME (2013) Reproductive ecology of female chimpanzees: chimpanzee reproductive ecology. Am J Primatol 75:222–237. doi:10.1002/ajp.22084
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
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
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
van Noordwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79–94
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
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
van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144
van Schaik CP (1999) The socioecology of fission–fusion sociality in orangutans. Primates 40:69–86
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
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
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
Watts DP (1991) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–225
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
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
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
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
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
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10
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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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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DOI: https://doi.org/10.1007/s10329-016-0567-6