Abstract
In most mammals, females pay for reproduction by dramatically increasing net energy intake from conception to mid- or late lactation. To do this, they time their reproductive events in relation to environmental cycles so that periods of peak food availability coincide with peak demand or are used to build energy stores. This timing is not possible in species with slow development in which lactation is prolonged over a multi-year period with fluctuating food availability. Here, mothers are expected to sustain a stable but generally lower level of nutrient transfer. In a sample of over 1,050 complete follow days of eight mother–infant pairs collected over 7 years, we document maternal effort for wild Bornean orangutans (Pongo pygmaeus wurmbii) over their average 6.5-year lactation period. As predicted, maternal feeding time was independent of the age of her growing offspring, indicating a stable sustained “plateau” effort of ≤ 25 % above baseline level, instead of a short peak lactation as seen in seasonal breeders. Infant orangutans started to regularly supplement milk with self-harvested food when they were 1–1.5 years old, indicating milk intake was insufficient from this age onwards, even though maternal effort did not decrease. We expect the same regulation of sustained maternal effort in other large and large-brained mammals with slow infant development. We also predict that mother–infant conflict over suckling may show another peak at the onset of the milk + solid food phase, in addition to the well-known conflict around the endpoint of lactation (weaning), which is reached after a long and gradual increase in solid food intake by the infant.
Similar content being viewed by others
References
Ainsworth BE, Haskell WT, Whitt MC, Irwin ML, Swartz AM, Strath SJ, O'Brien WL, Bassett DRJ, Schmitz KH, Emplancourt PO, Jacobs DRJ, Leon AS (2000) Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc S498–S516
Altmann J (1980) Baboon mothers and infants. Harvard University, Cambridge, MA
Altmann J, Samuels A (1992) Costs of maternal care: infant-carrying in baboons. Behav Ecol Sociobiol 29:391–398
Alvarez HP (2000) Grandmother hypothesis and primate life histories. Am J Phys Anthropol 113:435–450
Barrett L, Halliday J, Henzi SP (2006) The ecology of motherhood, the structuring of lactation costs by chacma baboons. J Anim Ecol 75:875–886
Barrett L, Henzi SP (2000) Are baboon infants Sir Phillip Sydney's offspring? Ethology 106:645–658
Brockman DK, van Schaik CP (2005) Seasonality and reproductive function. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 269–305
Butte NF (2005) Energy requirements of infants. Publ Health Nutr 8:953–967
Butte NF, Wong WW, Hopkinson JM (2001) Energy requirements of lactating women derived from doubly labeled water and milk energy output. J Nutr 131:53–58
Clutton-Brock T (1991) The evolution of parental care. Princeton University Press, Princeton
Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. The University of Chicago Press, Chicago
Di Fiore A, Campbell CJ (2007) The Atelines. Variation in ecology, behavior, and social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 155–185
Dufour DL, Sauther ML (2002) Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation. Am J Hum Biol 14:584–602
Dunbar RIM, Dunbar P (1988) Maternal time budgets of gelada baboons. Anim Behav 36:970–980
Eveleth PB, Tanner JM (1976) Worldwide variation in human growth. Cambridge University Press, Cambridge
Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875
Goodall J (1986) The chimpanzees of Gombe. Harvard University Press, Cambridge, MA
Grund A, Vollbrecht H, Frandsen W, Krause H, Siewers M, Rieckert H, Müller MJ (2000) No effect of gender on different components of daily energy expenditure in free living prepubertal children. Int J Obes 24:299–305
Hiraiwa-Hasegawa M (1990) A note on the ontogeny of feeding. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. Sexual and life history strategies. University of Tokyo Press, Tokyo, pp 277–283
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108
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 (2005) Energetic responses to food availability in the great apes: implications for hominin evolution. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 351–378
Knott CD, Emery Thompson M, Wich SA (2009) The ecology of female reproduction in wild orangutans. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 171–188
König B, Markl H (1987) Maternal care in house mice: I. The weaning strategy as a means for parental manipulation of offspring quality. Behav Ecol Sociobiol 20:1–9
Kramer PA (1998) The costs of human locomotion: maternal investment in child transport. Am J Phys Anthropol 107:71–85
Kuzawa CW (1998) Adipose tissue in human infancy and childhood: an evolutionary perspective. Yearb Phys Anthropol 41:177–209
Langer P (2008) The phases of maternal investment in eutherian mammals. Zoology 111:148–162
Lappan S (2009) The effects of lactation and infant care on adult energy budgets in wild siamangs (Symphalangus syndactylus). Am J Phys Anthropol 140:290–301
Lee PC (1996) The meanings of weaning: growth, lactation, and life history. Evol Anthropol 5:87–96
Lee PC, Lindsay WK, Moss CJ (2011) Ecological patterns of variability in demographic rates. In: Moss CJ, Croze H, Lee PC (eds) The Amboseli elephants. Long-term perspective on a long-lived mammal. University of Chicago Press, Chicago, pp 74–88
Lee PC, Moss CJ (2011) Calf development and maternal rearing strategies. In: Moss CJ, Croze H, Lee PC (eds) The Amboseli elephants. Long-term perspective on a long-lived mammal. University of Chicago Press, Chicago, pp 224–237
Leigh SR, Shea BT (1995) Ontogeny and the evolution of adult body size dimorphism in apes. Am J Primatol 36:37–60
Lycett JE, Henzi SP, Barrett L (1998) Maternal investment in mountain baboons and the hypothesis of reduced care. Behav Ecol Sociobiol 42:49–56
Marshall AJ, Ancrenaz M, Brearley FQ, Frederiksson GB, Ghaffar N, Heydon M, Husson SJ, Leighton M, McConkey KR, Morrogh-Bernard HC, Proctor J, van Schaik CP, Yeager CP, Wich SA (2009) The effects of forest phenology and floristics on populations of Bornean and Sumatran orangutans. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 97–117
Martin PS (1984) The meaning of weaning. Anim Behav 32:1257–1259
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, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 119–133
Murray CM, Lonsdorf EV, Eberly LE, Pusey AE (2009) Reproductive energetics in free-living female chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol 20:1211–1216
Nowell AA, Fletcher AW (2008) The development of feeding behaviour in wild western lowland gorillas (Gorilla gorilla gorilla). Behaviour 145:171–193
Oftedal OT (2000) Use of maternal reserves as a lactation strategy in large mammals. Proc Nutr Soc 59:99–106
Pellew RA (1984) Food consumption and energy budgets of the giraffe. J Appl Ecol 21:141–159
Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge
Piperata BA (2009) Variation in maternal strategies during lactation: the role of the biosocial context. Am J Hum Biol 21:817–827
Plavcan JM, van Schaik CP (1997) Intrasexual competition and body weight dimorphism in anthropoid primates. Am J Phys Anthropol 103:37–68
Pontzer H, Raichlen DA, Shumaker RW, Ocobock C, Wich SA (2010) Metabolic adaptation for low energy throughput in orangutans. P Natl Acad Sci USA 107:14048–14052
Prentice AM, Prentice AM (1988) Energy cost of lactation. Annu Rev Nutr 8:63–79
Prentice AM, Whitehead RG (1987) The energetics of human reproduction. Symp Zool Soc Lond 57:275–304
R-Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Robson SL, van Schaik CP, Hawkes K (2006) The derived features of human life history. In: Hawkes K, Paine RR (eds) The evolution of human life history. School of American Research Press, Santa Fe, NM, pp 17–44
Rosetta L, Lee PC, Garcia C (2011) Energetics during reproduction: a double labeled water study of lacatating baboons. Am J Phys Anthropol 144:661–668
Russon AE, Wich SA, Ancrenaz M, Kanamori T, Knott CD, Kuze N, Morrogh-Bernard HC, Pratje P, Ramlee H, Rodman P, Sawang A, Sidiyasa K, Singleton I, van Schaik CP (2009) Geographic variation in orangutan diets. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and conservation. Oxford University Press, Oxford, pp 135–156
Schmidt-Nielsen K (1984) Scaling. Cambridge University Press, Cambridge
Sellen DW (2001) Comparison of infant feeding patterns reported for nonindustrial populations with current recommendations. J Nutr 131:2707–2715
Smith RJ, Jungers WL (1997) Body mass in comparative primatology. J Hum Evol 32:523–559
Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos T Roy Soc B 363:375–398
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Tarnaud L (2006) Feeding behavior of lactating brown lemur females (Eulemur fulvus) in Mayotte: influence of infant age and plant phenology. Am J Primatol 68:966–977
Terborgh J, van Schaik CP (1987) Convergence vs. non-convergence in primate communities. In: Gee JHR, Giller PS (eds) Organization of communities: past and present. Blackwell, Oxford, pp 205–226
Trivers RL (1974) Parent–offspring conflict. Am Zool 14:249–264
van Noordwijk MA, Sauren SEB, Nuzuar, Abulani A, Morrogh-Bernard HC, Utami Atmoko SS, van Schaik CP (2009) Development of independence Sumatran and Bornean orangutans compared. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP (eds) Orangutans: geographic variation in behavioral ecology and eonservation. Oxford University Press, pp 189–203
van Noordwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79–94
Vogel ER, Knott CD, Crowley BE, Blakely MD, Larsen MD, Dominy NJ (2012) Bornean orangutans on the brink of protein bankruptcy. Biol Lett 8:333–336
Wells JCK, Davies PSW (1998) Estimation of the energy cost of physical activity in infancy. Arch Dis Childhood 78:131–136
Whitehead H, Mann J (2000) Female reproductive strategies of Cetaceans: life histories and calf care. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies. Field studies of dolphins and whales. University of Chicago Press, Chicago, pp 219–246
Wich SA, Utami-Atmoko SS, Mitra Setia T, Rijksen HD, Schurmann C, van Hooff JARAM, van Schaik CP (2004) Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol 47:385–398
Acknowledgments
We are indebted to the Tuanan team of assistants and students over many years for their efforts in data collection. We thank Tatang Mitra Setia MSc and the students of the Fakultas Biologi Universitas Nasional (UNAS) in Jakarta, and in particular Rahmalia N. Amda and Neneng Mardianah as well as Erin Vogel, for their collaboration and support for the Tuanan project. We gratefully acknowledge the Indonesian Institute of Science (LIPI), and the Indonesian State Ministry for Research and Technology (RisTek), the Director General Departemen Kehutanan (PHKA), Departamen Dalam Negri, the local government in Central Kalimantan, the BKSDA Palangkaraya, the Bornean Orangutan Survival Foundation (BOSF) and MAWAS in Palangkaraya for their permission and support to the project. For major financial support we thank the University of Zurich, and the A.H. Schultz Stiftung. We appreciate the constructive comments by the anonymous reviewers.
Ethical standards
The observations on wild orangutans were conducted in accordance with the local regulations.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Charpentier
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 381 kb)
Rights and permissions
About this article
Cite this article
van Noordwijk, M.A., Willems, E.P., Utami Atmoko, S.S. et al. Multi-year lactation and its consequences in Bornean orangutans (Pongo pygmaeus wurmbii). Behav Ecol Sociobiol 67, 805–814 (2013). https://doi.org/10.1007/s00265-013-1504-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-013-1504-y