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Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques

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Abstract

In most mammals, female fertility and reproduction are strongly influenced by nutritional status and, therefore, by foraging conditions. Here, we investigate the relationship between food resources, feeding competition, energy intake and reproduction in a group of wild female Assamese macaques (Macaca assamensis) in northeastern Thailand. Over 2,100 h of data on feeding behaviour, energy intake and activity budgets were combined with data on resource characteristics, female reproduction and physical condition. We found that an increase in food availability had a positive effect on female energy intake and conception rates. In addition, it appeared that females incurred energetic costs during lactation and that females with a better physical condition during the mating season were more likely to conceive. The annual birth season occurred a few months before the annual peak in food availability, causing peak lactation to coincide with a period of high food availability. This suggests that females use the increased food abundance to compensate for the energetic costs of lactation. Neither energy intake rates nor activity budgets were influenced by female dominance rank, even during periods when the levels of contest competition were predicted to be high. In line with this, we found no evidence for rank-related differences in reproduction. The apparently limited influence of feeding competition in female Assamese macaques adds to the debate on the extent to which patterns in feeding competition and fitness can reliably be predicted based on ecological conditions. We suggest that this may partially be resolved by including potential competition-reducing mechanisms into the predictive framework.

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References

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

    Article  PubMed  CAS  Google Scholar 

  • Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge

    Google Scholar 

  • Altmann J, Alberts S (2003) Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401–409

    Article  PubMed  Google Scholar 

  • Altmann J, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savannah baboons, Papio cynocephalus. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 403–418

    Google Scholar 

  • Baayen RH (2008) Analyzing linguistic data. Cambridge University Press, Cambridge

    Google Scholar 

  • Baayen RH (2011) R package languageR. R package version 1.4. http://CRAN.R-project.org/package=languageR

  • 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

    Article  PubMed  Google Scholar 

  • Barton RA (1993) Sociospatial mechanisms of feeding competition in female olive baboons, Papio anubis. Anim Behav 46:791–802

    Article  Google Scholar 

  • Barton RA, Whiten A (1993) Feeding competition among female olive baboons, Papio anubis. Anim Behav 46:777–789

    Article  Google Scholar 

  • Barton RA, Whiten A, Strum SC, Byrne RW, Simpson AJ (1992) Habitat use and resource availability in baboons. Anim Behav 43:831–844

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2012) lme4—linear mixed effects models using S4 classes. R package version 0.999999-0. http://CRAN.R-project.org/package=lme4

  • Bercovitch FB (1987) Female weight and reproductive condition in a population of olive baboons (Papio anubis). Am J Primatol 12:189–195

    Article  Google Scholar 

  • Bercovitch FB, Strum SC (1993) Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behav Ecol Sociobiol 33:313–318

    Article  Google Scholar 

  • Berman CM, Schwartz S (1988) A nonintrusive method for determining relative body fat in free-ranging monkeys. Am J Primatol 14:53–64

    Article  Google Scholar 

  • Borries C, Koenig A, Winkler P (2001) Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behav Ecol Sociobiol 50:391–402

    Article  Google Scholar 

  • Borries C, Larney E, Kreetiyutanont K, Koenig A (2002) The diurnal primate community in a dry evergreen forest in Phu Khieo Wildlife Sanctuary, northeast Thailand. Nat Hist Bull Siam Soc 50:75–88

    Google Scholar 

  • Borries C, Lu A, Ossi-Lupo K, Larney E, Koenig A (2011) Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. Am J Phys Anthropol 144:286–299

    Article  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Bulger J, Hamilton WJ (1987) Rank and density correlates of inclusive fitness measures in a natural chacma baboon (Papio ursinus) troop. Int J Primatol 5:247–261

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer, Berlin

    Google Scholar 

  • Carnegie SD, Fedigan LM, Melin AD (2011) Reproductive seasonality in female capuchins (Cebus capucinus) in Santa Rosa (Area de Conservación Guanacaste), Costa Rica. Int J Primatol 32:1076–1090

    Article  Google Scholar 

  • Chapman C, Rothman J (2009) Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50:12–22

    Article  PubMed  Google Scholar 

  • Clutton-Brock T, Janson C (2012) Primate socioecology at the crossroads: past, present, and future. Evol Anthropol 21:136–150

    Article  PubMed  Google Scholar 

  • Coelho AM (1986) Time and energy budgets comparative primate biology. In: Mitchell G, Erwin J (eds) Vol. 2A: behaviour, conservation and ecology. Alan R. Liss, Inc., New York, p 141–166

  • Crockett CM, Rudran R (1987) Red howler monkey birth data 1: Seasonal variation. Am J Primatol 13:347–368

    Article  Google Scholar 

  • Dasilva G (1992) The Western black-and-white colobus as a low-energy strategist: activity budgets, energy expenditure and energy intake. J Anim Ecol 61:79–91

    Article  Google Scholar 

  • Deutsch JC, Lee PC (1991) Dominance and feeding competition in captive rhesus monkeys. Int J Primatol 12:615–625

    Article  Google Scholar 

  • Di Bitetti MS, Janson CH (2000) When will the stork arrive? Patterns of birth seasonality in neotropical primates. Am J Primatol 50:109–130

    Article  PubMed  Google Scholar 

  • Drent R, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Dunbar R (1980) Demographic and life history variables of a population of gelada baboons. J Anim Ecol 49:485–506

    Article  Google Scholar 

  • Dunbar RIM, Dunbar P (1988) Maternal time budgets of gelada baboons. Anim Behav 36:970–980

    Article  Google Scholar 

  • Fürtbauer I, Schülke O, Heistermann M, Ostner J (2010) Reproductive and life history parameters of wild female Assamese macaques (Macaca assamensis). Int J Primatol 31:501–517

    Article  PubMed  Google Scholar 

  • Gilmore D, Cook B (1981) Environmental factors in mammal reproduction. MacMillan, London

    Google Scholar 

  • Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875

    Google Scholar 

  • Goering HK, Van Soest PJ (1970) Forage fiber analysis (apparatus, reagents, procedures and some applications). USDA Agricultural Handbook No. 379. Agriculture Research Service, U.S. Department of Agriculture, Washington, DC

  • Gore MA (1993) Effects of food distribution on foraging competition in rhesus monkeys, Macaca mulatta, and hamadryas baboons, Papio hamadryas. Anim Behav 45:773–786

    Article  Google Scholar 

  • Grassman LI, Tewes ME, Silvy NJ, Kreetiyutanont K (2005) Ecology of three sympatric felids in a mixed evergreen forest in north-central Thailand. J Mammal 86:29–38

    Article  Google Scholar 

  • Harcourt AH (1989) Environment, competition and reproductive performance of female monkeys. Trends Ecol Evol 4:101–105

    Article  PubMed  CAS  Google Scholar 

  • Isbell L, Pruetz J (1998) Differences between vervets (Cercophitecus aethiops) and patas monkeys (Erythrocebus patas) in agonistic interactions between adult females. Int J Primatol 19:837–855

    Article  Google Scholar 

  • Isbell L, Pruetz J, Young T (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behav Ecol Sociobiol 42:123–133

    Article  Google Scholar 

  • Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2:143–155

    Article  Google Scholar 

  • Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177–202

    Article  Google Scholar 

  • Janson C, Chapman C (1999) Resources and primate community structure. In: Fleagle J, Janson C, Reed J (eds) Primate communities. Cambridge University Press, Cambridge, pp 237–267

    Chapter  Google Scholar 

  • Janson C, Verdolin J (2005) Seasonality of primate births in relation to climate. 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 307–350

    Chapter  Google Scholar 

  • Janson CH (1985) Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behav Ecol Sociobiol 18:125–138

    Article  Google Scholar 

  • Janson CH (1988) Intra-specific food competition and primate social structure: a synthesis. Behaviour 105:1–17

    Article  Google Scholar 

  • Janson CH, van Schaik CP (1988) Recognizing the many faces of primate food competition: methods. Behaviour 105:165–186

    Article  Google Scholar 

  • Koenig A (2000) Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behav Ecol Sociobiol 48:93–109

    Article  Google Scholar 

  • Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783

    Article  Google Scholar 

  • Koenig A, Beise J, Chalise M, Ganzhorn J (1998) When females should contest for food - testing hypotheses about resource density, distribution, size, and quality with hanuman langurs (Presbytis entellus). Behav Ecol Sociobiol 42:225–237

    Article  Google Scholar 

  • Koenig A, Borries C (2001) Socioecology of Hanuman langurs: the story of their success. Evol Anthropol 10:122–137

    Article  Google Scholar 

  • Koenig A, Borries C (2009) The lost dream of ecological determinism: time to say goodbye? … Or a White Queen’s proposal? Evol Anthropol 18:166–174

    Article  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 

  • Koenig A, Borries C, Suarez S, Kreetiyutanont K, Prabnasuk J (2004) Socio-ecology of Phayre’s leaf monkeys (Trachypithecus phayrei) at Phu Khieo Wildlife Sanctuary. J Wildlife Thail 12:150–163

    Google Scholar 

  • Kuester J, Paul A (1984) Female reproductive characteristics in semifree-ranging Barbary Macaques (Macaca sylvanus L. 1758). Folia Primatol 43:69–83

    Article  Google Scholar 

  • Kumsuk M, Kreetiyutanont K, Suvannakorn V, Sanguanyat N (1999) Diversity of wildlife vertebrates in Phu Khieo Wildlife Sanctuary, Chaiyaphum Province. Wildlife Conservation Division, Natural Resources Conservation Office, Royal Forest Department, Bangkok

  • 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

    Article  PubMed  Google Scholar 

  • Lee PC (1987) Nutrition, fertility and maternal investment in primates. J Zool 213:409–422

    Article  Google Scholar 

  • Lewis R, Kappeler P (2005) Are Kirindy sifaka capital or income breeders? It depends. Am J Primatol 67:365–369

    Article  PubMed  CAS  Google Scholar 

  • Lomnicki A (1988) Population ecology of individuals. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Loudon ASI, Racey PA (1987) Reproductive energetics in mammals. Clarendon, Oxford

    Google Scholar 

  • Majolo B, Lehmann J, de Bortoli VA, Schino G (2012) Fitness-related benefits of dominance in primates. Am J Phys Anthropol 147:652–660

    Article  PubMed  CAS  Google Scholar 

  • Miller KE, Bales KL, Ramos JH, Dietz JM (2006) Energy intake, energy expenditure, and reproductive costs of female wild golden lion tamarins (Leontopithecus rosalia). Am J Primatol 68:1037–1053

    Article  PubMed  Google Scholar 

  • Mori A (1979) Analysis of population changes by measurement of body weight in the Koshima troop of Japanese monkeys. Primates 20:371–397

    Article  Google Scholar 

  • Murray C, Eberly L, Pusey A (2006) Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes). Behav Ecol 17:1020–1028

    Article  Google Scholar 

  • Nievergelt CM, Martin RD (1999) Energy intake during reproduction in captive common marmosets (Callithrix jacchus). Physiol Behav 65:849–854

    Article  PubMed  CAS  Google Scholar 

  • Ostner J, Heistermann M, Schülke O (2008) Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm Behav 54:613–619

    Article  PubMed  Google Scholar 

  • Pereira ME (1993) Seasonal adjustment of growth rate and adult body weight in ringtailed lemurs. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 205–221

    Google Scholar 

  • Pierce WC, Haenisch EL (1947) Quantitative analysis. Wiley, London

    Google Scholar 

  • Pruetz JD, Isbell LA (2000) Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behav Ecol Sociobiol 49:38–47

    Article  Google Scholar 

  • R Development Core Team (2012) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Richard AF, Dewar RE, Schwartz M, Ratsirarson J (2000) Mass change, environmental variability and female fertility in wild Propithecus verreauxi. J Hum Evol 39:381–391

    Article  PubMed  CAS  Google Scholar 

  • Roberts SB, Cole TJ, Coward WA (1985) Lactational performance in relation to energy intake in the baboon. Am J Clin Nutr 41:1270–1276

    PubMed  CAS  Google Scholar 

  • Robinson JG (1981) Spatial structure in foraging groups of wedge-capped capuchin monkeys Cebus nigrivittatus. Anim Behav 29:1036–1056

    Article  Google Scholar 

  • Sadleir RMF (1969) The ecology and reproduction in wild and domestic mammals. Methuen, London

    Book  Google Scholar 

  • Saito C (1996) Dominance and feeding success in female Japanese macaques, Macaca fuscata: effects of food patch size and inter-patch distance. Anim Behav 51:967–980

    Article  Google Scholar 

  • Sawada A, Sakaguchi E, Hanya G (2011) Digesta passage time, digestibility, and total gut fill in captive Japanese macaques (Macaca fuscata): effects food type and food intake level. Int J Primatol 32:390–405

    Article  Google Scholar 

  • Schülke O, Chalise M, Koenig A (2006) The importance of ingestion rates for estimating food quality and energy intake. Am J Primatol 68:951–965

    Article  PubMed  Google Scholar 

  • Schülke O, Ostner J (2012) Ecological and social influences on sociality. In: Mitani J, Call J, Kappeler P, Palombit R, Silk J (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 193–219

    Google Scholar 

  • Schülke O, Pesek D, Whitman B, Ostner J (2011) Ecology of Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary. J Wildlife Thail 18:1–15

    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 

  • Soumah AG, Yokota N (1991) Female rank and feeding strategies in a free-ranging provisioned troop of Japanese macaques. Folia Primatol 57:191–200

    Article  Google Scholar 

  • Stearns S (1992) The evolution of life histories. Oxford University Press, New York

    Google Scholar 

  • Sterck EHM, Steenbeek R (1997) Female dominance relationships and food competition in the sympatric Thomas langur and long-tailed macaque. Behaviour 134:749–774

    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 

  • Strum SC, Western JD (1982) Variations in fecundity with age and environment in olive baboons (Papio anubis). Am J Primatol 3:61–76

    Article  Google Scholar 

  • Su H, Birky W (2007) Within-group female-female agonistic interactions in Taiwanese macaques (Macaca cyclopis). Am J Primatol 69:199–211

    Article  PubMed  Google Scholar 

  • Suzuki S, Noma N, Izawa K (1998) Inter-annual variation of reproductive parameters and fruit availability in two populations of Japanese macaques. Primates 39:313–324

    Article  Google Scholar 

  • Takahashi H (2002) Female reproductive parameters and fruit availability: factors determining onset of estrus in Japanese macaques. Am J Primatol 57:141–153

    Article  PubMed  Google Scholar 

  • Thierry B (2008) Primate socioecology, the lost dream of ecological determinism. Evol Anthropol 17:93–96

    Article  Google Scholar 

  • van Noordwijk MA, van Schaik CP (1987) Competition among female long-tailed macaques, Macaca fascicularis. Anim Behav 35:577–589

    Article  Google Scholar 

  • van Noordwijk MA, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105–130

    Article  PubMed  Google Scholar 

  • van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative socioecology: the behavioural ecology of humans and other mammals. Blackwell Scientific, Oxford, pp 195–218

    Google Scholar 

  • van Schaik CP, van Noordwijk MA (1985) Interannual variability in fruit abundance and the reproductive seasonality in Sumatran long-tailed macaques (Macaca fascicularis). J Zool 206:533–549

    Article  Google Scholar 

  • van Schaik CP, van Noordwijk MA (1988) Scramble and contest in feeding competition among female long-tailed macaques (Macaca fascicularis). Behaviour 105:77–98

    Article  Google Scholar 

  • Van Soest PJ, Robertson JB (1980) Systems of analysis for evaluating fibrous feeds. In: Pigden WJ, Balch CC, Graham M (eds) Standardization of analytical methodology in feeds. International Research Development Center, Ottawa, Canada

    Google Scholar 

  • Vogel E (2005) Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: the effects of contest competition. Behav Ecol Sociobiol 58:333–344

    Article  Google Scholar 

  • Vogel E, Janson CH (2007) Predicting the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree method. Am J Primatol 69:533–550

    Article  PubMed  CAS  Google Scholar 

  • Wade GN, Schneider JE, Li HY (1996) Control of fertility by metabolic cues. Am J Physiol-Endoc M 270:E1–E19

    CAS  Google Scholar 

  • White FJ, Overdorff DJ, Keith-Luca T, Rasmussen MA, Kallan WE, Forward Z (2007) Female dominance and feeding priority in a prosimian primate: experimental manipulation of feeding competition. Am J Primatol 69:295–304

    Article  PubMed  Google Scholar 

  • Whitten PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol 5:139–159

    Article  Google Scholar 

  • Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300

    Article  Google Scholar 

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Acknowledgments

We thank the National Research Council of Thailand (NRCT) and the Department of National Parks, Wildlife and Plant Conservation (DNP) for permission (no. 0004.3/3618; 0002.3/2647) to conduct this study. We are grateful to J. Prabnasuk, K. Nitaya, M. Kumsuk and K. Kreetiyutanont (Phu Khieo Wildlife Sanctuary) for their cooperation and permission to carry out this research. We thank A. Koenig and C. Borries (Stony Brook University) who developed the field site at Huai Mai Sot Yai. We are very thankful to N. Juntuch, N. Ponganan, D. Bootros, S. Jomhlotwong, T. Kilawit, T. Wisate, P. Saisawatdikul and especially M. Swagemakers for their help in the field. We are also very grateful to W. Nuagchiyo, A. Chunchaen and S. Macdonald for their help with data collection. We thank N. Bhumpakphan, W. Eiadthong (Kasetsart University) and W. Brockelman (Mahidol University) for their support and cooperation. Furthermore, we would like to thank Dr. Marie Charpentier and two anonymous reviewers for helpful comments on an earlier draft of the manuscript. This project was supported with funds from the Max Planck Society, the National Geographic Society and the University of Göttingen through funding from the German Initiative of Excellence.

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The authors declare that they have no conflict of interest.

Ethical standards

Approval and permission to conduct research was granted by the authorities of Thailand (permit no. 0004.3/3618 and 0002.3/2647), and all research was undertaken in strict accordance with the laws set forth by the National Research Council of Thailand and the regulations of the Department of National Parks, Wildlife and Plant Conservation, Bangkok, as well as the guidelines of the involved institutes.

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  1. Primate Social Evolution Group, Courant Research Centre Evolution of Social Behaviour, Georg-August University Göttingen, Kellnerweg 6, 37077, Göttingen, Germany

    Marlies Heesen, Sebastian Rogahn & Julia Ostner

  2. Courant Research Centre Evolution of Social Behaviour, Georg-August University Göttingen, Kellnerweg 6, 37077, Göttingen, Germany

    Oliver Schülke

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  1. Marlies Heesen
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  2. Sebastian Rogahn
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  4. Oliver Schülke
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Correspondence to Marlies Heesen.

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Heesen, M., Rogahn, S., Ostner, J. et al. Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behav Ecol Sociobiol 67, 1053–1066 (2013). https://doi.org/10.1007/s00265-013-1530-9

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