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Reproductive seasonality in wild northern pig-tailed macaques (Macaca leonina)

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Abstract

Macaque reproductive patterns range from strictly seasonal breeding to non-seasonal breeding, but factors explaining this variation are not fully understood. Valid reproductive seasonality data are also still lacking for many wild macaque populations because the majority of birth data are from captive animals living outside of their geographic range. We evaluated whether the reproductive seasonality of wild northern pig-tailed macaques falls as expected by the ecological (latitude) or phylogenetic inertia hypotheses in comparison with other macaque species. We recorded monthly occurrences of births (N = 22), copulations (N = 563), and females exhibiting sex skin swellings (N = 18) in one group at Khao Yai National Park (KYNP), Thailand. Births, copulations, and females exhibiting sex skin swellings were significantly different from a random distribution. Using measures of circular statistics and the van Schaik and colleagues’ (Schaik et al. Lee (ed), Comparative primate socioecology, Cambridge University Press, Cambridge, 1999) seasonality categorizations, the population at KYNP is best characterized as moderately seasonal breeding. Despite some inconsistency, macaque reproductive seasonality was significantly influenced by latitudinal location. We broadly found that: (1) non-seasonal breeding macaque populations (birth r-vector < 0.3) lived at latitudes close to the equator between 1°S and 3°N, (2) moderately seasonal breeding macaque populations (0.3 < birth r-vector < 0.7) were found between 3°N and 14°N and at 5°S, and (3) strictly seasonal breeding macaque populations (birth r-vector > 0.7) ranged ≥ 12°N. A strong phylogenetic signal in reproductive seasonality on the macaque phylogeny was also detected. However, further studies of wild macaque populations are still needed to better characterize reproductive seasonality in this taxon.

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References

  • Agostinelli C, Lund U (2017) R package 'circular': Circular Statistics (version 0.4–93). Accessed 13 February 2018

  • Albert A, Savini T, Huynen M-C (2011) Sleeping site selection and presleep behavior in wild pigtailed macaques. Am J Primatol 73:1222–1230

    PubMed  Google Scholar 

  • Albert A, Huynen M-C, Savini T, Hambuckers A (2013) Influence of food resources on the ranging pattern of northern pig-tailed macaques (Macaca leonina). Int J Primatol 34:696–713. https://doi.org/10.1007/s10764-013-9690-z

    Article  Google Scholar 

  • Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196

    Google Scholar 

  • Altmann SA (1962) A field study of the sociobiology of rhesus monkeys Macaca mulatta. Ann NY Acad Sci 102:338–435

    CAS  PubMed  Google Scholar 

  • Altmann J (1974) Observational study of behavior: Sampling methods. Behaviour 49:227–266

    CAS  PubMed  Google Scholar 

  • Bartlett TQ (2009) Seasonal home range use and defendability in white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand. In: Whittaker D, Lappan S (eds) The gibbons: new perspectives on small ape socioecology and population biology. Springer New York, New York, NY, pp 265–275. https://doi.org/10.1007/978-0-387-88604-6_13

    Chapter  Google Scholar 

  • Batschelet E (1981) Circular statistics in biology. Academic Press, New York

    Google Scholar 

  • Bercovitch FB, Harvey N (2004) Reproductive life history. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, pp 61–80

    Google Scholar 

  • Bivand R, Rundel C, Pebesma E, Stuetz R, Ove Hufthammer K, Giraudoux P, Davis M, Santilli S (2020) rgeos: Interface to Geometry Engine - Open Source ('GEOS'). Accessed 12 October 2020

  • 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 269–306

    Google Scholar 

  • Bronson FH, Heideman PD (1994) Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD (eds) The physiology of reproduction, 2nd edn. Raven Press, New York, pp 541–558

    Google Scholar 

  • Bullock DW, Paris CA, Goy RW (1972) Sexual behaviour, swelling of the sex skin and plasma progesterone in the pigtail macaque. J Reprod Fertil 31:225–236

    CAS  PubMed  Google Scholar 

  • Caldecott JO (1986) An ecological and behavioural study of the pig-tailed macaque. Contrib Primatol 21:1–259

    Google Scholar 

  • Carlisle KS, Brenner RM, Montagna W (1981) Hormonal regulation of sex skin in Macaca nemestrina. Biol Reprod 25:1053–1063

    CAS  PubMed  Google Scholar 

  • Carlson C (2011) Behavioral mechanisms of postcopulatory sexual selection in wild pigtailed macaques (Macaca leonina) Dissertation. University of Chicago

    Google Scholar 

  • Chandrashekar V, Wolf RC, Dierschke DJ, Sholl SA, Bridson WE, Clark JR (1980) Serum progesterone and corpus luteum function in pregnant pigtailed monkeys (Macaca nemestrina). Steroids 36:483–495

    CAS  PubMed  Google Scholar 

  • Choudhury A (2008) Ecology and behaviour of the pig tailed macaque Macaca nemestrina leonina in some forests of Assam in North East India. J Bombay Nat Hist Soc 105:279–291

    Google Scholar 

  • Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41:1045–1056. https://doi.org/10.1016/S0003-3472(05)80642-6

    Article  Google Scholar 

  • Delson E (1980) Fossil macaques, phyletic relationships and a scenario of deployment. In: Lindburg D (ed) The macaques: Studies in ecology, behavior and evolution. van Nostrand Reinhold, New York, pp 10–29

    Google Scholar 

  • Dixson AF (2012) Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, Oxford

    Google Scholar 

  • Dubuc C, Muniz L, Heistermann M, Engelhardt A, Widdig A (2011) Testing the priority-of-access model in a seasonally breeding primate species. Behav Ecol Sociobiol 65:1615–1627. https://doi.org/10.1007/s00265-011-1172-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Dubuc C, Muniz L, Heistermann M, Widdig A, Engelhardt A (2012) Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques? Horm Behav 61:696–705

    PubMed  PubMed Central  Google Scholar 

  • Dunnington D, Thorne B (2020) ggspatial: Spatial Data Framework for ggplot2. Accessed 12 October 2020

  • Engelhardt A, Heistermann M, Hodges JK, Nürnberg P, Niemitz C (2006) Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms? Behav Ecol Sociobiol 59:740–752. https://doi.org/10.1007/s00265-005-0104-x

    Article  Google Scholar 

  • Evans BJ, Gansauge M-T, Tocheri MW, Schillaci MA, Sutikna T, Saptomo EW, Klegarth A, Tosi AJ, Melnick DJ, Meyer M (2020) Mitogenomics of macaques (Macaca) across Wallace’s Line in the context of modern human dispersals. J Hum Evol 146:102852

    PubMed  Google Scholar 

  • Fan P, Liu Y, Zhang Z, Zhao C, Li C, Liu W, Liu Z, Li M (2017) Phylogenetic position of the white-cheeked macaque (Macaca leucogenys), a newly described primate from southeastern Tibet. Mol Phylogenet Evol 107:80–89

    PubMed  Google Scholar 

  • Feeroz MM (2003) Breeding activities of the pig-tailed macaque (Macaca leonina) in Bangladesh. Zoos’ Print Journal 18:1175–1179

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2015) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Garamszegi LZ (2014) Uncertainties due to within‐species variation in comparative studies: Measurement errors and statistical weights. Modern phylogenetic comparative methods and their application in evolutionary biology. Springer, Berlin Heidelberg, pp 157–199

  • Gogarten JF, Koenig A (2013) Reproductive seasonality is a poor predictor of receptive synchrony and male reproductive skew among nonhuman primates. Behav Ecol Sociobiol 67:123–134. https://doi.org/10.1007/s00265-012-1432-2

    Article  Google Scholar 

  • Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Hansen TF, Orzack SH (2005) Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons. Evolution 59:2063–2072

    PubMed  Google Scholar 

  • Heldstab SA, van Schaik CP, Müller DW, Rensch E, Lackey LB, Zerbe P, Hatt JM, Clauss M, Matsuda I (2020) Reproductive seasonality in primates: patterns, concepts and unsolved questions. Biol Rev 96:66–88

    PubMed  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, New York, pp 307–350

    Google Scholar 

  • José-Domínguez JM, Huynen M-C, Garcia CJ, Albert-Daviaud A, Savini T, Asensio N (2015a) Non-territorial macaques can range like territorial gibbons when partially provisioned with food. Biotropica 47:733–744

    Google Scholar 

  • José-Domínguez JM, Savini T, Asensio N (2015b) Ranging and site fidelity in northern pigtailed macaques (Macaca leonina) over different temporal scales. Am J Primatol 77:841–853. https://doi.org/10.1002/ajp.22409

    Article  PubMed  Google Scholar 

  • Kitamura S, Suzuki S, Yumoto T, Chuailua P, Plongmai K, Poonswad P, Noma N, Maruhashi T, Suckasam C (2005) A botanical inventory of a tropical seasonal forest in Khao Yai National Park, Thailand: Implications for fruit-frugivore interactions. Biodivers Conserv 14:1241–1262

    Google Scholar 

  • Kitamura S, Yumoto T, Noma N, Chuailua P, Maruhashi T, Wohandee P, Poonswad P (2008) Aggregated seed dispersal by wreathed hornbills at a roost site in a moist evergreen forest of Thailand. Ecol Res 23:943–952

    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. https://doi.org/10.1111/j.1469-7998.1997.tb02778.x

    Article  Google Scholar 

  • Kutsukake N, Nunn CL (2006) Comparative tests of reproductive skew in male primates: The roles of demographic factors and incomplete control. Behav Ecol Sociobiol 60:695–706

    Google Scholar 

  • MacArthur RH (1972) Geographical ecology: patterns in the distribution of species. Princeton University Press, Princeton

    Google Scholar 

  • Maestripieri D (1994) Mother-infant relationships in three species of macaques (Macaca mulatta, M. nemestrina, M. arctoides). I. Development of the mother-infant relationship in the first three months. Behaviour 131:75–96

    Google Scholar 

  • Malaivijitnond S, Arsaithamkul V, Tanaka H, Pomchote P, Jaroenporn S, Suryobroto B, Hamada Y (2012) Boundary zone between northern and southern pig-tailed macaques and their morphological differences. Primates 53:377–389

    PubMed  Google Scholar 

  • Manson JH (1996) Male dominance and mount series duration in Cayo Santiago rhesus macaques. Anim Behav 51:1219–1231

    Google Scholar 

  • Martin P, Bateson P (2007) Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  • Newton-Fisher NE (2012) Animal Behaviour Pro: V1.

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

    Google Scholar 

  • Nunn CL (1999) The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229–246. https://doi.org/10.1006/anbe.1999.1159

    Article  CAS  PubMed  Google Scholar 

  • Oi T (1996) Sexual behaviour and mating system of the wild pig-tailed macaque in west Sumatra. In: Fa D, Lindburg D (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, pp 342–368

    Google Scholar 

  • Ostner J, Nunn CL, Schülke O (2008) Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol 19:1150–1158

    PubMed  PubMed Central  Google Scholar 

  • Overduin-de Vries AM, Massen JJM, Spruijt BM, Sterck EHM (2012) Sneaky monkeys: an audience effect of male rhesus macaques (Macaca mulatta) on sexual behavior. Am J Primatol 74:217–228. https://doi.org/10.1002/ajp.21988

    Article  CAS  PubMed  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    CAS  PubMed  Google Scholar 

  • Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    CAS  PubMed  Google Scholar 

  • Paul A (1997) Breeding seasonality affects the association between dominance and reproductive success in non-human male primates. Folia Primatol (Basel) 68:344–349

    CAS  Google Scholar 

  • Paul A (2002) Sexual selection and mate choice. Int J Primatol 23:877–904

    Google Scholar 

  • Pebesma E (2018) Simple features for R: standardized support for spatial vector data. The R Journal 10:439–446

    Google Scholar 

  • Pewsey A (2002) Testing circular symmetry. Canadian J Stat 30:591–600

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2020) nlme: linear and nonlinear mixed effects models. R package version 3.1–151. Accessed 20 January 2021

  • R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reichard UH, Ganpanakngan M, Barelli C (2012) White-handed gibbons of Khao Yai: social flexibility, complex reproductive strategies, and a slow life history. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer-Verlag, Berlin Heidelberg, New York, pp 237–258. https://doi.org/10.1007/978-3-642-22514-7_11

    Chapter  Google Scholar 

  • Revell L (2012) phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–233

    Google Scholar 

  • Roos C, Zinner D (2015) Diversity and evolutionary history of macaques with special focus on Macaca mulatta and Macaca fascicularis. In: Bluemel J, Korte S, Schenck E, Weinbauer GF (eds) The nonhuman primate in nonclinical drug development and safety assessment. Academic Press, San Diego, pp 3–16

    Google Scholar 

  • Setchell JM, Kappeler PM (2003) Selection in relation to sex in primates. In: Slater PJB, Rosenblatt JS, Roper TJ, Snowdon CT, Naguib M (eds) Advances in the study of behavior, vol 33. Academic Press, San Diego, pp 87–173

    Google Scholar 

  • Setchell JM, Charpentier M, Wickings EJ (2005) Mate guarding and paternity in mandrills: factors influencing alpha male monopoly. Anim Behav 70:1105–1120. https://doi.org/10.1016/j.anbehav.2005.02.021

    Article  Google Scholar 

  • Sharma AK, Singh M, Kaumanns W, Krebs E, Singh M, Kumar MA, Kumara H (2006) Birth patterns in wild and captive lion-tailed macaques (Macaca silenus). Int J Primatol 27:1429–1439

    Google Scholar 

  • Smitinand T (1989) Floristic inventory of tropical countries. In: Cambell DC, Hammond HD (eds) Thailand. New York Botanical Garden, Boston, pp 65–82

    Google Scholar 

  • Soltis J (2004) Mating systems. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 135–151

    Google Scholar 

  • Soltis J, Mitsunaga F, Shimizu K, Yanagihara Y, Nozaki M (1999) Female mating strategy in an enclosed group of Japanese macaques. Am J Primatol 47:263–278

    CAS  PubMed  Google Scholar 

  • South A (2017a) rnaturalearth: world map data from natural earth. Accessed 12 October 2020

  • South A (2017b) rnaturalearthdata: world vector map data from natural earth used in ‘rnaturalearth’. Accessed 12 October 2020

  • Symonds MR, Blomberg SP (2014) A primer on phylogenetic generalised least squares. In: Garamszegi L (ed) Modern phylogenetic comparative methods and their application in evolutionary biology. Springer-Verlag, Berlin Heidelberg, pp 105–130

    Google Scholar 

  • Tardif S, Carville A, Elmore D, Williams LE, Rice K (2012) Reproduction and breeding of nonhuman primates. Nonhum Primates Biomed Res. https://doi.org/10.1016/B978-0-12-381365-7.00008-X

    Article  Google Scholar 

  • Thierry B (2011) The macaques: A double-layered social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective. Oxford University Press, Oxford, pp 229–241

    Google Scholar 

  • Tian J-D, Wang Z-L, Lu JQ, Wang BS, Chen JR (2013) Reproductive parameters of female Macaca mulatta tcheliensis in the temperate forest of Mount Taihangshan Jiyuan, China. Am J Primatol 75:605–612

    PubMed  Google Scholar 

  • van Schaik CP, van Noordwijk MA, Nunn CL (1999) Sex and social evolution in primates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 204–231

    Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Google Scholar 

  • Xiang Z, Yang W, Qi X, Yao H, Grueter CC, Garber PA, Li B, Li M (2017) An examination of factors potentially influencing birth distributions in golden snub-nosed monkeys (Rhinopithecus roxellana). PeerJ 5:e2892. https://doi.org/10.7717/peerj.2892

    Article  PubMed  PubMed Central  Google Scholar 

  • Young C, Majolo B, Heistermann M, Schulke O, Ostner J (2013) Male mating behaviour in relation to female sexual swellings, socio-sexual behaviour and hormonal changes in wild Barbary macaques. Horm Behav 63:32–39. https://doi.org/10.1016/j.yhbeh.2012.11.004

    Article  CAS  PubMed  Google Scholar 

  • Zinner D, Nunn C, van Schaik CP, Kappeler PM (2004) Sexual selection and exaggerated sexual swellings of female primates. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 71–89

    Google Scholar 

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Acknowledgements

We thank the National Research Council of Thailand (NRCT) for permitting FT and UHR to conduct research in the Kingdom of Thailand, and the Department of National Parks, Wildlife, and Plant Conservation (DNP) for allowing us to conduct research in Khao Yai National Park (KYNP). We also thank Mr. Kanchit Srinopawan, superintendent of KYNP, and his staff for their support of science research and administrative help. Data collection would have never been possible without the help of our field assistants, Corey Bither, Christopher Coll-Beswick, Nik Long, and Michelle Reed. Additionally, we thank Dr. Kazunari Matsudaira for assistance with phylogenetic analysis and Kaleigh Best for proofreading. Finally, we thank the anonymous reviewers and the editor-in-chief for their insightful comments on the manuscript. The project was partially funded by a grant from the SIU Graduate and Professional Student Research Awards to FT.

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Authors and Affiliations

  1. Department of Anthropology, Southern Illinois University Carbondale, Carbondale, USA

    Florian Trébouet & Ulrich H. Reichard

  2. Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, Thailand

    Suchinda Malaivijitnond

  3. National Primate Research Center of Thailand-Chulalongkorn University, Saraburi, Thailand

    Suchinda Malaivijitnond

  4. Center for Ecology, Southern Illinois University Carbondale, Carbondale, USA

    Ulrich H. Reichard

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  1. Florian Trébouet
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  2. Suchinda Malaivijitnond
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FT, SM, and UHR conceived and designed the study. FT and UHR submitted the ethical form. FT conducted fieldwork and analyzed the data. FT, SM, and UHR wrote the manuscript.

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Correspondence to Florian Trébouet.

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This research was non-invasive and based solely on observational data, without any animal experiments. Non-human primates observed in this research were previously habituated to human presence.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This research was conducted under research permission from NRCT, DNP, and KYNP in Thailand. All procedures performed in this study involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This research was carried out under IACUC permit number 15–008 from SIUC.

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Trébouet, F., Malaivijitnond, S. & Reichard, U.H. Reproductive seasonality in wild northern pig-tailed macaques (Macaca leonina). Primates 62, 491–505 (2021). https://doi.org/10.1007/s10329-021-00901-1

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