Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Differential responses of non-human primates to seasonal temperature fluctuations

  • 41 Accesses

Abstract

Non-human primates (NHPs) can adapt to conditions outside of their natural habitat and climatic ranges but this can be influenced by inherent evolutionary traits or plasticity of species that evolved in diverse environmental conditions. In this study, we investigated how five species of NHPs that have natural distributions across a range of climatic conditions responded to seasonal temperature changes in a captive environment. The activity levels of NHPs were affected by temperature changes over the season, where activity levels were generally reduced at the lower and higher temperature ranges. Species that are naturally found within narrower and warmer climatic ranges, compared to those found in colder environments with wider fluctuations in temperature, showed more marked changes in activity levels in response to temperature changes. In lower temperature conditions, three out of five species showed significantly lower activity levels; whereas in higher temperature conditions, the activity levels of all species did not significantly decrease. The frequency of thermoregulation behaviours was higher, and use of artificial thermoregulatory sources lower, for species that did not substantially adjust their activity levels in different temperature conditions. Our results suggest that NHPs largely retained the evolutionary traits related to thermoregulation, according to the different ambient conditions they evolved in and may have low behavioural plasticity in adapting to conditions outside of their natural ranges. These results provide insights for improving conservation and captive management and may have implications for understanding NHP resilience to the increasing impact of global climate change.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Agetsuma N (1995) Dietary selection by Yakushima macaques (Macaca fuscata yakui): the influence of food availability and temperature. Int J Primatol 16:611–627

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

  3. Aristizabal JF, Lévêque L, Chapman CA, Serio-Silva JC (2018) Impacts of temperature on behaviour of the Mexican endangered black howler monkey Alouatta pigra Lawrence, 1933 (Primates: Atelidae) in a fragmented landscape. Acta Zool Bugarica 70:377–382

  4. Bergmann C (1847) Uber die Verhältnisse der warmeokonomiedie Thiere zu ihrer grösse. Göttinger Studien 3:595–708.

  5. Bethge J, Wist B, Stalenberg E, Dausmann K (2017) Seasonal adaptations in energy budgeting in the primate Lepilemur leucopus. J Comp Physiol B 187:827–834

  6. Bicca-Marques JC, Calegaro-Marques C (1998) Behavioral thermoregulation in a sexually and developmentally dichromatic neotropical primate, the black-and-gold howling monkey (Alouatta caraya). Am J Phys Anthropol 106:533–546

  7. Campbell LA, Tkaczynski PJ, Lehmann J, Mouna M, Majolo B (2018) Social thermoregulation as a potential mechanism linking sociality and fitness: Barbary macaques with more social partners form larger huddles. Sci Rep 8:6074

  8. Campos FA, Fedigan LM (2009) Behavioral adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. Am J Phys Anthropol 138:101–111

  9. Carvalho JS, Graham B, Rebelo H, Bocksberger G, Meyer CFJ, Wich S, Kühl HS (2019) A global risk assessment of primates under climate and land use/cover scenarios. Glob Change Biol 25:3163–3179

  10. Cristóbal-Azkarate J, Maréchal L, Semple S, Majolo B, MacLarnon A (2016) Metabolic strategies in wild male Barbary macaques: evidence from faecal measurement of thyroid hormone. Biol Lett 12:20160168

  11. DaSilva GL (1993) Postural changes and behavioural thermoregulation in Colobus polykomos: the effect of climate and diet. Afr J Ecol 31:226–241

  12. Defler TR (1979) On the ecology and behavior of Cebus albifrons in eastern Colombia: I. Ecol Primates 20:475–490

  13. Del Grosso S, Parton W, Stohlgren T, Zheng D, Bachelet D, Prince S, Hibbard K, Olso R (2008) Global potential net primary production predicted from vegetation class, precipitation, and temperature. Ecology 89:2117–2126

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

  15. Donati G, Ricci E, Baldi N, Morelli V, Borgognini-Tarli SM (2011) Behavioral thermoregulation in a gregarious lemur, Eulemur collaris: effects of climatic and dietary-related factors. Am J Phys Anthropol 144:355–364

  16. Eppley TM, Watzek J, Dausmann KH, Ganzhorn JU, Donati G (2017) Huddling is more important than rest site selection for thermoregulation in southern bamboo lemurs. Anim Behav 127:153–161

  17. Erkert HG, Kappeler PM (2004) Arrived in the light: diel and seasonal activity patterns in wild Verreaux’s sifakas (Propithecus v. verreauxi; Primates: Indriidae). Behav Ecol Sociobiol 57:174–186

  18. Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Nekaris KA, Nijman V, Heymann EW, Lambert JE, Rovero F (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946

  19. Fietz J, Dausmann KH (2006) Big is beautiful: fat storage and hibernation as a strategy to cope with marked seasonality in the fat-tailed dwarf lemur (Cheirogaleus medius). In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 97–110

  20. Fleagle JG, Gilbert CC (2006) The biogeography of primate evolution: the role of plate tectonics, climate and chance. In: Fleagle JG, Lehman SM (eds) Primate biogeography. Springer, Boston, pp 375–418

  21. Galán-Acedo C, Arroyo-Rodríguez V, Andresen E, Arasa-Gisbert R (2019) Ecological traits of the world's primates database (Version 3). Zenodo. https://doi.org/10.5281/zenodo.2600338

  22. Ganzhorn JU, Klaus S, Ortmann S, Schmid J (2003) Adaptations to seasonality: some primate and non-primate examples. In: Pereira ME, Kappeler PM (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 132–148

  23. Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291

  24. Gestich CC, Caselli CB, Setz EZ (2014) Behavioural thermoregulation in a small Neotropical primate. Ethology 120:331–339

  25. Goodman SM, Langrand O (1996) A high mountain population of the ring-tailed lemur Lemur catta on the Andringitra Massif, Madagascar. Oryx 30:259–268

  26. Graham TL, Matthews HD, Turner SE (2016) A global-scale evaluation of primate exposure and vulnerability to climate change. Int J Primatol 37:158–174

  27. Grueter CC, Li D, Ren B, Li M (2013) Substrate use and postural behavior in free-ranging snub-nosed monkeys (Rhinopithecus bieti) in Yunnan. Integr Zool 8:335–345

  28. Guo ST, Hou R, Garber PA, Raubenheimer D, Righini N, Ji WH, Jay O, He SJ, Wu F, Li FF, Li BG (2018) Nutrient-specific compensation for seasonal cold stress in a free-ranging temperate colobine monkey. Funct Ecol 32:2170–2180

  29. Hanya G (2004) Seasonal variations in the activity budget of Japanese macaques in the coniferous forest of Yakushima: effects of food and temperature. Am J Primatol 63:165–177

  30. Hanya G, Kiyono M, Hayaishi S (2007) Behavioral thermoregulation of wild Japanese macaques: comparisons between two subpopulations. Am J Primatol 69:802–815

  31. Hanya G, Otani Y, Hongo S, Honda T, Okamura H, Higo Y (2018) Activity of wild Japanese macaques in Yakushima revealed by camera trapping: patterns with respect to season, daily period and rainfall. PLoS One 13:e0190631

  32. Heldmaier G, Steinlechner S, Ruf T, Wiesinger H, Klingenspor M (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhythms 4:139–153

  33. Hill RA (2006) Thermal constraints on activity scheduling and habitat choice in baboons. Am J Phys Anthropol 129:242–249

  34. Hill RA, Weingrill T, Barrett L, Henzi SP (2004) Indices of environmental temperatures for primates in open habitats. Primates 45:7–13

  35. Ioannou S, Chotard H, Davila-Ross M (2015) No strings attached: physiological monitoring of rhesus monkeys (Macaca mulatta) with thermal imaging. Front Behav Neurosci 9:160

  36. Janson C, Verdolin J (2005) Seasonally of primate births in relation to climate. Seasonality in primates: studies of living and extinct human and non-human primates. In: Brockman DK, Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 307–350

  37. Kamilar JM, Muldoon KM (2010) The climatic niche diversity of Malagasy primates: a phylogenetic perspective. PLoS One 5:e11073

  38. Kelley EA, Jablonski NG, Chaplin G, Sussman RW, Kamilar JM (2016) Behavioral thermoregulation in Lemur catta: the significance of sunning and huddling behaviors. Am J Primatol 78:745–754

  39. Kobbe S, Nowack J, Dausmann KH (2014) Torpor is not the only option: seasonal variations of the thermoneutral zone in a small primate. J Comp Physiol B 184:789–797

  40. Korstjens AH, Lehmann J, Dunbar RI (2010) Resting time as an ecological constraint on primate biogeography. Anim Behav 79:361–374

  41. Kumar A, Singh M, Molur S (2008) Macaca silenus. The IUCN Red List of Threatened Species 2008. https://www.iucnredlist.org/. Accessed 18 Nov 2019

  42. Kurup GU, Kumar A (1993) Time budget and activity patterns of the lion-tailed macaque (Macaca silenus). Int J Primatol 14:27–39

  43. Lambert JE (1998) Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20

  44. Lhota S, Sha CM, Bernard H, Matsuda I (2019) Proboscis monkey conservation: beyond the science. In: Behie AM, Teichroeb JA, Malone N (eds) Primate conservation in the anthropocene. Cambridge University Press, Cambridge, pp 182–196

  45. Li D, Ren B, Grueter CC, Li B, Li M (2010) Nocturnal sleeping habits of the Yunnan snub-nosed monkey in Xiangguqing, China. Am J Primatol 72:1092–1099

  46. Lippold LK (1989) Reproduction and survivorship in Douc langurs Pygathrix nemaeus in zoos. Int Zoo Yearbook 28:252–255

  47. Litchfield C, Dorrian J, Davis J, Lushington K, Dawson D (2011) Lessons in primate heat tolerance: a commentary based on the “Human Zoo” experience. J Appl Anim Welfare Sci 14:162–169

  48. Lubbe A, Hetem RS, McFarland R, Barrett L, Henzi PS, Mitchell D, Meyer LC, Maloney SK, Fuller A (2014) Thermoregulatory plasticity in free-ranging vervet monkeys, Chlorocebus pygerythrus. J Comp Physiol B 184:799–809

  49. Majolo B, McFarland R, Young C, Qarro M (2013) The effect of climatic factors on the activity budgets of a temperate primate, the Barbary macaque (Macaca sylvanus). Int J Primatol 34:500–514

  50. McFarland R, Majolo B (2013) Coping with the cold: predictors of survival in wild Barbary macaques Macaca sylvanus. Biol Let 9:20130428

  51. McFarland R, Barrett L, Boner R, Freeman NJ, Henzi SP (2014) Behavioral flexibility of vervet monkeys in response to climatic and social variability. Am J Phys Anthropol 154:357–364

  52. McFarland R, Fuller A, Hetem RS, Mitchell D, Maloney SK, Henzi SP, Barrett L (2015) Social integration confers thermal benefits in a gregarious primate. J Anim Ecol 84:871–878

  53. Mendiratta U, Kumar A, Mishra C, Sinha A (2009) Winter ecology of the Arunachal macaque Macaca munzala in Pangchen Valley, western Arunachal Pradesh, northeastern India. Am J Primatol 71:939–947

  54. Milton K (1998) Physiological ecology of howlers (Alouatta): energetic and digestive considerations and comparison with the Colobinae. Int J Primatol 19:513–548

  55. Morland HS (1993) Seasonal behavioral variation and its relationships to thermoregulation in ruffed lemurs. In: Ganzhorn JU, Kappeler PM (eds) Lemur social systems and their ecological basis. Plenum, New York, pp 193–205

  56. Mutschler T (2002) Alaotran gentle lemur: some aspects of its behavioral ecology. Evol Anthropol 11:101–104

  57. Nüchel J, Bøcher PK, Xiao W, Zhu AX, Svenning JC (2018) Snub-nosed monkeys (Rhinopithecus): potential distribution and its implication for conservation. Biodivers Conserv 1:1–22

  58. Ostner J, Kappeler PM (2004) Male life history and the unusual adult sex ratios of redfronted lemur, Eulemur fulvus rufus, groups. Anim Behav 67:249–259

  59. Paterson JD (1981) Postural-positional thermoregulatory behaviour and ecological factors in primates. Can Rev Phys Anthropol 3:3–11

  60. Pochron ST (2000) Sun avoidance in the yellow baboons (Papio cynocephalus cynocephalus) of Ruaha National Park, Tanzania. Variations with season, behavior and weather. Int J Biometeorol 44:141–147

  61. Pontzer H, Raichlen DA, Gordon AD, Schroepfer-Walker KK, Hare B, O’Neill MC, Muldoon KM, Dunsworth HM, Wood BM, Isler K, Burkart J (2014) Primate energy expenditure and life history. Proc Natl Acad Sci 111:1433–1437

  62. Randall D, Burggren W, French K (1997) Eckert animal physiology: mechanisms and adaptations, 4th edn. Freeman, New York

  63. Reed KE, Fleagle JG (1995) Geographic and climatic control of primate diversity. Proc Natl Acad Sci 92:7874–7876

  64. Rothman JM, Bryer MA (2019) The effects of humans on the primate nutritional landscape. In: Behie AM, Teichroeb JA, Malone N (eds) Primate conservation in the anthropocene. Cambridge University Press, Cambridge, pp 199–215

  65. Rothman JM, Chapman CA, Struhsaker TT, Raubenheimer D, Twinomugisha D, Waterman PG (2015) Long-term declines in nutritional quality of tropical leaves. Ecology 96:873–878

  66. Satinoff E (2011) Behavioral thermoregulation in the cold. Compr Physiol 14:481–505

  67. Schmid J, Speakman JR (2000) Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor. J Comp Physiol B 170:633–641

  68. Sha JCM, Kurihara Y, Tsuji Y, Take M, He T, Kaneko A, Suda-Hashimoto N, Morimoto M, Takayoshi N, Zahariev A, Blanc S, Hanya G (2018) Seasonal variation of energy expenditure in Japanese macaques (Macaca fuscata). J Therm Biol 76:139–146

  69. Silk JB (1994) Social relationships of male bonnet macaques: male bonding in a matrilineal society. Behaviour 130:271–291

  70. Sussman RW (1991) Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. Am J Phys Anthropol 84:43–58

  71. Struhsaker T, Oates JF, Hart J, Butynski TM (2008) Cercopithecus neglectus. The IUCN Red List of Threatened Species 2008. Accessed 21 Nov 2019

  72. Tattersall GJ, Cadena V (2010) Insights into animal temperature adaptations revealed through thermal imaging. Imaging Sci J 58:261–268

  73. Terrien J, Perret M, Aujard F (2011) Behavioral thermoregulation in mammals: a review. Front Biosci 16:1428–1444

  74. Thierry B, Bynum EL, Baker S, Matsumura S, Muroyama Y, Brien TGO, Petit O, Watanabe K (2000) The social repertoire of Sulawesi macaques. Primate Res 16:203–226

  75. Thompson CL, Powell BL, Williams SH, Hanya G, Glander KE, Vinyard CJ (2017) Thyroid hormone fluctuations indicate a thermoregulatory function in both a tropical (Alouatta palliata) and seasonally cold-habitat (Macaca fuscata) primate. Am J Primatol 79:e22714

  76. Tsuji Y (2010) Regional, temporal, and interindividual variation in the feeding ecology of Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, Japan, pp 99–127

  77. Troisi A, Schino G (1986) Diurnal and climatic influences on allogrooming behaviour in a captive group of Java monkeys. Anim Behav 34:1420–1426

  78. Van Doorn AC, O'riain MJ, Swedell L (2010) The effects of extreme seasonality of climate and day length on the activity budget and diet of semi-commensal chacma baboons (Papio ursinus) in the Cape Peninsula of South Africa. Am J Primatol 72:104–112

  79. Van Schaik CP (2013) The costs and benefits of flexibility as an expression of behavioural plasticity: a primate perspective. Philos Trans R Soc B Biol Sci 368:20120339

  80. Van Schaik CP, Brockman DK (2005) Seasonality in primate ecology, reproduction and life history: an overview. In: Brockman DK, Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 3–20

  81. Walker FM, Sajita NK (2011) Long-term persistence of de Brazza's Monkey (Cercopithecus neglectus) in a Kenyan Forest fragment. J East Afr Nat Hist 100:69–87

  82. Weingrill T, Gray DA, Barrett L, Henzi SP (2004) Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Horm Behav 45:259–269

  83. Yang J, Liu HZ, Ou CQ, Lin GZ, Zhou Q, Shen GC, Chen PY, Guo Y (2013) Global climate change: impact of diurnal temperature range on mortality in Guangzhou, China. Environ Pollut 175:131–136

  84. Yanuar A, Chivers DJ, Sugardjito J, Martyr DJ, Holden JT (2009) The population distribution of pig-tailed macaque (Macaca nemestrina) and long-tailed macaque (Macaca fascicularis) in west central Sumatra, Indonesia. Asian Primates J 1:2–11

  85. Zhao X, Ren B, Li D, Garber PA, Zhu P, Xiang Z, Grueter CC, Liu Z, Li M (2019) Climate change, grazing, and collecting accelerate habitat contraction in an endangered primate. Biol Cons 231:88–97

Download references

Acknowledgement

We wish to thank the management of Guangzhou Zoo for supporting this study and the staff of the primate section for accommodating the logistical arrangements and providing valuable information and knowledge about the primates under their care. We also wish to thank the School of Sociology and Anthropology and the School of Life Sciences at Sun Yat-sen University for their support.

Author information

Correspondence to John Chih Mun Sha.

Ethics declarations

Ethical approval

All research conducted in this study adhered to international guidelines for the ethical treatment of animals. No invasive experiments were conducted. The authors declare that there are no financial, professional or personal conflicts of interest related to this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sha, J.C.M., Du, H., Deng, J. et al. Differential responses of non-human primates to seasonal temperature fluctuations. Primates (2020). https://doi.org/10.1007/s10329-020-00801-w

Download citation

Keywords

  • Activity
  • Adaptation
  • Behavioural plasticity
  • Captive primates
  • Thermoregulation