Keeping cool in the heat: Behavioral thermoregulation and body temperature patterns in wild vervet monkeys.
behavior
body temperature
climate
thermoregulation
Journal
American journal of physical anthropology
ISSN: 1096-8644
Titre abrégé: Am J Phys Anthropol
Pays: United States
ID NLM: 0400654
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
07
05
2019
revised:
19
10
2019
accepted:
22
10
2019
pubmed:
13
11
2019
medline:
21
11
2020
entrez:
13
11
2019
Statut:
ppublish
Résumé
Climate change is having a significant impact on biodiversity and increasing attention is therefore being devoted to identifying the behavioral strategies that a species uses to cope with climatic stress. We explore how wild vervet monkeys (Chlorocebus pygerythrus) respond to heat stress, and how behavioral adaptations are used to regulate body temperature. We implanted wild vervet monkeys with temperature-sensitive data loggers and related the body temperature rhythms of these animals to their use of thermoregulatory behaviors. Environmental temperature had a positive effect on the mean, minima and maxima of daily body temperatures. Environmental temperature had a positive effect on the amount of time that vervet monkeys spent in the shade, and animals that spent more time in the shade had lower body temperature maxima. Drinking water did not have a proximate effect on body temperature, most likely a consequence of their regular access to drinking water. Body temperatures were observed to decrease after swimming events, but tended to return to pre-swim temperatures within 1 hr, suggesting a limited thermal benefit of this behavior. Our data support the view that vervet monkeys cope well in the heat, and use behavior as a means to aid thermoregulation. The ability of primates to be flexible in their use of thermoregulatory behaviors can contribute positively to their capacity to cope with environmental variability. However, given its broad effect on plant productivity and habitat loss, climate change is a major threat to species' biogeographical distribution and survival.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
407-418Informations de copyright
© 2019 Wiley Periodicals, Inc.
Références
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227-266. https://doi.org/10.1163/156853974X00534
Baker, M. A. (1989). Thermoregulation in dehydrated vertebrates. Milestones in Environmental Physiology, 7, 101-107.
Barrett, L., Gaynor, D., Rendall, D., Mitchell, D., & Henzi, S. P. (2004). Habitual cave use and thermoregulation in chacma baboons (Papio hamadryas ursinus). Journal of Human Evolution, 46, 215-222. https://doi.org/10.1016/j.jhevol.2003.11.005
Barton, K., & Barton, M. K. (2015). Package “MuMIn”. ftp://155.232.191.229/cran/web/packages/MuMIn/.
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48. https://doi.org/10.18637/jss.v067.i01
Bicca-Marques, J. C., & Calegaro-Marques, C. (1998). Behavioral thermoregulation in a sexually and developmentally dichromatic neotropical primate, the black-and-gold howling monkey (Alouatta caraya). American Journal of Physical Anthropology, 106(4), 533-546. https://doi.org/10.1002/(SICI)1096-8644(199808)
Blanco, M. B., Dausmann, K. H., Ranaivoarisoa, J. F., & Yoder, A. D. (2013). Underground hibernation in a primate. Scientific Reports, 3, 1768. https://doi.org/10.1038/srep01768
Bouchama, A., Roberts, G., Al Mohanna, F., El-Sayed, R., Lach, B., Chollet-Martin, S., … de Prost, D. (2005). Inflammatory, hemostatic, and clinical changes in a baboon experimental model for heatstroke. Journal of Applied Physiology, 98, 697-705. https://doi.org/10.1152/japplphysiol.00461.2004
Brain, C., & Mitchell, D. (1999). Body temperature changes in free-ranging baboons (Papio hamadryas ursinus) in the Namib Desert, Namibia. International Journal of Primatology, 20, 585-598. https://doi.org/10.1023/A:1020394824547
Cahill, A. E., Aiello-Lammens, M. E., Fisher-Reid, M. C., Hua, X., Karanewsky, C. J., Yeong Ryu, H., … Wiens, J. J. (2013). How does climate change cause extinction? Proceedings of the Royal Society of London B: Biological Sciences, 280(1750), 20121890. https://doi.org/10.1098/rspb.2012.1890
Campos, F. A., & Fedigan, L. M. (2009). Behavioural adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. American Journal of Physical Anthropology, 138, 101-111. https://doi.org/10.1002/ajpa.20908
Campos, F. A., Morris, W. F., Alberts, S. C., Altmann, J., Brockman, D. K., Cords, M., … Fedigan, L. M. (2017). Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species. Global Change Biology, 23(11), 4907-4921. https://doi.org/10.1111/gcb.13754
Cheney, D. L., Seyfarth, R. M., Fischer, J., Beehner, T., Bergman, T., Johnson, S. E., … Silk, J. B. (2004). Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. International Journal of Primatology, 25, 401-428. https://doi.org/10.1023/B:IJOP.0000019159.75573.13
Colquhoun, D. (2014). An investigation of the false discovery rate and the misinterpretation of p-values. Royal Society Open Science, 1, 140216. https://doi.org/10.1098/rsos.140216
Danzy, J., Grobler, J. P., Freimer, N., & Turner, T. (2012). Sunbathing: A behavioral response to seasonal climatic change among south African vervet monkeys (Chlorocebus aethiops). African Primates, 7(2), 230-237.
Dausmann, K. H. (2005). Measuring body temperature in the field-Evaluation of external vs. implanted transmitters in a small mammal. Journal of Thermal Biology, 30(3), 195-202. https://doi.org/10.1016/j.jtherbio.2004.11.003
Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2004). Physiology: Hibernation in a tropical primate. Nature, 429(6994), 825-826. https://doi.org/10.1038/429825a
Dunbar, R. I. M., Korstjens, A. H., & Lehmann, J. (2009). Time as an ecological constraint. Biological Reviews, 84, 413-429. https://doi.org/10.1111/j.1469-185X.2009.00080.x
Duncan, L. M., & Pillay, N. (2013). Shade as a thermoregulatory resource for captive chimpanzees. Journal of Thermal Biology, 38(4), 169-177. https://doi.org/10.1016/j.jtherbio.2013.02.009
Engelbrecht, F., Adegoke, J., Bopape, M. J., Naidoo, M., Garland, R., Thatcher, M., … Gatebe, C. (2015). Projections of rapidly rising surface temperatures over Africa under low mitigation. Environmental Research Letters, 10(8), 085004. https://doi.org/10.1088/1748-9326/10/8/085004
Eppley, T. M., Watzek, J., Dausmann, K. H., Ganzhorn, J. U., & Donati, G. (2017). Huddling is more important than rest site selection for thermoregulation in southern bamboo lemurs. Animal Behaviour, 127, 153-161. https://doi.org/10.1016/j.anbehav.2017.03.019
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Di Fiore, A., … Rovero, F. (2017). Impending extinction crisis of the world's primates: Why primates matter. Science Advances, 3, e1600946. https://doi.org/10.1126/sciadv.1600946
Fedigan, L. (1972). Social and solitary play in a colony of vervet monkeys (Cercopithecus aethiops). Primates, 13(4), 347-364. https://doi.org/10.1007/BF01793655
Fleagle, J. G., & Gilbert, C. C. (2006). The biogeography of primate evolution: The role of plate tectonics, climate and chance. In S. M. Lehman & J. G. Fleagle (Eds.), Primate biogeography (pp. 375-418). Boston, MA: Springer. https://doi.org/10.1007/0-387-31710-4_13
Fuchs, A. J., Gilbert, C. C., & Kamilar, J. M. (2017). Ecological niche modeling of the genus Papio. American Journal of Physical Anthropology, 166(4), 812-823. https://doi.org/10.1002/ajpa.23470
Fuller, A., Dawson, T., Helmuth, B., Hetem, R. S., Mitchell, D., & Maloney, S. K. (2010). Physiological mechanisms in coping with climate change. Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches, 83, 713-720. https://doi.org/10.1086/652242
Fuller, A., Mitchell, D., Maloney, S. K., & Hetem, R. S. (2016). Towards a mechanistic understanding of the responses of large terrestrial mammals to heat and aridity associated with climate change. Climate Change Responses, 3, 10. https://doi.org/10.1186/s40665-016-0024-1
Fuller, A., Oosthuyse, T., Maloney, S. K., & Mitchell, D. (1999). Evaluation of miniature data loggers for body temperature measurement during sporting activities. European Journal of Applied Physiology and Occupational Physiology, 79(4), 341-346. https://doi.org/10.1007/s004210050518
Gelman, A. (2008). Scaling regression inputs by dividing by two standard deviations. Statistics in Medicine, 27(15), 2865-2873. https://doi.org/10.1002/sim.3107
Grueter, C. C., Li, D., Ren, B., Wei, F., Xiang, Z., & van Schaik, C. P. (2009). Fallback foods of temperate-living primates: A case study on snub-nosed monkeys. American Journal of Physical Anthropology, 140(4), 700-715. https://doi.org/10.1002/ajpa.21024
Guo, S. T., Hou, R., Garber, P. A., Raubenheimer, D., Righini, N., Ji, W. H., … Li, B. G. (2018). Nutrient-specific compensation for seasonal cold stress in a free-ranging temperate colobine monkey. Functional Ecology, 32(9), 2170-2180. https://doi.org/10.1111/1365-2435.13134
Henzi, S. P., Hetem, R., Fuller, A., Maloney, S., Young, C., Mitchell, D., … McFarland, R. (2017). Consequences of sex-specific sociability for thermoregulation in male vervet monkeys during winter. Journal of Zoology, 302(3), 193-200. https://doi.org/10.1111/jzo.12448
Hetem, R. S., Fuller, A., Maloney, S. K., & Mitchell, D. (2014). Responses of large mammals to climate change. Temperature, 1(2), 115-127. https://doi.org/10.4161/temp.29651
Hetem, R. S., Maloney, S. K., Fuller, A., Meyer, L. C., & Mitchell, D. (2007). Validation of a biotelemetric technique, using ambulatory miniature black globe thermometers, to quantify thermoregulatory behaviour in ungulates. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 307(6), 342-356. https://doi.org/10.1002/jez.389
Hetem, R. S., Maloney, S. K., Fuller, A., & Mitchell, D. (2016). Heterothermy in large mammals: Inevitable or implemented. Biological Reviews of the Cambridge Philosophical Society, 91, 187-205. https://doi.org/10.1111/brv.12166
Hidden, P. A. (2009). Thermoregulation in African elephants (Loxodonta African). (Unpublished doctoral dissertation). University of the Witwatersrand, South Africa.
Hiley, P. G. (1976). The thermoregulatory responses of the galago (Galago crassicaudatus), the baboon (Papio cynocephalus) and the chimpanzee (Pan stayrus) to heat stress. The Journal of Physiology, 254(3), 657-671. https://doi.org/10.1113/jphysiol.1976.sp011251
Hill, R. A. (2006). Thermal constraints on activity scheduling and habitat choice in baboons. American Journal of Physical Anthropology, 129(2), 242-249. https://doi.org/10.1002/ajpa.20264
Hill, S. E., & Winder, I. C. (2019). Predicting the impacts of climate change on Papio baboon biogeography: Are widespread, generalist primates “safe”? Journal of Biogeography, 46(7), 1380-1405. https://doi.org/10.1111/jbi.13582
Hoffman, M. T., Carrick, P. J., Gillson, L., & West, A. G. (2009). Drought, climate change and vegetation response in the succulent karoo, South Africa. South African Journal of Science, 105, 54-60. https://doi.org/10.1590/S0038-23532009000100021
Kappeler, P. M., Barrett, L., Blumstein, D. T., & Clutton-Brock, T. H. (2013). Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Philosophical Transactions of the Royal Society B, 368, 20120337. https://doi.org/10.1098/rstb.2012.0337
Kearney, M., Shine, R., & Porter, W. P. (2009). The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proceedings of the National Academy of Sciences USA, 106, 3835-3840. https://doi.org/10.1073/pnas.0808913106
Kelley, E. A., Jablonski, N. G., Chaplin, G., Sussman, R. W., & Kamilar, J. M. (2016). Behavioral thermoregulation in Lemur catta: The significance of sunning and huddling behaviors. American Journal of Primatology, 78(7), 745-754. https://doi.org/10.1002/ajp.22538
Kempf, E. (2009). Patterns of water use in primates. Folia Primatologica, 80(4), 275-294. https://doi.org/10.1159/000252586
Kimani, J. K. (1983). Some histological aspects of the palmar digital pads in the vervet monkey. Folia Primatologica, 41(1), 147-155. https://doi.org/10.1159/000156125
Kobbe, S., Nowack, J., & Dausmann, K. H. (2014). Torpor is not the only option: Seasonal variations of the thermoneutral zone in a small primate. Journal of Comparative Physiology B, 184(6), 789-797. https://doi.org/10.1007/s00360-014-0834-z
Korstjens, A. H., Lehmann, J., & Dunbar, R. I. M. (2010). Resting time as an ecological constraint on primate biogeography. Animal Behaviour, 79, 361-374. https://doi.org/10.1016/j.anbehav.2009.11.012
Kutner, M. H., Nachtsheim, C. J., & Neter, J. (2004). Applied linear regression models (4th ed.). New York, USA: McGraw-Hill Irwin.
Lehmann, J., Korstjens, A. H., & Dunbar, R. I. M. (2010). Apes in a changing world-the effects of global warming on the behaviour and distribution of African apes. Journal of Biogeography, 37(12), 2217-2231. https://doi.org/10.1111/j.1365-2699.2010.02373.x
Lopes, K. G., & Bicca-Marques, J. C. (2017). Ambient temperature and humidity modulate the behavioural thermoregulation of a small arboreal mammal (Callicebus bernhardi). Journal of Thermal Biology, 69, 104-109. https://doi.org/10.1016/j.jtherbio.2017.06.010
Lubbe, A., Hetem, R. S., McFarland, R., Barrett, L., Henzi, P. S., Mitchell, D., … Fuller, A. (2014). Thermoregulatory plasticity in free-ranging vervet monkeys, Chlorocebus pygerythrus. Journal of Comparative Physiology B, 184(6), 799-809. https://doi.org/10.1007/s00360-014-0835-y
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). International Journal of Primatology, 34, 500-514. https://doi.org/10.1007/s10764-013-9678-8
Mathewson, P. D. 2018. Biophysical models as tools to improve understanding of endotherm responses to environmental change. (PhD dissertation), Department of Zoology, University of Wisconsin, Madison, Wisconsin, USA. ProQuest Dissertations Publishing: 13425321.
McDougall, P., Forshaw, N., Barrett, L., & Henzi, S. P. (2010). Leaving home: Responses to water depletion by vervet monkeys. Journal of Arid Environments, 74, 924-927. https://doi.org/10.1016/j.jaridenv.2010.04.003
McFarland, R., Barrett, L., Boner, R., Freeman, N. J., & Henzi, S. P. (2014). Behavioral flexibility of vervet monkeys in response to climatic and social variability. American Journal of Physical Anthropology, 154(3), 357-364. https://doi.org/10.1002/ajpa.22518
McFarland, R., Barrett, L., Costello, M., Fuller, A., Hetem, R. S., Maloney, S. K., … Henzi, S. P. (2019). Supporting data: Keeping cool in the heat: Behavioral thermoregulation and body temperature patterns in wild vervet monkeys. Figshare. https://doi.org/10.6084/m9.figshare.8089220
McFarland, R., Fuller, A., Hetem, R. S., Mitchell, D., Maloney, S. K., Henzi, S. P., & Barrett, L. (2015). Social integration confers thermal benefits in a gregarious primate. Journal of Animal Ecology, 84(3), 871-878. https://doi.org/10.1111/1365-2656.12329
McFarland, R., Henzi, S. P., & Barrett, L. (2019). The social and thermal competence of wild vervet monkeys. In T. Turner (Ed.), Savannah monkeys: The genus Chlorocebus (pp. 199-207). Cambridge, England: Cambridge University Press.
McFarland, R., Hetem, R. S., Fuller, A., Mitchell, D., Henzi, S. P., & Barrett, L. (2013). Assessing the reliability of biologger techniques to measure activity in a free-ranging primate. Animal Behaviour, 85, 861-866. https://doi.org/10.1016/j.anbehav.2013.02.005
McFarland, R., & Majolo, B. (2013). Coping with the cold: Predictors of survival in wild barbary macaques, Macaca sylvanus. Biology Letters, 9(4), 20130428. https://doi.org/10.1098/rsbl.2013.0428
McFarland, R., Murphy, D., Lusseau, D., Henzi, S. P., Parker, J. L., Pollet, T. V., & Barrett, L. (2017). The “strength of weak ties” among female baboons: Fitness-related benefits of social bonds. Animal Behaviour, 126, 101-106. https://doi.org/10.1016/j.anbehav.2017.02.002
Mitchell, D., Fuller, A., & Maloney, S. K. (2009). Homeothermy and primate bipedalism: Is water shortage or solar radiation the main threat to baboon (Papio hamadryas) homeothermy? Journal of Human Evolution, 56(5), 439-446. https://doi.org/10.1016/j.jhevol.2009.03.003
Mitchell, D., Snelling, E. P., Hetem, R. S., Maloney, S. K., Strauss, W. M., & Fuller, A. (2018). Revisiting concepts of thermal physiology: Predicting responses of mammals to climate change. Journal of Animal Ecology, 87(4), 956-973. https://doi.org/10.1111/1365-2656.12818
Mitchell, N. J., Kearney, M. R., Nelson, N. J., & Porter, W. P. (2008). Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara? Proceedings of the Royal Society B, 275, 2185-2193. https://doi.org/10.1098/rspb.2008.0438
Nakagawa, S., & Schielzeth, H. (2012). A general and simple method for obtaining Rcol2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4, 133-142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Nowack, J., Mzilikazi, N., & Dausmann, K. H. (2010). Torpor on demand: Heterothermy in the non-lemur primate Galago moholi. PLoS One, 5(5), e10797. https://doi.org/10.1371/journal.pone.0010797
Nowack, J., Wippich, M., Mzilikazi, N., & Dausmann, K. H. (2013). Surviving the cold, dry period in Africa: Behavioral adjustments as an alternative to heterothermy in the African lesser bushbaby (Galago moholi). International Journal of Primatology, 34(1), 49-64. https://doi.org/10.1007/s10764-012-9646-8
Ogawa, H., & Takahashi, H. (2003). Triadic positions of Tibetan macaques huddling at a sleeping site. International Journal of Primatology, 24, 591-606. https://doi.org/10.1023/A:1023792431064
Ostner, J., & Schülke, O. (2018). Linking sociality to fitness in primates: A call for mechanisms. Advances in the Study of Behavior, 50, 127-175. https://doi.org/10.1016/bs.asb.2017.12.001
Pacifici, M., Foden, W. B., Visconti, P., Watson, J. E., Butchart, S. H., Kovacs, K. M., … Corlett, R. T. (2015). Assessing species vulnerability to climate change. Nature Climate Change, 5, 215-224. https://doi.org/10.1038/nclimate2448
Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics, 37, 637-669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Pasternak, G., Brown, L. R., Kienzle, S., Fuller, A., Barrett, L., & Henzi, S. P. (2013). Population ecology of vervet monkeys in a high latitude, semi-arid riparian woodland. Koedoe, 55(1), 1-9. https://doi.org/10.4102/koedoe.v55i1.1078
Pruetz, J. D. (2007). Evidence of cave use by savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal: Implications for thermoregulatory behavior. Primates, 48(4), 316-319. https://doi.org/10.1007/s10329-007-0038-1
Pruetz, J. D., & Bertolani, P. (2009). Chimpanzee (Pan troglodytes verus) behavioral responses to stresses associated with living in a savanna-mosaic environment: Implications for hominin adaptations to open habitats. PaleoAnthropology, 2009, 252-262. https://doi.org/10.4207/PA.2009.ART33
R Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing https://www.R-project.org/
Rideout, B. A., Gardiner, C. H., Stalis, I. H., Zuba, J. R., Hadfield, T., & Visvesvara, G. S. (1997). Fatal infections with Balamuthia mandrillaris (a free-living amoeba) in gorillas and other Old World primates. Veterinary Pathology, 34, 15-22. https://doi.org/10.1177/030098589703400103
Scheffers, B. R., De Meester, L., Bridge, T. C., Hoffmann, A. A., Pandolfi, J. M., Corlett, R. T., … Pacifici, M. (2016). The broad footprint of climate change from genes to biomes to people. Science, 354(6313), aaf7671. https://doi.org/10.1126/science.aaf7671
Schmid, J. (2000). Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: Energetic consequences and biological significance. Oecologia, 123(2), 175-183. https://doi.org/10.1007/s004420051003
Schmid, J., Ruf, T., & Heldmaier, G. (2000). Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. Journal of Comparative Physiology B, 170(1), 59-68. https://doi.org/10.1007/s003600050008
Seebacher, F., & Franklin, C. E. (2012). Determining environmental causes of biological effects: the need for amechanistic physiological dimension in conservation biology. Philosophical Transactions of the Royal Society B, 367, 1607-1614. https://doi.org/10.1098/rstb.2012.0036
Setchell, J., Bedjabaga, I.-B., Goossens, B., Reed, P., Wickings, E., & Knapp, L. (2007). Parasite revalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. International Journal of Primatology, 28, 1345-1362. https://doi.org/10.1007/s10764-007-9225-6
Smith, T., Rose, K. D., & Gingerich, P. D. (2006). Rapid Asia-Europe-North America geographic dispersal of earliest Eocene primate Teilhardina during the Paleocene-Eocene thermal maximum. Proceedings of the National Academy of Sciences, 103(30), 11223-11227. https://doi.org/10.1073/pnas.0511296103
Stelzner, J. K., & Hausfater, G. (1986). Posture, microclimate, and thermoregulation in yellow baboons. Primates, 27(4), 449-463. https://doi.org/10.1007/BF02381890
Strier, K. B. (2017). What does variation in primate behavior mean? American Journal of Physical Anthropology, 162, 4-14. https://doi.org/10.1002/ajpa.23143
Sussman, R. W. (1991). Primate origins and the evolution of angiosperms. American Journal of Primatology, 23(4), 209-223. https://doi.org/10.1002/ajp.1350230402
Sussman, R. W., Rasmussen, D. T., & Raven, P. H. (2013). Rethinking primate origins again. American Journal of Primatology, 75(2), 95-106. https://doi.org/10.1002/ajp.22096
Takahashi, H. (1997). Huddling relationships in night sleeping groups among wild Japanese macaques in Kinkazan Island during winter. Primates, 38, 57-68. https://doi.org/10.1007/BF02385922
Thompson, C. L., Powell, B. L., Williams, S. H., Hanya, G., Glander, K. E., & Vinyard, C. J. (2017). Thyroid hormone fluctuations indicate a thermoregulatory function in both a tropical (Alouatta palliata) and seasonally cold-habitat (Macaca fuscata) primate. American Journal of Primatology, 79(11), e22714. https://doi.org/10.1002/ajp.22714
Thompson, C. L., Williams, S. H., Glander, K. E., Teaford, M. F., & Vinyard, C. J. (2014). Body temperature and thermal environment in a generalized arboreal anthropoid, wild mantled howling monkeys (Alouatta palliata). American Journal of Physical Anthropology, 154(1), 1-10. https://doi.org/10.1002/ajpa.22505
Urban, M. C., Bocedi, G., Hendry, A. P., Mihoub, J. B., Pe'er, G., Singer, A., … Gonzalez, A. (2016). Improving the forecast for biodiversity under climate change. Science, 353(6304), aad8466. https://doi.org/10.1126/science.aad8466
van Schaik, C. P., van Amerongen, A., & van Noordwijk, M. A. (1996). Riverine refuging by wild Sumatran longtailed macaques (Macaca fascicularis). In Fa, J. E., & Lindburg, D. G. Evolution and ecology of macaque societies, pp 160-181. Cambridge University Press, Cambridge, England.
Weingrill, T., Gray, D. A., Barrett, L., & Henzi, S. P. (2004). Fecal cortisol levels in free-ranging female chacma baboons: Relationship to dominance, reproductive state and environmental factors. Hormones and Behavior, 45(4), 259-269. https://doi.org/10.1016/j.yhbeh.2003.12.004