Abstract
High temperatures pose a significant risk to mammals, especially those living in hot and dry environments such as southern Madagascar, the location of Bezà Mahafaly Special Reserve (BMSR). At BMSR, we observed sifakas (Propithecus verreauxi) hugging tree trunks while resting on the ground during the mid-day heat of the late dry season. These highly arboreal lemurs are more vulnerable to predation on the ground. To explore whether tree hugging affords a thermal advantage, we collected 615.7 hours of behavioral data on sifakas in six groups, together with the temperature of the air, ground, and tree trunks used during hugging bouts. We observed hugging only when ambient temperatures were high (above 30°C), and mean daytime temperature had a significant positive effect on whether sifakas engaged in tree hugging on a given day. The surface at the base of hugged trees were significantly cooler (by ~3-5°C) than ambient air temperatures and surface temperatures further up the trunk, likely enabling animals to dissipate body heat. These data suggest that terrestrial tree hugging behavior contributes to thermoregulation in this lemur population and, coupled with evidence from koalas (Phasocolarctos cinereus), indicate that trees may provide a widespread thermal benefit for mammals facing heat stress. The capacity of sifakas to avoid heat stress will be critical to their persistence under predicted temperature increases in southern Madagascar over coming decades, and needs to be better understood in the context of long-term conservation planning.
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References
Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716–723. https://doi.org/10.1109/TAC.1974.1100705.
Avdelidis, N. P., & Moropoulou, A. (2003). Emissivity considerations in building thermography. Energy and Buildings, 35(7), 663–667. https://doi.org/10.1016/S0378-7788(02)00210-4.
Baker, M. A. (1984). Thermoregulatory responses to exercise in dehydrated dogs. Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, 56(3), 635–640. https://doi.org/10.1152/jappl.1984.56.3.635.
Baker, M. A. (1989). Effects of dehydration and rehydration on thermoregulatory sweating in goats. Journal of Physiology, 417, 421–435. https://doi.org/10.1097/00005768-200110000-00013.
Barton, A. M., Fetcher, N., & Redhead, S. (1989). The relationship between treefall gap size and light flux in a neotropical rain forest in Costa Rica. Journal of Tropical Ecology, 5, 437–439. https://doi.org/10.1017/S0266467400003898.
Barton, K. (2020). MuMIn: Multi-model inference. https://CRAN.R-project.org/package=MuMIn.
Bates, D., Mächler, M., Bolker, B. M., & Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01.
Bernard, V., Staffa, E., Mornstein, V., & Bourek, A. (2013). Infrared camera assessment of skin surface temperature — Effect of emissivity. Physica Medica, 29(6), 583–591. https://doi.org/10.1016/j.ejmp.2012.09.003.
Best, A., & Kamilar, J. M. (2018). The evolution of eccrine sweat glands in human and nonhuman primates. Journal of Human Evolution, 117(February), 33–43. https://doi.org/10.1016/j.jhevol.2017.12.003.
Blanco, M B, & Godfrey, L. R. (2014). Hibernation patterns of dwarf lemurs in the high altitude forest of eastern Madagascar. In N. B. Grow, S. Gursky-Doyen, & A. Krzton (Eds.), High altitude primates (pp. 23–42). New York, NY: Springer.
Blanco, M. B., Dausmann, K. H., Ranaivoarisoa, J. F., & Yoder, A. D. (2013). Underground hibernation in a primate. Scientific Reports, 3, 1–4. https://doi.org/10.1038/srep01768.
Blanco, M. B., Andriantsalohimisantatra, A. A., Rivoharison, T. V., & Andriambeloson, J. B. (2017). Evidence of prolonged torpor in Goodman’s mouse lemurs at Ankafobe forest, Central Madagascar. Primates, 58, 31–37. https://doi.org/10.1007/s10329-016-0586-3.
Blanco, M. B., Dausmann, K. H., Faherty, S. L., & Yoder, A. D. (2018). Tropical heterothermy is “cool”: The expression of daily torpor and hibernation in primates. Evolutionary Anthropology, 27(4), 147–161. https://doi.org/10.1002/evan.21588.
Briscoe, N. J., Handasyde, K. A., Griffiths, S. R., Porter, W. P., Krockenberger, A., & Kearney, M. R. (2014). Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals. Biology Letters, 10(6), 20140235. https://doi.org/10.1098/rsbl.2014.0235.
Brockman, D. K., Godfrey, L. R., Dollar, L. J., & Ratsirarson, J. (2008). Evidence of invasive Felis silvestris predation on Propithecus verreauxi at Beza Mahafaly special reserve. Madagascar. International Journal of Primatology, 29(1), 135–152. https://doi.org/10.1007/s10764-007-9145-5.
Brown, K. J., & Downs, C. T. (2006). Seasonal patterns in body temperature of free-living rock ryax (Procavia capensis). Comparative Biochemistry and Physiology, Part A, 143, 42–49.
Buck, C. L., & Barnes, B. M. (2000). Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. American Journal of Physiology — Regulatory Integrative and Comparative. Physiology, 279, R255–R262. https://doi.org/10.1152/ajpregu.2000.279.1.r255.
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information–theoretic approach (2nd ed.). Springer.
Campos, F. A., & Fedigan, L. M. (2009). Behavioral 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(1), 101–111. https://doi.org/10.1002/ajpa.20908.
Chaplin, G., Jablonski, N. G., Sussman, R. W., & Kelley, E. A. (2014). The role of piloerection in primate thermoregulation. Folia Primatologica, 85(1), 1–17. https://doi.org/10.1159/000355007.
Chen-Kraus, C. (2020). Assessing anthropogenic impacts on endangered Verreaux’s sifaka (Propithecus verreauxi) and prospects for human–lemur coexistence. PhD Dissertation. Yale University.
Chen-Kraus, C., Raharinoro, N. A., Randrianirinarisoa, M. A., Anderson, D. J., Lawler, R. R., Watts, D. P., & Richard, A. F. (2022). Human–lemur coexistence in a multiple-use landscape. Frontiers in Ecology and Evolution, 10, 1–12. https://doi.org/10.3389/fevo.2022.779861.
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
Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2004). Hibernation in a tropical primate. Nature, 429, 825–826.
Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2005). Hibernation in the tropics: Lessons from a primate. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 175(3), 147–155. https://doi.org/10.1007/s00360-004-0470-0.
Dollar, L., Ganzhorn, J. U., & Goodman, S. M. (2007). Primates and other prey in the seasonally variable diet of Cryptoprocta ferox in the dry deciduous forest of western Madagascar. In S. L. Gursky & K. A. I. Nekaris (Eds.), Primate anti-predator strategies (pp. 63–77). Springer Science+Business Media, LLC. https://doi.org/10.1007/978-0-387-34810-0.
Donati, G., Ricci, E., Baldi, N., Morelli, V., & Borgognini-Tarli, S. M. (2011). Behavioral thermoregulation in a gregarious lemur, Eulemur collaris: Effects of climatic and dietary-related factors. American Journal of Physical Anthropology, 144(3), 355–364. https://doi.org/10.1002/ajpa.21415.
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.
Fajardo, L. F. (1984). Pathological effects of hyperthermia in normal tissues. Cancer Research, 44, 4826s–4836s.
Fichtel, C., & Kappeler, P. M. (2011). Variation in the meaning of alarm calls in Verreaux’s and Coquerel’s sifakas (Propithecus verreauxi, P. coquereli). International Journal of Primatology, 32(2), 346–361. https://doi.org/10.1007/s10764-010-9472-9.
Fick, L. G., Kucio, T. A., Fuller, A., Matthee, A., & Mitchell, D. (2009). The relative roles of the parasol-like tail and burrow shuttling in thermoregulation of free-ranging cape ground squirrels, Xerus inauris. Comparative Biochemistry and Physiology — A Molecular and Integrative Physiology, 152(3), 334–340. https://doi.org/10.1016/j.cbpa.2008.11.004.
Fluke Process Instruments. (2022). Emissivity values for common materials. https://www.flukeprocessinstruments.com/en-us/service-and-support/knowledge-center/infrared-technology/emissivity-non-metals. Accessed 20 June 2022.
Hannah, L., Dave, R., Lowry, P. P., Andelman, S., Andrianarisata, M., Andriamaro, L., et al. (2008). Climate change adaptation for conservation in Madagascar. Biology Letters, 4(5), 590–594. https://doi.org/10.1098/rsbl.2008.0270
Ikeuchi, I., Mori, A., & Hasegawa, M. (2005). Natural history of Phelsuma madagascariensis kochi from a dry forest in Madagascar. Amphibia-Reptilia, 26, 475–483. https://doi.org/10.1163/156853805774806142.
IPCC (2014). In (Ed.), Climate change 2014 synthesis report. Contribution of working groups i, ii and iii to the fifth assessment report of the intergovernmental panel on climate change. Geneva, Switzerland: IPCC.
Jolly, A., Koyama, N., Rasamimanana, H., Crowley, H., & Williams, G. (2006). Berenty Reserve: A research site in southern Madagascar. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (pp. 32–42). Springer. https://doi.org/10.1007/978-0-387-34126-2
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.
LaFleur, M., Sauther, M., Cuozzo, F., Yamashita, N., Jacky Youssouf, I. A., & Bender, R. (2014). Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: Camera trap data and preliminary behavioral observations. Primates, 55(2), 207–217. https://doi.org/10.1007/s10329-013-0391-1.
Larsen, R. S., Moresco, A., Sauther, M. L., & Cuozzo, F. P. (2011). Field anesthesia of wild ring-tailed lemurs (Lemur catta) using tiletamine–zolazepam, medetomidine, and butorphanol. Journal of Zoo and Wildlife Medicine, 42(1), 75–87. https://doi.org/10.1638/2010-0144.1.
Le Maho, Y., Delclitte, P., & Chatonnet, J. (1976). Thermoregulation in fasting emperor penguins under natural conditions. American Journal of Physiology, 231(3), 913–922. https://doi.org/10.1152/ajplegacy.1976.231.3.913.
Lenhardt, R. (2010). The effect of anesthesia on body temperature control. Frontiers in Bioscience, 2(3), 1145–1154.
Licht, P., & Leitner, P. (1967). Behavioral responses to high temperatures in three species of California bats. Journal of Mammalogy, 48(1), 52–61.
Lopes, K. G. D., & 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.
López, K. R., Gibbs, P. H., & Reed, D. S. (2002). A comparison of body temperature changes due to the administration of ketamine-acepromazine and tiletamine-zolazepam anesthetics in cynomolgus macaques. Contemporary Topics in Laboratory Animal Science, 41(2), 47–50.
Loudon, J. E., & Sauther, M. L. (2013). Verreaux’s sifaka (Propithecus verreauxi) and ring-tailed lemur (Lemur catta) endoparasitism at the Bezà Mahafaly special reserve. Madagascar Conservation & Development, I(1), 21–28.
McCafferty, D. J. (2007). The value of infrared thermography for research on mammals: Previous applications and future directions. Mammal Review, 37(3), 207–223. https://doi.org/10.1111/j.1365-2907.2007.00111.x.
McCann, N. P., Moen, R. A., & Harris, T. R. (2013). Warm-season heat stress in moose (Alces alces). Canadian Journal of Zoology, 91(12), 893–898. https://doi.org/10.1139/cjz-2013-0175.
McFarland, R., Barrett, L., Fuller, A., Hetem, R. S., Maloney, S. K., Mitchell, D., & Henzi, S. P. (2019a). Keeping their cool: Behavioral thermoregulation and body temperature patterns of wild vervet monkeys. American Journal of Physical Anthropology, 171(3), 1–12. https://doi.org/10.1002/ajpa.23962.
McFarland, R., Henzi, P., & Barrett, L. (2019b). The social and thermal competence of wild vervet monkeys. In T. R. Turner, C. A. Schmitt, & J. D. Cramer (Eds.), Savanna monkeys: The genus Chlorocebus (pp. 199–207). Cambridge University Press. https://doi.org/10.1017/9781139019941.015.
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.
Nakagawa, S., & Schielzeth, H. (2013). A general and simple method for obtaining R2 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.
R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rasambainarivo, F. T., Junge, R. E., & Lewis, R. J. (2014). Biomedical evaluation of Verreaux’s sifaka (Propithecus verreauxi) from Kirindy Mitea National Park in Madagascar. Journal of Zoo and Wildlife Medicine, 45(2), 247–255. https://doi.org/10.1638/2013-0038R1.1.
Rasamimanana, N., Ratsirarson, J., Ramahatratra, E., Ranaivonasy, J., & Richard, A. (2016). Variabilité et changement du climat à Bezà Mahafaly. Malagasy Nature, 10, 5–14.
Schmidt-Nielsen, K. (1997). Animal physiology: Adaptation and environment (fifth edit.). Cambridge, UK: Cambridge University Press.
Sharma, H. S., & Hoopes, P. J. (2003). Hyperthermia induced pathophysiology of the central nervous system. International Journal of Hyperthermia, 19(3), 325–354. https://doi.org/10.1080/0265673021000054621.
Springer, A., Razafimanantsoa, L., Fichtel, C., & Kappeler, P. M. (2015). Comparison of three short-term immobilization regimes in wild Verreaux’s sifakas (Propithecus verreauxi): Ketamine–xylazine, ketamine–xylazine–atropine, and tiletamine–zolazepam. Journal of Zoo and Wildlife Medicine, 46(3), 482–490. https://doi.org/10.1638/2014-0154.1.
Tadross, M., Randriamarolaza, L., Rabefitia, Z., & Ki Yip, Z. (2008). Climate change in Madagascar; recent past and future. Washington, DC: World Bank
Tansey, E. A., & Johnson, C. D. (2015). Recent advances in thermoregulation. Advances in Physiology Education, 39(3), 139–148. https://doi.org/10.1152/advan.00126.2014.
Vieilledent, G., Grinand, C., Rakotomalala, F. A., Ranaivosoa, R., Rakotoarijaona, J. R., Allnutt, T. F., & Achard, F. (2018). Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Biological Conservation, 222, 189–197. https://doi.org/10.1016/j.biocon.2018.04.008.
Walter, E. J., & Carraretto, M. (2016). The neurological and cognitive consequences of hyperthermia. Critical Care, 20(199), 1–8. https://doi.org/10.1186/s13054-016-1376-4.
Acknowledgements
We thank the government of Madagascar and Madagascar National Parks for permitting our research on sifaka behavioral ecology (No.139/18/MEEF/SG/DGF/DSAP/SCB/Re), and the National Science Foundation (NSF-BSC-1745371), National Geographic Society (EC-420R-18), and Yale University MacMillan Center for facilitating our field research at Bezà Mahafaly. We are extremely grateful to our colleagues at École Supérieure des Sciences Agronomiques, Université d’Antananarivo and the Bezà Mahafaly monitoring team for helping to facilitate our research and for many thoughtful discussions. We thank the editor and two reviewers for comments that greatly improved this manuscript. We are also grateful to Dr. Richard McFarland, one of the reviewers, who kindly provided assistance with statistical analyses.
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Chen-Kraus, C., Raharinoro, N.A., Lawler, R.R. et al. Terrestrial Tree Hugging in a Primarily Arboreal Lemur (Propithecus verreauxi): a Cool Way to Deal with Heat?. Int J Primatol 44, 178–191 (2023). https://doi.org/10.1007/s10764-022-00328-5
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DOI: https://doi.org/10.1007/s10764-022-00328-5