Thermal and morphometric correlates of the extremely low rate of energy use in a wild frugivorous primate, the Mayotte lemur.
Body composition
Doubly labeled water
Fattening
Field metabolic rate
Heat stress
Seasonality
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
17 Sep 2024
17 Sep 2024
Historique:
received:
11
04
2024
accepted:
04
09
2024
medline:
18
9
2024
pubmed:
18
9
2024
entrez:
17
9
2024
Statut:
epublish
Résumé
Primates spend on average half as much energy as other placental mammals while expressing a wide range of lifestyles. However, little is known about how primates adapt their rate of energy use in the context of natural environmental variations. Using doubly labelled water, behavioral and accelerometric methods, we measured the total energy expenditure (TEE) and body composition of a population of Eulemur fulvus (N = 12) living in an agroforest in Mayotte. We show that the TEE of this medium-sized cathemeral primate is one of the lowest recorded to date in eutherians. Regression models show that individual variation in the rate of energy use is predicted by fat-free mass, body size, thigh thickness and maximum temperature. TEE is positively correlated with increasing temperature, suggesting that thermoregulation is an important component of the energy budget of this frugivorous species. Mass-specific TEE is only 10% lower than that of a closely related species previously studied in a gallery forest, consistent with the assertion that TEE varies within narrow physiological limits. As lemur communities include many species with unique thermoregulatory adaptations, circadian and/or seasonal temperature variations may have constituted a major selective pressure on the evolution of lemur metabolic strategies.
Identifiants
pubmed: 39289438
doi: 10.1038/s41598-024-72189-2
pii: 10.1038/s41598-024-72189-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
21700Informations de copyright
© 2024. The Author(s).
Références
van Schaik, C. P. & Isler, K. Life-history evolution. In The Evolution of Primate Societies (Mitani, J. et al. eds.). 220–244 (Chicago University Press, 2012).
Martin, R. D. & MacLarnon, A. M. Gestation period, neonatal size and maternal investment in placental mammals. Nature 313, 220–223 (1985).
doi: 10.1038/313220a0
Read, A. F. & Harvey, P. H. Life history differences among the eutherian radiations. J. Zool. 219, 329–353 (1989).
doi: 10.1111/j.1469-7998.1989.tb02584.x
Canale, C. I. & Henry, P. Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim. Res. 43, 135–147 (2010).
doi: 10.3354/cr00897
Visser, M. E. Keeping up with a warming world: Assessing the rate of adaptation to climate change. Proc. R. Soc. B. 275, 649–659 (2008).
pubmed: 18211875
pmcid: 2409451
doi: 10.1098/rspb.2007.0997
Gogarten, J. F. et al. Seasonal mortality patterns in non-human primates: Implications for variation in selection pressures across environments. Evolution 66, 3252–3266 (2012).
pubmed: 23025613
pmcid: 3955579
doi: 10.1111/j.1558-5646.2012.01668.x
Janson, C. H. & van Schaik, C. P. Ecological risk aversion in juvenile primates: Slow and steady wins the race. In Juvenile Primates: Life History, Development, and Behavior (Pereira, M. E. & Fairbanks, L. A. eds.). 57–76 (Oxford University Press, 1993).
Hladik, C. M. Diet and the evolution of feeding strategies among forest primates. In Omnivorous Primates. Gathering and Hunting in Human Evolution (Harding, R. S. O & Teleki, G. eds.). 215–254 (Columbia University Press, 1981).
Oates, J. F. Food distribution and foraging behavior. In Primate Societies (Smuts, B. B., Cheney D. L., Seyfarth, R. M. & Wrangham, R. W. eds.). 197–209 https://doi.org/10.7208/9780226220468-019 (University of Chicago Press, 1986).
Nagy, K. A., Girard, I. A. & Brown, T. K. Energetics of free-ranging mammals, reptiles, and birds. Ann. Rev. Nutr. 19, 247–277 (1999).
doi: 10.1146/annurev.nutr.19.1.247
Pontzer, H. Energy expenditure in humans and other primates: A new synthesis. Annu. Rev. Anthropol. 44, 169–187 (2015).
doi: 10.1146/annurev-anthro-102214-013925
Charnov, E. L. & Berrigan, D. Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evol. Anthropol. 1, 191–194 (1993).
doi: 10.1002/evan.1360010604
Jones, J. H. Primates and the evolution of long, slow life histories. Curr. Biol. 21, R708–R717 (2011).
pubmed: 21959161
pmcid: 3192902
doi: 10.1016/j.cub.2011.08.025
Kappeler, P. M. Causes and consequences of life-history variation among strepsirhine primates. Am. Nat. 148, 868–891 (1996).
doi: 10.1086/285960
Harvey, P. H. & Clutton-Brock, T. H. Primate home-range size and metabolic needs. Behav. Ecol. Sociobiol. 8, 151–155 (1981).
doi: 10.1007/BF00300828
Sibly, R. M. & Brown, J. H. Effects of body size and lifestyle on evolution of mammal life histories. Proc. Natl. Acad. Sci. USA 104, 17707–17712 (2007).
pubmed: 17940028
pmcid: 2077039
doi: 10.1073/pnas.0707725104
Speakman, J. R. Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717–1730 (2005).
pubmed: 15855403
doi: 10.1242/jeb.01556
Simmen, B., Morino, L., Blanc, S. & Garcia, C. The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates. Sci. Rep. 11, 14196. https://doi.org/10.1038/s41598-021-93764-x (2021).
pubmed: 34244546
pmcid: 8270931
Pontzer, H. et al. Primate energetics and life history. Proc. Natl. Acad. Sci. USA 111, 1433–1437 (2014).
pubmed: 24474770
pmcid: 3910615
doi: 10.1073/pnas.1316940111
Simmen, B. et al. Total energy expenditure and body composition in two free-living sympatric lemurs. PLoS One 5, e9860. https://doi.org/10.1371/journal.pone.0009860 (2010).
pubmed: 20360848
pmcid: 2845615
Pontzer, H. et al. Constrained total energy expenditure and metabolic adaptation to physical activity in adult humans. Curr. Biol. 26, 410–417 (2016).
pubmed: 26832439
pmcid: 4803033
doi: 10.1016/j.cub.2015.12.046
Pontzer, H., Raichlen, D. A., Shumaker, R. W., Ocobock, C. & Wich, S. A. Metabolic adaptation for low energy throughput in orangutans. Proc. Natl. Acad. Sci. USA 107, 14048–14052 (2010).
pubmed: 20679208
pmcid: 2922585
doi: 10.1073/pnas.1001031107
Pontzer, H., Raichlen, D. A. & Sockol, M. D. From treadmill to tropics: Calculating ranging cost in chimpanzees. In Primate Locomotion: Linking Field and Laboratory Research, Developments in Primatology: Progress and Prospects (D’Août, K. & Vereecke, E. E. eds.). 289–309 (Springer, 2011).
Schmid, J. & Speakman, J. R. Daily energy expenditure of the grey mouse lemur (Microcebus murinus): A small primate that uses torpor. J. Comp. Physiol. B 170, 633–641 (2000).
pubmed: 11192269
doi: 10.1007/s003600000146
Schmid, J. & Speakman, J. R. Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): A comparison of dry and wet forests. Naturwiss. 96, 609–620 (2009).
pubmed: 19229507
doi: 10.1007/s00114-009-0515-z
Wright, P. C. Lemur traits and Madagascar ecology: Coping with an island environment. Yearb. Phys. Anthropol. 42, 31–72 (1999).
doi: 10.1002/(SICI)1096-8644(1999)110:29+<31::AID-AJPA3>3.0.CO;2-0
Dewar, R. E. & Richard, A. F. Evolution in the hypervariable environment of Madagascar. Proc. Natl. Acad. Sci. USA 104, 13723–13727 (2007).
pubmed: 17698810
pmcid: 1947998
doi: 10.1073/pnas.0704346104
Bourlière, F., Petter, J. J. & Petter-Rousseaux, A. Variabilité de la température centrale chez les lémuriens. Mém. Inst. Sci. Madagascar Sér. A Tome X, 303–304 (1956).
Chevillard, M. C. Capacités Thermorégulatrices d’un Lémurien Malgache, Microcebus murinus (Ph.D. Thesis, University Paris VII, 1976).
Blanco, M. B., Dausmann, K. H., Ranaivoarisoa, J. F. V. & Yoder, A. D. Underground hibernation in a primate. Sci. Rep. 3, 1768 (2013).
pubmed: 23636180
pmcid: 3641607
doi: 10.1038/srep01768
Lewis, R. J. & Kappeler, P. M. Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi. Am. J. Primatol. 66, 1–18 (2005).
Walker, M. L., Schwartz, S. M., Wilson, M. E. & Musey, P. I. Estimation of body fat in female rhesus monkeys. Am. J. Phys. Anthrop. 63, 323–329 (1984).
pubmed: 6731604
doi: 10.1002/ajpa.1330630309
Pastorini, J., Forstner, M. R. J. & Martin, R. D. Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 16, 418–429 (2000).
pubmed: 10991794
doi: 10.1006/mpev.2000.0796
Tarnaud, L. Eulemur fulvus (Schlegel, 1866), Maki brun. In Atlas des Mammifères Sauvages de France. Vol. 3. Carnivores et Primates (Savouré-Soubelet, A. et al. eds.). 336–341 (Museum National d’Histoire Naturelle, 2024).
Kappeler, P. M. & Erkert, H. G. On the move around the clock: Correlates and determinants of cathemeral activity in wild redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 54, 359–369 (2003).
doi: 10.1007/s00265-003-0652-x
Curtis, D., Zaramody, A. & Martin, R. D. Cathemerality in the mongoose lemur, Eulemur mongoz. Am. J. Primatol. 47, 279–298 (1999).
pubmed: 10206207
doi: 10.1002/(SICI)1098-2345(1999)47:4<279::AID-AJP2>3.0.CO;2-U
Pereira, M. & Pond, C. Organization of white adipose tissue in lemuridae. Am. J. Primatol. 35, 1–13 (1995).
pubmed: 31924060
doi: 10.1002/ajp.1350350102
Hamada, Y., Hayakawa, S., Suzuki, J., Watanabe, K. & Ohkura, S. Seasonal variation in the body fat of Japanese macaques Macaca fuscata. Mammal Study 28, 79–88 (2003).
doi: 10.3106/mammalstudy.28.79
Bowman, J. E. & Lee, P. C. Growth and threshold weaning weights among captive rhesus macaques. Am. J. Phys. Anthropol. 96, 159–175 (1995).
pubmed: 7755106
doi: 10.1002/ajpa.1330960205
Schoeller, D. A. et al. Energy expenditure by the doubly labeled water: Validation in humans and proposed calculations. Am. J. Physiol. 250, R823–R830 (1986).
pubmed: 3085521
Speakman, J. R. Doubly Labelled Water: Theory and Practice (Chapman, Hall, 1997).
Speakman, J. R. et al. A standard calculation methodology for human doubly labeled water studies. Cell Rep. Med. 16, 100203. https://doi.org/10.1016/j.xcrm.2021.100203 (2021).
Altmann, J. Observational study of behaviour—Sampling methods. Behavior 49, 227–267 (1974).
doi: 10.1163/156853974X00534
Simmen, B., Hladik, A. & Ramasiarisoa, P. L. Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, Southern Madagascar. Int. J. Primatol. 24, 949–968 (2003).
doi: 10.1023/A:1026366309980
Pinkus, S., Smith, J. N. M. & Jolly, A. Feeding competition between introduced Eulemur fulvus and native Lemur catta during the birth season at Berenty reserve, Southern Madagascar. In Ringtailed Lemur Biology: Lemur catta in Madagascar (Jolly, A., Sussman, R. W., Koyama, N. & Rasamimanana, H. eds.). 119–140 (Springer, 2006).
Tarnaud, L. Ontogeny of feeding behavior of Eulemur fulvus in the dry forest of Mayotte. Int. J. Primatol. 25, 803–823 (2004).
doi: 10.1023/B:IJOP.0000029123.78167.63
James, G., Witten, D., Hastie, T. & Tibshirani, R. (eds.). An Introduction to Statistical Learning: with Applications in R (Springer, 2013).
Kherad-Pajouh, S. & Renaud, O. A general permutation approach for analyzing repeated measures ANOVA and mixed-model designs. Stat. Pap. 56, 947–967 (2015).
doi: 10.1007/s00362-014-0617-3
RStudio Team. RStudio: Integrated Development Environment for R. http://www.rstudio.com/ . (RStudio, PBC, 2020).
R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/ (R Foundation for Statistical Computing, 2022).
Lê, S., Josse, J. & Husson, F. FactoMineR: An R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).
doi: 10.18637/jss.v025.i01
Fox, J. The R Commander: A basic statistics graphical user interface to R. J. Stat. Softw. 14, 1–42. https://www.jstatsoft.org/article/view/v014i09 (2005)
Fox, J., Marquez, M. M. & Bouchet-Valat, M. Rcmdr: R Commander. R package version 2.9-2. https://socialsciences.mcmaster.ca/jfox/Misc/Rcmdr/ (2024).
Fox, J. & Weisberg, S. An R Companion to Applied Regression. 3rd Ed. https://socialsciences.mcmaster.ca/jfox/Books/Companion/ (Sage, 2019).
Fox, J. & Weisberg, S. Visualizing fit and lack of fit in complex regression models with predictor effect plots and partial residuals. J. Stat. Softw. 87, 1–27. https://doi.org/10.18637/jss.v087.i09 (2018).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26. https://doi.org/10.18637/jss.v082.i13 (2017).
Frossard, J. & Renaud, O. Permutation tests for regression, ANOVA, and comparison of signals: The permuco package. J. Stat. Softw. 99, 1–32. https://doi.org/10.18637/jss.v099.i15 (2021).
Simmen, B., Darlu, P., Hladik, C. M. & Pasquet, P. Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans. Physiol. Behav. 138, 193–199 (2015).
pubmed: 25447337
doi: 10.1016/j.physbeh.2014.10.018
Tattersall, I. Patterns of activity in the Mayotte lemur, Lemur fulvus mayottensis. J. Mammal. 60, 314–323 (1979).
doi: 10.2307/1379802
Sato, H. Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: Implications for seasonal thermoregulation. Primates 53, 255–263 (2012).
pubmed: 22388421
doi: 10.1007/s10329-012-0301-y
Tanaka, M. Habitat use and social structure of a brown lemur hybrid population in the Berenty Reserve, Madagascar. Am. J. Primatol. 69, 1189–1194 (2007).
pubmed: 17294429
doi: 10.1002/ajp.20416
Sussman, R. W. Ecological distinctions in sympatric species of Lemur. In Prosimian Biology (Martin, R. D., Doyle, G. A. & Walker, A. C. eds.). 75–108 (Duckworth, 1974).
Tarnaud, L. Feeding behavior of lactating brown lemur females (Eulemur fulvus) in Mayotte: Influence of infant age and plant phenology. Am. J. Primatol. 68, 966–977 (2006).
pubmed: 16900506
doi: 10.1002/ajp.20288
Tattersall, I. Ecology and behavior of Lemur fulvus mayottensis, primate lémuriformes. Anthrop. Pap. Am. Mus. Nat. Hist. N. Y. 54, 425–482 (1977).
Rimbach, R. & Pontzer, H. Increased physical activity is not related to markers of cardiometabolic health in two lemur species. Am. J. Primatol. https://doi.org/10.1002/ajp.23564 (2024).
pubmed: 37839049
Nie, Y. et al. Exceptionally low daily energy expenditure in the bamboo-eating giant panda. Science 349, 171–174 (2015).
pubmed: 26160943
doi: 10.1126/science.aab2413
Speakman, J. R. & Król, E. Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726–746 (2010).
pubmed: 20443992
doi: 10.1111/j.1365-2656.2010.01689.x
Daniels, H. L. Oxygen consumption in Lemur fulvus: deviation from the ideal model. J. Mammal. 65, 584–592 (1984).
doi: 10.2307/1380841
Briscoe, N. J. et al. Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals. Biol. Lett. 10, 20140235. https://doi.org/10.1098/rsbl.2014.0235 (2014).
pubmed: 24899683
pmcid: 4090547
Chen-Kraus, C., Raharinoro, N. A., Lawler, R. R. & Richard, A. Terrestrial tree hugging in a primarily arboreal lemur (Propithecus verreauxi): A cool way to deal with heat?. Int. J. Primatol. 44, 178–191. https://doi.org/10.1007/s10764-022-00328-5 (2023).
Cliffe, R. N. et al. The metabolic response of the Bradypus sloth to temperature. PeerJ https://doi.org/10.7717/peerj.5600 (2018).
pubmed: 30258712
pmcid: 6151113
Hoegh-Guldberg, O. et al. Impacts of 1.5 ºC global warming on natural and human systems. Global Warming of 1.5 °C. In An IPCC Special Report on the Impacts of Global Warming of 1.5 °C Above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty (Masson-Delmotte, V. et al. eds.). 175–312 https://doi.org/10.1017/9781009157940.005 (Cambridge University Press, 2018).