Arboreal Folivores Limit Their Energetic Output, All the Way to Slothfulness

By exploiting unutilized resources, organisms expand into novel niches, which can lead to adaptive radiation. However, some groups fail to diversify despite the apparent opportunity to do so. Although arising multiple times, arboreal folivores are rare and have not radiated, presumably because of energetic constraints. To explore this hypothesis, we quantified the field metabolic rate (FMR), movement, and body temperature for syntopic two- and three-toed sloths, extreme arboreal folivores that differ in their degree of specialization. Both species expended little energy, but three-toed sloths (162 kJ/day*kg0.734) possessed the lowest FMR recorded for any mammal. Three-toed sloths were more heterothermic and moved less than two-toed sloths. We then compared FMRs and basal metabolic rates (BMRs) for 19 species of arboreal folivores along a spectrum of specialization. Overall, arboreal folivores had lower BMRs and FMRs than other mammals, and increasing specialization led to lower FMRs but not BMRs. Thus, reduced energetic expenditure in specialized species was the result of thermoregulatory and behavioral strategies, rather than simply a proportionate reduction in BMR. Altogether, our findings support the concept that arboreal folivores are tightly constrained by nutritional energetics and help to explain the lack of radiation among species exploiting a lifestyle in the trees.

[1]  B. Green,et al.  Energy allocation for reproduction in a marsupial arboreal folivore, the common ringtail possum (Pseudocheirus peregrinus) , 2004, Oecologia.

[2]  J. Diniz‐Filho,et al.  Phylogenetic analyses: comparing species to infer adaptations and physiological mechanisms. , 2012, Comprehensive Physiology.

[3]  K. Nagy,et al.  Energetics of free-ranging mammals, reptiles, and birds. , 1999, Annual review of nutrition.

[4]  J. Ganzhorn,et al.  Resting metabolic rates of Lepilemur ruficaudatus , 1996, American journal of primatology.

[5]  K. Nagy,et al.  Field Metabolic Rate, Water Flux, and Food Consumption in Three-Toed Sloths (Bradypus variegatus) , 1980 .

[6]  Campbell O. Webb,et al.  Bioinformatics Applications Note Phylocom: Software for the Analysis of Phylogenetic Community Structure and Trait Evolution , 2022 .

[7]  B. Grant,et al.  How and Why Species Multiply: The Radiation of Darwin's Finches , 2011 .

[8]  Alan Y. Chiang,et al.  Generalized Additive Models: An Introduction With R , 2007, Technometrics.

[9]  J. Pauli,et al.  Shade‐grown cacao supports a self‐sustaining population of two‐toed but not three‐toed sloths , 2014 .

[10]  Jonathan N Pauli,et al.  A syndrome of mutualism reinforces the lifestyle of a sloth , 2014, Proceedings of the Royal Society B: Biological Sciences.

[11]  A. Richard,et al.  Female social dominance and basal metabolism in a malagasy primate, Propithecus verreauxi , 1987, American journal of primatology.

[12]  G. Turner The Ecology of Adaptive Radiation , 2001, Heredity.

[13]  Masami Hasegawa,et al.  Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny , 2012, Proceedings of the Royal Society B: Biological Sciences.

[14]  Natalie J Briscoe,et al.  Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals , 2014, Biology Letters.

[15]  F. Delsuc,et al.  Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans , 2004, BMC Evolutionary Biology.

[16]  P. Charles-Dominique,et al.  The passage of digesta, particle size, and in vitro fermentation rate in the three‐toed sloth Bradypus tridactylus (Edentata: Bradypodidae) , 1995 .

[17]  W. Godsoe,et al.  Ecological opportunity and the origin of adaptive radiations , 2010, Journal of evolutionary biology.

[18]  K. Nagy,et al.  ENERGY METABOLISM AND FOOD CONSUMPTION BY WILD HOWLER MONKEYS (ALOUATTA PALLIATA) , 1979 .

[19]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[20]  T. Dawson,et al.  Metabolism and heat balance in an arboreal marsupial, the koala (Phascolarctos cinereus) , 1979, Journal of comparative physiology.

[21]  James H. Brown,et al.  Effects of Size and Temperature on Metabolic Rate , 2001, Science.

[22]  Ari Löytynoja,et al.  webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser , 2010, BMC Bioinformatics.

[23]  Jonathan B. Losos,et al.  Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles , 2009 .

[24]  T. Garland Scaling the Ecological Cost of Transport to Body Mass in Terrestrial Mammals , 1983, The American Naturalist.

[25]  Roger G. Linington,et al.  Sloth Hair as a Novel Source of Fungi with Potent Anti-Parasitic, Anti-Cancer and Anti-Bacterial Bioactivity , 2014, PloS one.

[26]  F. Geiser,et al.  Metabolic rate and body temperature reduction during hibernation and daily torpor. , 2004, Annual review of physiology.

[27]  S. O’Brien,et al.  A Molecular Phylogeny of Living Primates , 2011, PLoS genetics.

[28]  M. Holton,et al.  Mitigating the squash effect: sloths breathe easily upside down , 2014, Biology Letters.

[29]  G. Dasilva The western black-and-white colobus as a low-energy strategist : activity budgets, energy expenditure and energy intake , 1992 .

[30]  Ole Seehausen,et al.  African cichlid fish: a model system in adaptive radiation research , 2006, Proceedings of the Royal Society B: Biological Sciences.

[31]  J. Speakman,et al.  Exceptionally low daily energy expenditure in the bamboo-eating giant panda , 2015, Science.

[32]  A. du Plessis,et al.  Thermoregulatory patterns of two sympatric rodents: Otomys unisulcatus and Parotomys brantsii. , 1989, Comparative biochemistry and physiology. A, Comparative physiology.

[33]  J. Pauli,et al.  Resource use by the two-toed sloth (Choloepus hoffmanni) and the three-toed sloth (Bradypus variegatus) differs in a shade-grown agro-ecosystem , 2014, Journal of Tropical Ecology.

[34]  G. Grigg,et al.  The Evolution of Endothermy and Its Diversity in Mammals and Birds , 2004, Physiological and Biochemical Zoology.

[35]  S. Guindon,et al.  A Simple, Fast, and Accurate Method to Estimate Large Phylogenies by Maximum Likelihood , 2017 .

[36]  N. Ramankutty,et al.  Estimating historical changes in global land cover: Croplands from 1700 to 1992 , 1999 .

[37]  James O. McInerney,et al.  Clann: investigating phylogenetic information through supertree analyses , 2005, Bioinform..

[38]  Robert R. Harris,et al.  Doubly-Labelled Water – Theory and Practice , 2001 .

[39]  A. Kinnear,et al.  Metabolism and temperature regulation in marsupials. , 1975, Comparative biochemistry and physiology. A, Comparative physiology.

[40]  G. Maloiy,et al.  A comparative study of basal metabolism and thermoregulation in a folivorous (Colobus guereza) and an omnivorous (Cercopithecus mitis) primate species. , 1983, Comparative biochemistry and physiology. A, Comparative physiology.

[41]  K. Nagy,et al.  Energy and Water Metabolism in Free-living Greater Gliders, Petauroides volans , 1990 .

[42]  B. McNab Energy Conservation in a Tree-Kangaroo (Dendrolagus matschiei) and the Red Panda (Ailurus fulgens) , 1988, Physiological Zoology.

[43]  Robin Huw Crompton,et al.  Diet, Body Size and the Energy Costs of Locomotion in Saltatory Primates , 1998, Folia Primatologica.

[44]  D. Schoeller,et al.  Doubly labeled water analysis using cavity ring-down spectroscopy. , 2011, Rapid communications in mass spectrometry : RCM.

[45]  H. Pontzer,et al.  Metabolic adaptation for low energy throughput in orangutans , 2010, Proceedings of the National Academy of Sciences.

[46]  J. Pauli,et al.  Unexpected Strong Polygyny in the Brown-Throated Three-Toed Sloth , 2012, PloS one.

[47]  W. Karasov,et al.  Daily Energy Expenditure and the Cost of Activity in Mammals , 1992 .

[48]  W. Foley Digestion and energy metabolism in a small arboreal marsupial, the Greater Glider (Petauroides volans), fed high-terpeneEucalyptus foliage , 1987, Journal of Comparative Physiology B.

[49]  I. Boyd,et al.  Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods , 2004 .

[50]  T. Casey,et al.  The Basal Metabolism of Mantled Howler Monkeys (Alouatta palliata) , 1979 .

[51]  S. Farley,et al.  Seasonal body composition, water turnover, and field metabolic rates in porcupines (Erethizon dorsatum) in Alaska , 2011 .

[52]  Judith M Burkart,et al.  Primate energy expenditure and life history , 2014, Proceedings of the National Academy of Sciences.

[53]  K. Nagy Field metabolic rate and body size , 2005, Journal of Experimental Biology.

[54]  C. R. White,et al.  Mammalian basal metabolic rate is proportional to body mass2/3 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  T. Dawson,et al.  Standard metabolism, body temperature, and surface areas of Australian marsupials. , 1970, The American journal of physiology.

[56]  B. McNab The comparative energetics of rigid endothermy: the Arvicolidae , 1992 .

[57]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[58]  B. McNab The Comparative Energetics of New Guinean Cuscuses (Metatheria: Phalangeridae) , 2008 .

[59]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[60]  Thomas J Naughton,et al.  Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified , 2006, BMC Evolutionary Biology.

[61]  T. J. Robinson,et al.  Impacts of the Cretaceous Terrestrial Revolution and KPg Extinction on Mammal Diversification , 2011, Science.

[62]  Ming Li,et al.  Seasonal energy utilization in bamboo by the red panda (Ailurus fulgens) , 2000 .

[63]  K. Nagy,et al.  Field Metabolic Rate, Water Flux, Food Consumption and Time Budget of Koalas, Phascolarctos Cinereus (Marsupialia: Phascolarctidae) in Victoria. , 1985 .

[64]  A. Gentry,et al.  Tropical Forest Structure and the Distribution of Gliding and Prehensile-Tailed Vertebrates , 1983, The American Naturalist.