Digestive physiology, metabolism and methane production of captive Linné's two-toed sloths (Choloepus didactylus)

Journal of Animal Physiology and Animal Nutrition

Volumn 100, Issue 3, 2016, Pages 552-564

  Vendl, C ^a   Frei, S ^a   Dittmann, M T ^a,b   Furrer, S ^c   Osmann, C ^d   Ortmann, S ^e   Munn, A ^f   Kreuzer, M ^b   Clauss, M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c Zoo Zurich   (Switzerland)

^d Zoo Dortmund   (Germany)

^e LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^f UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

Acetoclastic archaea; Digestibility; Enteric methanogenesis; Folivora; Foregut; Pilosa; Xenarthra

Indexed keywords

METHANE;

ANIMAL; BIOSYNTHESIS; DIGESTION; ENERGY METABOLISM; FEMALE; MALE; PHYSIOLOGY; SLOTH; ZOO ANIMAL;

ANIMALS; ANIMALS, ZOO; DIGESTION; ENERGY METABOLISM; FEMALE; MALE; METHANE; SLOTHS;

EID: 84933574391     PISSN: 09312439     EISSN: 14390396     Source Type: Journal    
DOI: 10.1111/jpn.12356     Document Type: Article

References (76)

1. Adam, P. J., 1999: Choloepus didactylus. Mammalian Species 621, 1-8.
2. Aguilar, R. F.; Superina, M., 2015: Xenarthra, In: R. E. Miller, M. E. Fowler (eds), Fowler's Zoo and Wild Animal Medicine. Elsevier Saunders, St. Louis, pp. 355-369.
3. Andersen, R.; Hjeljord, O.; Sæther, B. E., 1992: Moose defecation rates in relation to habitat quality. Alces 28, 95-100.
4. AOAC, 1995: Official Methods of Analysis of AOAC International. Association of Official Analytical Chemists, Arlington, VA.
5. Barnett, M. C.; McFarlane, J. R.; Hegarty, R. S., 2015: Low ambient temperature elevates plasma triiodothyronine concentrations while reducing digesta mean retention time and methane yield in sheep. Journal of Animal Physiology and Animal Nutrition 99, 483-491.
6. Blaxter, K. L.; Clapperton, J. L., 1965: Prediction of the amount of methane produced by ruminants. British Journal of Nutrition 19, 511-522.
7. Britton, S. W., 1941: Function and form in the sloth. Quarterly Review of Biology 16, 13-34, 190-207.
8. Bryant, M. P., 1979: Microbial methane production-theoretical aspects. Journal of Animal Science 48, 193-201.
9. Clauss, M.; Dierenfeld, E. S., 2008: The nutrition of browsers. In: M. E. Fowler, R. E. Miller (eds), Zoo and Wild Animal Medicine. Current Therapy 6. Saunders Elsevier, St. Louis, pp. 444-454.
10. Clauss, M.; Löhlein, W.; Kienzle, E.; Wiesner, H., 2003: Studies on feed digestibilities in captive Asian elephants (Elephas maximus). Journal of Animal Physiology and Animal Nutrition 87, 160-173.
11. Clauss, M.; Schwarm, A.; Ortmann, S.; Alber, D.; Flach, E. J.; Kühne, R.; Hummel, J.; Streich, W. J.; Hofer, H., 2004: Intake, ingesta retention, particle size distribution and digestibility in the hippopotamidae. Comparative Biochemistry and Physiology A 139, 449-459.
12. Clauss, M.; Hummel, J.; Streich, W. J.; Südekum, K.-H., 2008: Mammalian metabolic rate scaling to 2/3 or 3/4 depends on the presence of gut contents. Evolutionary Ecology Research 10, 153-154.
13. Clauss, M.; Lang-Deuerling, S.; Müller, D. W. H.; Kienzle, E.; Steuer, P.; Hummel, J., 2010: Retention of fluid and particles in captive tapirs (Tapirus spp.). Comparative Biochemistry and Physiology A 157, 95-101.
14. Dellow, D. W., 1982: Studies on the nutrition of macropodine marsupials. III. The flow of digesta through the stomach and intestine of macropodines and sheep. Australian Journal of Zoology 30, 399-406.
15. Delsuc, F.; Metcalf, J. L.; Wegener Parfrey, L.; Song, S. J.; Gonzales, A.; Knight, R., 2014: Convergence of gut microbiomes in myrmecophagous mammals. Molecular Ecology 23, 1301-1317.
16. Denis, C.; Jeuniaux, C.; Gerebtzoff, M. A.; Goffart, M., 1967: La digestion stomacale chez un paresseux: l'unau Choloepus hoffmanni Peters. Annales de la Societe Royale Zoologique de Belgique 97, 9-29.
17. Derno, M.; Jentsch, W.; Schweigel, M.; Kuhla, S.; Metges, C. C.; Matthes, H. D., 2005: Measurements of heat production for estimation of maintenance energy requirements of Hereford steers. Journal of Animal Science 83, 2590-2597.
18. Dittmann, M. T.; Hummel, J.; Runge, U.; Galeffi, C.; Kreuzer, M.; Clauss, M., 2014a: Characterising an artiodactyl family inhabiting arid habitats by its metabolism: low metabolism and maintenance requirements in camelids. Journal of Arid Environments 107, 41-48.
19. Dittmann, M. T.; Runge, U.; Lang, R. A.; Moser, D.; Galeffi, C.; Kreuzer, M.; Clauss, M., 2014b: Methane emission by camelids. PLoS ONE 9, e94363.
20. Eisenberg, J. F.; Maliniak, E., 1985: Maintenance and reproduction of two-toed sloth (Choloepus didactylus) in captivity. In: G. G. Montgomery (ed.), The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institution Press, Washington, pp. 327-331.
21. El Oufir, L.; Bruley des Varannes, S.; Barry, J. L.; Cloarec, D.; Bornet, F.; Galmiche, J. P., 1996: Relations between transit time, fermentation products, and hydrogen consuming flora in healthy humans. Gut 38, 870-877.
22. Foley, W. J.; von Engelhardt, W.; Charles-Dominique, P., 1995: The passage of digesta, particle size, and in vitro fermentation rate in the three-toed sloth Bradypus tridactylus (Edentata: Bradypodidae). Journal of Zoology 236, 681-696.
23. Franz, R.; Soliva, C. R.; Kreuzer, M.; Steuer, P.; Hummel, J.; Clauss, M., 2010: Methane production and body mass in ruminants and equids. Evolutionary Ecology Research 12, 727-738.
24. Franz, R.; Hummel, J.; Müller, D. W. H.; Bauert, M.; Hatt, J.-M.; Clauss, M., 2011a: Herbivorous reptiles and body mass: effects on food intake, digesta retention, digestibility and gut capacity, and a comparison with mammals. Comparative Biochemistry and Physiology A 158, 94-101.
25. Franz, R.; Soliva, C. R.; Kreuzer, M.; Hatt, J.-M.; Furrer, S.; Hummel, J.; Clauss, M., 2011b: Methane output of tortoises: its contribution to energy loss related to herbivore body mass. PLoS ONE 6, e17628.
26. Franz, R.; Soliva, C. R.; Kreuzer, M.; Hummel, J.; Clauss, M., 2011c: Methane in rabbits (Oryctolagus cuniculus) and guinea pigs (Cavia porcellus) on a hay-only diet: implications for the scaling of methane production with body mass in nonruminant mammalian herbivores. Comparative Biochemistry and Physiology A 158, 177-181.
27. Frei, S.; Ortmann, S.; Reutlinger, C.; Kreuzer, M.; Hatt, J.-M.; Clauss, M., 2015: Comparative digesta retention patterns in ratites. The Auk: Ornithological Advances 132, 119-131.
28. Goffart, M., 1971: Function and Form in the Sloth. Pergamon Press, Oxford.
29. Goopy, J. P.; Donaldson, A.; Hegarty, R. S.; Vercoe, P. E.; Haynes, F.; Barnett, M.; Oddy, V. H., 2014: Low-methane yield sheep have smaller rumens and shorter rumen retention time. British Journal of Nutrition 111, 578-585.
30. Hackstein, J. H. P.; van Alen, T. A., 1996: Fecal methanogens and vertebrate evolution. Evolution 50, 559-572.
31. Haenlein, G. F. W.; Smith, R. C.; Yoon, Y. M., 1966: Determination of the fecal excretion rate of horses with chromic oxide. Journal of Animal Science 25, 1091-1095.
32. Hammond, K. J.; Pacheco, D.; Burke, J. L.; Koolaard, J. P.; Muetzel, S.; Waghorn, G. C., 2014: The effects of fresh forages and feed intake level on digesta kinetics and enteric methane emissions from sheep. Animal Feed Science and Technology 193, 32-43.
33. Hatt, J.-M.; Clauss, M.; Gisler, R.; Liesegang, A.; Wanner, M., 2005: Fiber digestibility in juvenile captive Galapagos tortoises (Geochelone nigra) and implications for the development of captive animals. Zoo Biology 24, 185-191.
34. Hayssen, V., 2011: Choloepus hoffmanni (Pilosa: Megalonychidae). Mammalian Species 43, 37-55.
35. Holleman, D. F.; White, R. G., 1989: Determination of digesta fill and passage rate from non absorbed particulate phase markers using the single dosing method. Canadian Journal of Zoology 67, 488-494.
36. Hummel, J.; Hammer, S.; Hammer, C.; Ruf, J.; Lechenne, M.; Clauss, M., 2015: Solute and particle retention in a small grazing antelope, the blackbuck (Antilope cervicapra). Comparative Biochemistry and Physiology A 182, 22-26.
37. Irving, L.; Scholander, P. F.; Grinnel, S. W., 1942: Experimental studies of the respiration of sloths. Journal of Cellular and Comparative Physiology 20, 189-210.
38. Johnson, D. E.; Ward, G. M., 1996: Estimates of animal methane emissions. Environmental Monitoring and Assessment 42, 133-141.
39. Johnson, C. N.; Jarman, P. J.; Southwell, C. J., 1987: Macropod studies at Wallaby Creek. 5. Patterns of defecation by eastern gray kangaroos and red-necked wallabies. Wildlife Research 14, 133-138.
40. Lambert, J. E., 2002: Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglotydes). International Journal of Primatology 23, 1169-1185.
41. Langer, P. (ed), 1988: The Mammalian Herbivore Stomach. Gustav Fischer Verlag, Stuttgart/New York.
42. Lemaire, M.; Goffart, M.; Closon, J.; Winand, R., 1969: La fonction thyroidienne chez l'unau (Choloepus hoffmanny Peters). General and Comparative Endocrinology 12, 181-199.
43. Madsen, J.; Bertelsen, M. F., 2012: Methane production by red-necked wallabies (Macropus rufogriseus). Journal of Animal Science 90, 1364-1370.
44. Matsuda, I.; Sha, J. C. M.; Ortmann, S.; Schwarm, A.; Grandl, F.; Caton, J.; Jens, W.; Kreuzer, M.; Marlena, D.; Hagen, K. B.; Clauss, M., 2015: Excretion patterns of solute and different-sized particle passage markers in foregut-fermenting proboscis monkey (Nasalis larvatus) do not indicate an adaptation for rumination. Physiology and Behavior 149, 45-52.
45. McNab, B. K., 1978: Energetics of arboreal folivores: physiological problems and ecological consequences of feeding on ubiquitous food supply. In: G. G. Montgomery (ed.), The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, pp. 153-162.
46. McNab, B. K., 2008: An analysis of the factors that influence the level and scaling of mammalian BMR. Comparative Biochemistry and Physiology A 151, 5-28.
47. Merrit, D. A., 1985: The two-toed sloth, Choloepus hoffmanni Peters. In: G. G. Montgomery (ed.), The Evolution and Ecology of Armadillos, Sloths and Vermilinguas. Smithsonian Institution Press, Washington and London, pp. 333-341.
48. Miller, T. L.; Wolin, M. J., 1986: Methanogens human and animal intestinal tracts. Systematic and Applied Microbiology 7, 223-229.
49. Mitchell, B.; Rowe, J. J.; Ratcliffe, P.; Hinge, M., 1985: Defecation frequency in roe deer (Capreolus capreolus) in relation to the accumulation rates of faecal deposits. Journal of Zoology 207, 1-7.
50. Montgomery, G. G.; Sunquist, M. E., 1975: Impact of sloths on neotropical energy flow and nutrient cycling. In: F. B. Golley, E. Medina (eds), Tropical Ecological Systems: Trends in Terrestrial and Aquatic Research. Springer-Verlag, New York, pp. 69-98.
51. Montgomery, G. G.; Sunquist, M. E., 1978: Habitat selection and use by two-toed and three-toed sloths. In: G. G. Montgomery (ed.), The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, pp. 329-359.
52. Müller, D. W. H.; Caton, J.; Codron, D.; Schwarm, A.; Lentle, R.; Streich, W. J.; Hummel, J.; Clauss, M., 2011: Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores. Comparative Biochemistry and Physiology A 160, 207-220.
53. Müller, D. W. H.; Codron, D.; Meloro, C.; Munn, A.; Schwarm, A.; Hummel, J.; Clauss, M., 2013: Assessing the Jarman-Bell Principle: scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comparative Biochemistry and Physiology A 164, 129-140.
54. Nagy, K. A.; Montgomery, G. G., 1980: Field metabolic rate, water flux and food consumption in three-toed sloths (Bradypus variegatus). Journal of Mammalogy 61, 465-472.
55. Nijboer, J.; Clauss, M., 2006: The Digestive Physiology of Colobine Primates. Fibre intake and faeces quality in leaf-eating monkeys. University of Utrecht, The Netherlands, pp. 9-28.
56. Okine, E. K.; Mathison, G. W.; Hardin, R. T., 1989: Effects of changes in frequency of reticular contractions on fluid and particulate passage rates in cattle. Journal of Animal Science 67, 3388-3396.
57. Oliveira, L. H. A.; Da Costa, C. P.; Huggins, S. E., 1980: Cardiac mass, blood temperature and ventricular fibrillation: a study of the comparative physiology of the three-toed sloth and the domestic cat. Comparative Biochemistry and Physiology A 67, 483-490.
58. Ozorio de Almeida, M.; Branco de Fialho, A., 1924: Métabolisme, température et quelques autres déterminations physiologiques faites sur le paresseux (Bradypus tridactylus). Comptes Rendus des Seances de la Societe de Biologie et de Ses Filiales 91, 1124-1125.
59. Pauli, J. N.; Mendoza, J. E.; Steffan, S. A.; Carey, C. C.; Weimer, P. J.; Peery, M. Z., 2014: A syndrome of mutualism reinforces the lifestyle of a sloth. Proceedings of the Royal Society B 281, 20133006.
60. Raines, J., 2005: Captive health and husbandry of the Bradypodidae. Zoo Biology 24, 557-568.
61. Rattenborg, N. C.; Voirin, B.; Vyssotski, A. L.; Kays, R. W.; Spoelstra, K.; Kuemmeth, F.; Heidrich, W.; Wikelski, M., 2008: Sleeping outside the box: electroencephalographic measures of sleep in sloths inhabiting a rainforest. Biology Letters 4, 402-405.
62. Robbins, C. T., 1993: Wildlife Feeding and Nutrition. Academic Press, San Diego.
63. Schwarm, A.; Ortmann, S.; Wolf, C.; Streich, W. J.; Clauss, M., 2009: Passage marker excretion in red kangaroo (Macropus rufus), collared peccary (Pecari tajacu) and colobine monkeys (Colobus angolensis, C. polykomos, Trachypithecus johnii). Journal of Experimental Zoology A 311, 647-661.
64. Schwarm, A.; Ortmann, S.; Fritz, J.; Rietschel, W.; Flach, E. J.; Clauss, M., 2013: No distinct stratification of ingesta particles and no distinct moisture gradient in the forestomach of nonruminants: the wallaby, peccary, hippopotamus, and sloth. Mammalian Biology 78, 412-421.
65. Silva, M.; Downing, J. A., 1995: CRC Handbook of Mammalian Body Masses. CRC Press, Bota Racon.
66. Stahl, M.; Osmann, C.; Ortmann, S.; Kreuzer, M.; Hatt, J.-M.; Clauss, M., 2012: Energy intake for maintenance in a mammal with a low basal metabolism, the Giant anteater (Myrmecophaga tridactyla). Journal of Animal Physiology and Animal Nutrition 96, 818-824.
67. de Stefani Munaó Diniz, L.; Oliveira, P. M., 1999: Clinical problems of sloths (Bradypus sp. and Choloepus sp.) in captivity. Journal of Zoo and Wildlife Medicine 30, 76-80.
68. Stevens, C. E.; Hume, I. D., 1998: Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiological Reviews 78, 393-427.
69. Thauer, R. K.; Kaster, A. K.; Seedorf, H.; Buckel, W.; Hedderich, R., 2008: Methanogenic archaea: ecologically relevant differences in energy conservation. Nature Reviews Microbiology 6, 579-591.
70. Thielemans, M. F.; Francois, E.; Bodart, C.; Thewis, A., 1978: Mesure du transit gastrointestinal chez le porc a l'aide des radiolanthanides. Comparaison avec le mouton. Annales De Biologie Animale, Biochimie, Biophysique 18, 237-247.
71. Udén, P.; Colucci, P. E.; Van Soest, P. J., 1980: Investigation of chromium, cerium and cobalt as markers in digesta. Rate of passage studies. Journal of the Science of Food and Agriculture 31, 625-632.
72. Van Soest, P. J., 1994: Nutritional Ecology of the Ruminant, 2nd edn. Cornell University Press, Ithaca.
73. Vaughan, C.; Ramírez, O.; Herrera, G.; Guries, R., 2007: Spatial ecology and conservation of two sloth species in a cacao landscape in Limón, Costa Rica. Biodiversity and Conservation 16, 2293-2310.
74. Vogel, I.; Vié, J. C.; de Thoisy, B.; Moreau, B., 1999: Hematological and serum chemistry profiles of free-ranging southern two-toed sloths in French Guiana. Journal of Wildlife Diseases 35, 531-535.
75. 2/3. Proceedings of the National Academy of Sciences of the United States of America 100, 4046-4049.
76. Wing, L. D.; Buss, I. O., 1970: Elephants and forests. Wildlife Monographs 19, 3-92.