Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-24T12:28:10.520Z Has data issue: false hasContentIssue false

Evolutionary adaptations of ruminants and their potential relevance for modern production systems

Published online by Cambridge University Press:  09 March 2010

M. Clauss*
Affiliation:
University of Zurich, Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, Switzerland
I. D. Hume
Affiliation:
University of Sydney, School of Biological Sciences, Australia
J. Hummel
Affiliation:
University of Bonn, Institute of Animal Science, Animal Nutrition Group, Germany
*
Get access

Abstract

Comparative physiology applies methods established in domestic animal science to a wider variety of species. This can lead to improved insight into evolutionary adaptations of domestic animals, by putting domestic species into a broader context. Examples include the variety of responses to seasonally fluctuating environments, different adaptations to heat and drought, and in particular adaptations to herbivory and various herbivore niches. Herbivores generally face the challenge that a high food intake compromises digestive efficiency (by reducing ingesta retention time and time available for selective feeding and for food comminution), and a variety of digestive strategies have evolved in response. Ruminants are very successful herbivores. They benefit from potential advantages of a forestomach without being constrained in their food intake as much as other foregut fermenters, because of their peculiar reticuloruminal sorting mechanism that retains food requiring further digestion but clears the forestomach of already digested material; the same mechanism also optimises food comminution. Wild ruminants vary widely in the degree to which their rumen contents ‘stratify’, with little stratification in ‘moose-type’ ruminants (which are mostly restricted to a browse niche) and a high degree of stratification into gas, particle and fluid layers in ‘cattle-type’ ruminants (which are more flexible as intermediate feeders and grazers). Yet all ruminants uniformly achieve efficient selective particle retention, suggesting that functions other than particle retention played an important role in the evolution of stratification-enhancing adaptations. One interesting emerging hypothesis is that the high fluid turnover observed in ‘cattle-type’ ruminants – which is a prerequisite for stratification – is an adaptation that not only leads to a shift of the sorting mechanism from the reticulum to the whole reticulo-rumen, but also optimises the harvest of microbial protein from the forestomach. Although potential benefits of this adaptation have not been quantified, the evidence for convergent evolution toward stratification suggests that they must be substantial. In modern production systems, the main way in which humans influence the efficiency of energy uptake is by manipulating diet quality. Selective breeding for conversion efficiency has resulted in notable differences between wild and domestic animals. With increased knowledge on the relevance of individual factors, that is fluid throughput through the reticulo-rumen, more specific selection parameters for breeding could be defined to increase productivity of domestic ruminants by continuing certain evolutionary trajectories.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alamer, M, Al-hozab, A 2004. Effect of water deprivation and season on feed intake, body weight and thermoregulation in Awassi and Najdi sheep breeds in Saudi Arabia. Journal of Arid Environments 59, 7184.CrossRefGoogle Scholar
Alexander, RM 1993. The relative merits of foregut and hindgut fermentation. Journal of Zoology 231, 391401.CrossRefGoogle Scholar
Archer, D, Sanson, G 2002. Form and function of the selenodont molar in southern African ruminants in relation to their feeding habits. Journal of Zoology 257, 1326.CrossRefGoogle Scholar
Argenzio, RA, Stevens, CE 1984. The large bowel – a supplementary rumen? Proceedings of the Nutrition Society 43, 1323.CrossRefGoogle ScholarPubMed
Arnold, W, Ruf, T, Reimoser, S, Tataruch, F, Onderscheka, K, Schober, F 2004. Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus). American Journal of Physiology. Regulatory Integrative and Comparative Physiology 286, R174R181.CrossRefGoogle ScholarPubMed
Asher, GW, Monfort, SL, Wemmer, C 1999. Comparative reproductive function in cervids: implications for management of farm and zoo populations. Journal of Reproduction and Fertility 54 (suppl.), 143156.Google ScholarPubMed
Baker, DL, Hobbs, NT 1987. Strategies of digestion: digestive efficiency and retention times of forage diets in montane ungulates. Canadian Journal of Zoology 65, 19781984.CrossRefGoogle Scholar
Barry, TN, Suttie, JM, Milne, JA, Kay, RNB 1991. Control of food intake in domesticated deer. In Physiological aspects of digestion and metabolism in ruminants. Proceedings of the VIIth International Symposium on ruminant physiology, Sendai, Japan (ed. T Tsuda, Y Sasaki and R Kawashima), pp. 385401. Academic Press, San Diego, CA, USA.CrossRefGoogle Scholar
Baumont, R, Deswysen, AG 1991. Mélange et propulsion du contenu du réticulo-rumen. Reproduction Nutrition Development 31, 335359.CrossRefGoogle ScholarPubMed
Becker, S, Katz, L 2005. Seasonal changes in serum leptin concentrations and body weight in captive female white-tailed deer. Annual Meeting of the Society for the Study of Reproduction, Québec City, Qc, Canada 38, W174.Google Scholar
Ben Salem, H, Priolo, A, Morand-Fehr, P 2008. Shrubby vegetation and agro-industrial by-products as alternative feed resources for sheep and goats: effects on digestion, performance and product quality. Animal Feed Science and Technology 147, 12.CrossRefGoogle Scholar
Beuchat, CA 1990. Body size, medullary thickness, and urine concentrating ability in mammals. American Journal of Physiology 258, R298R308.Google ScholarPubMed
Bird, AR, Croom, WJ, Bailey, JV, O’Sullivan, BM, Hagler, WM, Gordon, GL, Martin, PR 1993. Tropical pasture hay utilization with slaframine and cottonseed meal: ruminal characteristics and digesta passage in wethers. Journal of Animal Science 71, 16341640.CrossRefGoogle ScholarPubMed
Boyd, CS, Collins, WB, Urness, PJ 1996. Relationship of dietary browse to intake in captive muskoxen. Journal of Range Management 49, 27.CrossRefGoogle Scholar
Cain, JW, Krausman, PR, Rosenstock, SS, Turner, JC 2006. Mechanisms of thermoregulation and water balance in desert ungulates. Wildlife Society Bulletin 34, 570581.CrossRefGoogle Scholar
Cardillo, M, Huxtable, JS, Bromhan, L 2003. Geographic range size, life history and ratesof diversification in Australian mammals. Journal of Evolutionary Biology 16, 282288.CrossRefGoogle Scholar
Chalupa, W 1977. Manipulating rumen fermentation. Journal of Animal Science 45, 585599.CrossRefGoogle Scholar
Chemineau, P, Guillaume, D, Migaud, M, Thiéry, JC, Pellicer-Rubio, MT, Malpaux, B 2008. Seasonality of reproduction in mammals: intimate regulatory mechanisms and practical implications. Reproduction of Domesitc Animals 43 (suppl. 2), 4047.CrossRefGoogle ScholarPubMed
Chilliard, Y., Bocquier, F. 2000. Direct effects of photoperiod on lipid metabolism, leptin synthesis and milk secretion in adult sheep. In Ruminant physiology: digestion, metabolism, growth and reproduction (ed. PB Cronjé), pp. 205223. CABI Publishing, Wallingford, UK.CrossRefGoogle Scholar
Chilliard, Y, Delavaud, C, Bonnet, M 2005. Leptin expression in ruminants: nutritional and physiological regulations in relation with energy metabolism. Domestic Animal Endocrinology 29, 322.CrossRefGoogle ScholarPubMed
Chivers, DJ, Langer, P 1994. The digestive system in mammals. Food, form and function. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Clauss, M 2004. The potential interplay of posture, digestive anatomy, ingesta density and gravity in mammalian herbivores, or why sloths do not rest hanging upside down. Mammal Review 34, 241245.CrossRefGoogle Scholar
Clauss, M, Lechner-Doll, M 2001. Differences in selective reticulo-ruminal particle retention as a key factor in ruminant diversification. Oecologia 129, 321327.CrossRefGoogle ScholarPubMed
Clauss, M, Dierenfeld, ES 2008. The nutrition of browsers. In Zoo and wild animal medicine. Current therapy 6 (ed. ME Fowler and RE Miller), pp. 444454. Saunders Elsevier, St. Louis, MO, USA.CrossRefGoogle Scholar
Clauss, M, Suedmeyer, WK, Flach, EJ 1999. Susceptibility to cold in captive giraffe (Giraffa camelopardalis). Proceedings of the American Association of Zoo Veterinarians, 183186.Google Scholar
Clauss, M, Lechner-Doll, M, Behrend, A, Lason, K, Lang, D, Streich, WJ 2001. Particle retention in the forestomach of a browsing ruminant, the roe deer (Capreolus capreolus). Acta Theriologica 46, 103107.Google Scholar
Clauss, M, Lechner-Doll, M, Streich, WJ 2002. Faecal particle size distribution in captive wild ruminants: an approach to the browser/grazer-dichotomy from the other end. Oecologia 131, 343349.CrossRefGoogle Scholar
Clauss, M, Kienzle, E, Hatt, JM 2003a. Feeding practice in captive wild ruminants: peculiarities in the nutrition of browsers/concentrate selectors and intermediate feeders. A review. In Zoo animal nutrition (ed. A Fidgett, M Clauss, U Ganslosser, JM Hatt and J Nijboer), vol. 2, pp. 2752. Filander Verlag, Fürth, Germany.Google Scholar
Clauss, M, Lechner-Doll, M, Streich, WJ 2003b. Ruminant diversification as an adaptation to the physicomechanical characteristics of forage. A reevaluation of an old debate and a new hypothesis. Oikos 102, 253262.CrossRefGoogle Scholar
Clauss, M, Frey, R, Kiefer, B, Lechner-Doll, M, Loehlein, W, Polster, C, Rössner, GE, Streich, WJ 2003c. The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136, 1427.CrossRefGoogle ScholarPubMed
Clauss, M, Lechner-Doll, M, Streich, WJ 2004. Differences in the range of faecal dry matter content between feeding types of captive wild ruminants. Acta Theriologica 49, 259267.CrossRefGoogle Scholar
Clauss, M, Hummel, J, Streich, WJ 2006a. The dissociation of the fluid and particle phase in the forestomach as a physiological characteristic of large grazing ruminants: an evaluation of available, comparable ruminant passage data. European Journal of Wildlife Research 52, 8898.CrossRefGoogle Scholar
Clauss, M, Hofmann, RR, Hummel, J, Adamczewski, J, Nygren, K, Pitra, C, Streich, WJ, Reese, S 2006b. The macroscopic anatomy of the omasum of free-ranging moose (Alces alces) and muskoxen (Ovibos moschatus) and a comparison of the omasal laminal surface area in 34 ruminant species. Journal of Zoology 270, 346358.CrossRefGoogle Scholar
Clauss, M, Franz-Odendaal, TA, Brasch, J, Castell, JC, Kaiser, TM 2007a. Tooth wear in captive giraffes (Giraffa camelopardalis): mesowear analysis classifies free-ranging specimens as browsers but captive ones as grazers. Journal of Zoo and Wildlife Medicine 38, 433445.CrossRefGoogle ScholarPubMed
Clauss, M, Schwarm, A, Ortmann, S, Streich, WJ, Hummel, J 2007b. A case of non-scaling in mammalian physiology? Body size, digestive capacity, food intake, and ingesta passage in mammalian herbivores Comparative Biochemistry and Physiology. Part A: Molecular and Integrative Physiology 148, 249265.Google Scholar
Clauss, M, Streich, WJ, Schwarm, A, Ortmann, S, Hummel, J 2007c. The relationship of food intake and ingesta passage predicts feeding ecology in two different megaherbivore groups. Oikos 116, 209216.CrossRefGoogle Scholar
Clauss, M, Kaiser, T, Hummel, J 2008a. The morphophysiological adaptations of browsing and grazing mammals. In The ecology of browsing and grazing (ed. IJ Gordon and HHT Prins), pp. 4788. Springer, Heidelberg, Germany.CrossRefGoogle Scholar
Clauss, M, Schwarm, A, Ortmann, S, Hummel, J 2008b. Rumination frees mammalian herbivores from foregut fermentation’s metabolic constraints. Proceedings of the Symposium of the Comparative Nutrition Society 7, 3742.Google Scholar
Clauss, M, Hofmann, RR, Streich, WJ, Fickel, J, Hummel, J 2008c. Higher masseter mass in grazing than in browsing ruminants. Oecologia 157, 377385.CrossRefGoogle ScholarPubMed
Clauss, M, Streich, WJ, Nunn, CL, Ortmann, S, Hohmann, G, Schwarm, A, Hummel, J 2008d. The influence of natural diet composition, food intake level, and body size on ingesta passage in primates Comparative Biochemistry and Physiology. Part A: Molecular and Integrative Physiology 150, 274281.Google Scholar
Clauss, M, Grum, C, Hatt, JM 2009a. Polyunsaturated fatty acid content in adipose tissue in foregut and hindgut fermenting mammalian herbivores: a literature survey. Mammalian Biology 74, 153158.CrossRefGoogle Scholar
Clauss, M, Nunn, C, Fritz, J, Hummel, J 2009b. Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores Comparative Biochemistry and Physiology. Part A: Molecular and Integrative Physiology 154, 376382.Google Scholar
Clauss, M, Hofmann, RR, Fickel, J, Streich, WJ, Hummel, J 2009c. The intraruminal papillation gradient in wild ruminants of different feeding types: implications for rumen physiology. Journal of Morphology 270, 929942.CrossRefGoogle ScholarPubMed
Clauss, M, Fritz, J, Bayer, D, Hummel, J, Streich, WJ, Südekum, K-H, Hatt, JM 2009d. Physical characteristics of rumen contents in two small ruminants of different feeding type, the mouflon (Ovis ammon musimon) and the roe deer (Capreolus capreolus). Zoology 112, 195205.CrossRefGoogle ScholarPubMed
Clauss, M, Fritz, J, Bayer, D, Nygren, K, Hammer, S, Hatt, JM, Südekum, K-H, Hummel, J 2009e. Physical characteristics of rumen contents in four large ruminants of different feeding type, the addax (Addax nasomaculatus), bison (Bison bison), red deer (Cervus elaphus) and moose (Alces alces). Comparative Biochemistry and Physiology A 152, 398406.CrossRefGoogle Scholar
Clauss, M, Hofmann, RR, Streich, WJ, Fickel, J, Hummel, J 2010. Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of different feeding types and a new resulting hypothesis on reticular function. Journal of Zoology. In press, DOI:10.1111/j.1469-7998.2009.00675.x.CrossRefGoogle Scholar
Codron, D, Lee-Thorp, JA, Sponheimer, M, Codron, J, de Ruiter, D, Brink, JS 2007. Significance of diet type and diet quality for ecological diversity of African ungulates. Journal of Animal Ecology 76, 526537.CrossRefGoogle ScholarPubMed
Codron, D, Brink, JS, Rossouw, L, Clauss, M 2008a. The evolution of ecological specialization in southern African ungulates: competition or physical environmental turnover? Oikos 117, 344353.CrossRefGoogle Scholar
Codron, D, Brink, JS, Rossouw, L, Clauss, M, Codron, J, Lee-Thorp, JA, Sponheimer, M 2008b. Functional differentiation of African grazing ruminants: an example of specialized adaptations to very small changes in diet. Biological Journal of the Linnaean Society 94, 755764.CrossRefGoogle Scholar
Cork, SJ, Hume, ID, Faichney, GJ 1999. Digestive strategies of nonruminant herbivores: the role of the hindgut. In Nutritional ecology of herbivores. Proceedings of the 5th International Symposium on the Nutrition of Herbivores (ed. HJG Jung and GC Fahey), pp. 210260. American Society of Animal Science, Savoy, IL, USA.Google Scholar
Croom, WJ, Bird, AR, Blacks, BL, McBride, BW 1993. Manipulation of gastrointestinal nutrient delivery in livestock. Journal of Dairy Science 76, 21122124.CrossRefGoogle ScholarPubMed
Dellow, DW, Hume, ID, Clarke, RTJ, Bauchop, T 1988. Microcbial activity in the forestomach of free-living macropodid marsupials: comparisons with laboratory studies. Australian Journal of Zoology 36, 383395.CrossRefGoogle Scholar
DeMiguel, D, Fortelius, M, Azanza, B, Morales, J 2008. Ancestral feeding state of ruminants reconsidered: earliest grazing adaptation claims a mixed condition for cervidae. BMC Evolutionary Biology 8, 13.CrossRefGoogle ScholarPubMed
Demment, MW, Longhurst, WH 1987. Browsers and grazers: constraints on feeding ecology imposed by gut morphology and body size. In Proceedings of the IVth International Conference on Goats (ed. OP Santana, AG da Silva and WC Foote), pp. 9891004. Departimento de Disuao de Tecnologia, Brazilia, Brasil.Google Scholar
Dunson, WA 1974. Some aspects of salt and water balance of feral goats from arid islands. American Journal of Physiology 226, 662669.CrossRefGoogle ScholarPubMed
Elsden, SR, Hitchcock, MWS, Marshall, RA, Phillipson, AT 1946. Volatile acids in the digesta of ruminants and other animals. Journal of Experimental Biology 22, 191202.CrossRefGoogle ScholarPubMed
Faichney, GJ 2006. Digesta flow. In Quantitative aspects of ruminant digestion and metabolism (ed. J Dijkstra, JM Forbes and J France), pp. 4986. CAB International, Wellingford, UK.Google Scholar
Fritz, J, Hummel, J, Kienzle, E, Arnold, C, Nunn, C, Clauss, M 2009. Comparative chewing efficiency in mammalian herbivores. Oikos 118, 16231632.CrossRefGoogle Scholar
Froetschel, MA, Amos, HE, Evans, JJ, Croom, WJ, Hagler, WM 1989. Effects of a salivary stimulant, slaframine, on ruminal fermentation, bacterial protein synthesis and digestion in frequently fed steers. Journal of Animal Science 67, 827834.CrossRefGoogle ScholarPubMed
Fuller, A, Maloney, SK, Mitchell, G, Mitchell, D 2004. The eland and the oryx revisited: body and brain temperatures of free-living animals. International Congress Series 1275, 275282.CrossRefGoogle Scholar
Garrod, AH 1877. Notes on the visceral anatomy and osteology of the ruminants, with a suggestion regarding a method of expressing the relations of species by means of formulae. Proceedings of the Zoological Society of London, 218.Google Scholar
Gaspar-López, E, Casabiell, J, Estevez, JA, Landete-Castillejos, T, De La Cruz, LF, Gallego, L, García, AJ 2009. Seasonal changes in plasma leptin concentration related to antler cycle in Iberian red deer stags. Journal of Comparative Physiology B 179, 617622.CrossRefGoogle ScholarPubMed
Goodchild, AV, McMeniman, NP 1994. Intake and digestibility of low-quality roughages when supplemented with leguminous browse. Journal of Agricultural Science 122, 151160.CrossRefGoogle Scholar
Gordon, IJ, Illius, AW 1994. The functional significance of the browser-grazer dichotomy in African ruminants. Oecologia 98, 167175.CrossRefGoogle ScholarPubMed
Guernsey, MP, Jones, WT, Reid, CSW 1980. A method for investigating salivation in cattle using pilocarpine as a sialagogue. New Zealand Journal of Agricultural Research 23, 3341.CrossRefGoogle Scholar
Harrison, DG, McAllan, AB 1980. Factors affecting microbial growth yields in the reticulo-rumen. In Digestive physiology and metabolism in ruminants. Proceedings of the 5th International Symposium on Ruminant Physiology at Clermont-Ferrand, France (ed. Y Ruckebush and P Thivend), pp. 205226. MTP Press, Lancaster, UK.Google Scholar
Hatt, JM, Clauss, M 2006. Browse silage in zoo animal nutrition – feeding enrichment of browsers during winter. In Zoo animal nutrition Vol. III (ed. A Fidgett, M Clauss, K Eulenberger, JM Hatt, ID Hume, GP Janssens and J Nijboer), pp. 201204. Filander Verlag, Fürth, Germany.Google Scholar
Heydon, MJ, Sibbald, AM, Milne, JA, Brinklow, BR, Loudon, ASI 1993. The interaction of food availability and endogenous physiological cycles on the grazing ecology of red deer hinds (Cervus elaphus). Functional Ecology 7, 216222.CrossRefGoogle Scholar
Hofmann, RR 1973. The ruminant stomach. East African Literature Bureau, Nairobi, Kampala.Google Scholar
Hofmann, RR 1985. Digestive physiology of deer – their morphophysiological specialisation and adaptation. Royal Society of New Zealand Bulletin 22, 393407.Google Scholar
Hofmann, RR 1988. Morphophysiological evolutionary adaptations of the ruminant digestive system. In Aspects of digestive physiology in ruminants (ed. A Dobson and MJ Dobson), pp. 120. Cornell University Press, Ithaca, NY, USA.Google Scholar
Hofmann, RR 1989. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78, 443457.CrossRefGoogle ScholarPubMed
Hofmann, RR, Streich, WJ, Fickel, J, Hummel, J, Clauss, M 2008. Convergent evolution in feeding types: salivary gland mass differences in wild ruminant species. Journal of Morphology 269, 240257.CrossRefGoogle ScholarPubMed
Holechek, JL, Vavra, M, Skovlin, J, Krueger, WC 1982. Cattle diets in the Blue Mountains of Oregon. II. Forests. Journal of Range Management 35, 239242.CrossRefGoogle Scholar
Höllerl, S, Stimm, B, Hummel, J, Clauss, M 2006. Browse provision for captive herbivores: design and management of a browse plantation. In Zoo animal nutrition Vol. III (ed. A Fidgett, M Clauss, K Eulenberger, JM Hatt, ID Hume, GP Janssens and J Nijboer), pp. 211212. Filander Verlag, Fürth, Germany.Google Scholar
Hörnicke, H, Björnhag, G 1980. Coprophagy and related strategies for digesta utilization. In Digestive physiology and metabolism in ruminants (ed. Y Ruckebusch and P Thivent), pp. 707730. MTP Press, Lancaster, UK.CrossRefGoogle Scholar
Horst, RL, Langworthy, M 1971. Observations on the kidney of the desert bighorn sheep. Anatomical Record 2, 343Google Scholar
Hudson, RJ, White, RG 1985. Bioenergetics of wild herbivores. CRC Press, Boca Raton, FL, USA.Google Scholar
Hume, ID 1985. Evolution of herbivores – the ruminant in perspective. In Ruminant physiology: concepts and consequences. A tribute to R. J. Moir. Proceedings of a Symposium held at the University of Western Australia 7–10 May 1984 (ed. SK Baker, JM Gawthorne, JB Mackintosh and DB Purser), pp. 1525. University of Western Australia Press, Perth, Australia.Google Scholar
Hume, ID 1999. Marsupial nutrition. Cambridge University Press, Cambridge, UK.Google Scholar
Hume, ID 2005. Concepts of digestive efficiency. In Physiological and ecological adaptations to feeding in vertebrates (ed. JM Starck and T Wang), pp. 4358. Science Publishers, Enfield, NH, USA.Google Scholar
Hume, ID, Warner, ACI 1980. Evolution of microbial digestion in mammals. In Digestive physiology and metabolism in ruminants (ed. Y Ruckebusch and P Thivend), pp. 665684. MTP Press, Lancaster, UK.CrossRefGoogle Scholar
Hume, ID, Sakaguchi, E 1991. Patterns of digesta flow and digestion in foregut and hindgut fermenters. In Physiological aspects of digestion and metabolism in ruminants (ed. T Tsuda, Y Saaski and R Kawashima), pp. 427451. Academic Press, San Diego, CA, USA.CrossRefGoogle Scholar
Hummel, J, Clauss, M 2006. Feeding. In EAZA husbandry and management guidelines for Giraffa camelopardalis, pp. 2961. Burger’s Zoo, Arnhem, NL.Google Scholar
Hummel, J, Clauss, M, Zimmermann, W, Johanson, K, Norgaard, C, Pfeffer, E 2005. Fluid and particle retention in captive okapi (Okapia johnstoni) Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology 140, 436444.CrossRefGoogle Scholar
Hummel, J, Südekum, K-H, Streich, WJ, Clauss, M 2006a. Forage fermentation patterns and their implications for herbivore ingesta retention times. Functional Ecology 20, 9891002.CrossRefGoogle Scholar
Hummel, J, Clauss, M, Baxter, E, Flach, EJ, Johansen, K 2006b. The influence of roughage intake on the occurrence of oral disturbances in captive giraffids. In Zoo animal nutrition Vol. III (ed. A Fidgett, M Clauss, K Eulenberger, J Hatt, M, I Hume, G Janssens and J Nijboer), pp. 235252. Filander Verlag, Fürth, Germany.Google Scholar
Hummel, J, Pfeffer, E, Norgaard, C, Johanson, K, Clauss, M, Nogge, G 2006c. Energetic nutrition of the okapi in captivity: intake and digestion trials. Zoo Biology 25, 303316.CrossRefGoogle Scholar
Hummel, J, Steuer, P, Südekum, K-H, Hammer, S, Hammer, C, Streich, WJ, Clauss, M 2008a. Fluid and particle retention in the digestive tract of the addax antelope (Addax nasomaculatus) – adaptations of a grazing desert ruminant. Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology 149, 142149.CrossRefGoogle Scholar
Hummel, J, Fritz, J, Kienzle, E, Medici, EP, Lang, S, Zimmermann, W, Streich, WJ, Clauss, M 2008b. Differences in fecal particle size between free-ranging and captive individuals of two browser species. Zoo Biology 27, 7077.CrossRefGoogle ScholarPubMed
Hummel, J, Südekum, K-H, Bayer, D, Ortmann, S, Hatt, JM, Streich, WJ, Clauss, M 2009. Physical characteristics of reticuloruminal contents of cattle in relation to forage type and time after feeding. Journal of Animal Physiology and Animal Nutrition 93, 209220.CrossRefGoogle ScholarPubMed
Janis, C 1976. The evolutionary strategy of the Equidae and the origins of rumen and cecal digestion. Evolution 30, 757774.CrossRefGoogle ScholarPubMed
Jessen, C 2001. Temperature regulation in humans and other mammals. Springer, Berlin, Germany.CrossRefGoogle Scholar
Kaiser, TM, Brasch, J, Castell, JC, Schulz, E, Clauss, M 2008. Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics. Mammalian Biology 74, 425437.CrossRefGoogle Scholar
Kaiser, TM, Fickel, J, Streich, WJ, Hummel, J, Clauss, M 2010. Enamel ridge alignment in upper molars of ruminants in relation to their natural diet. Journal of Zoology In press DOI:10.1111/j.1469-7998.2009.00674.CrossRefGoogle Scholar
Karasov, WH, Martínez del Rio, C 2007. Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, Princeton, New Jersey, USA.CrossRefGoogle Scholar
Kay, RNB 1989. Adaptation of the ruminant digestive tract to diet. Acta Veterinaria Scandinavica 86 (suppl.), 196203.Google ScholarPubMed
Kay, RNB, von Engelhardt, W, White, RG 1980. The digestive physiology of wild ruminants. In Digestive physiology and metabolism in ruminants (ed. Y Ruckebush and P Thivend), pp. 743761. MTP Press, Lancaster, UK.CrossRefGoogle Scholar
Kempton, TJ, Murray, RM, Leng, RA 1976. Methane production and digestibility measurements in the grey kangaroo and sheep. Australian Journal of Biological Sciences 29, 209214.CrossRefGoogle ScholarPubMed
Kii, WY, Dryden, GM 2005. Effect of drinking saline water on food and water intake, food digestibility, and nitrogen and mineral balances of rusa deer stags (Cervus timorensis russa). Animal Science 81, 99105.CrossRefGoogle Scholar
Kirkwood, JK, Gaskin, CD, Markham, J 1987. Perinatal mortality and season of birth in captive wild ungulates. Veterinary Record 120, 386390.CrossRefGoogle ScholarPubMed
Knaus, W 2009. Dairy cows trapped between performance demands and adaptability. Journal of the Science of Food and Agriculture 89, 11071114.CrossRefGoogle Scholar
Langer, P 1991. Evolution of the digestive tract in mammals. Verhandlungen der Deutschen Zoologischen Gesellschaft 84, 169193.Google Scholar
Langer, P 1994. Food and digestion of Cenozoic mammals in Europe. In The digestive system of mammals: food, form and function (ed. DJ Chivers and P Langer), pp. 924. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Langer, P, Snipes, RL 1991. Adaptations of gut structure to function in herbivores. In Physiological aspects of digestion and metabolism in ruminants (ed. T Tsuda, Y Sasaki and R Kawashima), pp. 349384. Academic Press, San Diego, CA, USA.CrossRefGoogle Scholar
Lechner, I, Barboza, P, Collins, W, Günther, D, Hattendorf, B, Hummel, J, Clauss, M 2009. No ‘bypass’ in adult ruminants: passage of fluid ingested vs. fluid inserted into the rumen in fistulated muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces). Comparative Biochemistry and Physiology. Part A, Molecular and integrative physiology 154, 151156.CrossRefGoogle Scholar
Lechner, I, Barboza, P, Collins, W, Fritz, J, Günther, D, Hattendorf, B, Hummel, J, Südekum, K-H, Clauss, M 2010. Differential passage of fluids and different-sized particles in fistulated oxen (Bos primigenius f taurus), muskoxen (Ovibos moschatus), reindeer (Rangifer tarandus) and moose (Alces alces): rumen particle size discrimination is independent from contents stratification. Comparative Biochemistry and Physiology. Part A, Molecular and integrative physiology 155, 211222.CrossRefGoogle Scholar
Lechner-Doll, M, von Engelhardt, W 1989. Particle size and passage from the forestomach in camels compared to cattle and sheep fed a similar diet. Journal of Animal Physiology and Animal Nutrition 61, 120128.CrossRefGoogle Scholar
Lechner-Doll, M, Kaske, M, von Engelhardt, W 1991. Factors affecting the mean retention time of particles in the forestomach of ruminants and camelids. In Physiological aspects of digestion and metabolism in ruminants (ed. T Tsuda, Y Sasaki and R Kawashima), pp. 455482. Academic Press, San Diego, CA, USA.CrossRefGoogle Scholar
Lechner-Doll, M, Deutsch, A, Lang, D 2000. Nutritional management of ungulates in captivity – should we learn from natural seasonality of the vegetation?. In Zoo animal nutrition (ed. J Nijboer, J Hatt, W Kaumanns, A Beijnen and U Ganslosser), pp. 205212. Filander, Fürth, Germany.Google Scholar
Loudon, ASI 1991. Nutritional physiology of some Asian ruminants. In Physiological aspects of digestion and metabolism in ruminants (ed. T Tsuda, Y Sasaki and R Kawashima), pp. 403425. Academic Press, San Diego, CA, USA.CrossRefGoogle Scholar
Majak, W, Hall, JW, Rode, LM, Kalnin, CM 1986. Rumen clearance rates in relation to the occurence of alfalfa bloat in cattle. 1. Passage of water-soluble markers. Journal of Dairy Science 69, 15601567.CrossRefGoogle Scholar
Maloiy, GMO, Macfarlane, WV, Shkolnik, A 1979. Mammalian herbivores. In Comparative physiology of osmoregulation in animals (ed. GMO Maloiy), pp. 185209. Academic Press, New York, NY, USA.Google Scholar
Maloiy, GMO, Rugangazi, BM, Rowe, MF 2009. Energy expenditure during level locomotion in large desert ungulates: the one-humped camel and the domestic donkey. Journal of Zoology 277, 248255.CrossRefGoogle Scholar
Mauget, C, Mauget, R, Sempéré, A 1997. Metabolic rate in female European roe deer (Capreolus capreolus): incidence of reproduction. Canadian Journal of Zoology 75, 731739.CrossRefGoogle Scholar
McNab, BK 2006. The energetics of reproduction in endotherms and its implication for their conservation. Integrative and Comparative Biology 46, 11591168.CrossRefGoogle ScholarPubMed
McNab, BK 2008. An analysis of the factors that influence the level and scaling of mammalian BMR. Comparative Biochemistry and Physiology. Part A, Molecular and integrative physiology 151, 528.CrossRefGoogle Scholar
Mendel, VE, Boda, JM 1961. Physiological studies of the rumen with emphasis on the animal factors associated with bloat. Journal of Dairy Science 44, 18811898.CrossRefGoogle Scholar
Meot, F, Cirio, A, Biovin, R 1997. Parotid secretion daily patterns and measurement with ultrasonic flow probes in conscious sheep. Experimental Physiology 82, 905923.CrossRefGoogle ScholarPubMed
Milewski, A, Diamond, R 2000. Why are very large herbivores absent from Australia? A new theory of micronutrients. Journal of Biogeography 27, 957978.CrossRefGoogle Scholar
Moir, RJ 1965. The comparative physiology of ruminant-like animals. In Physiology of digestion in the ruminant (ed. RW Dougherty, BS Allen, W Burroughs, NL Jackson, AD McGilliard), pp. 114. Butterworths, Washington DC, USA.Google Scholar
Moir, RJ 1968. Ruminant digestion and evolution. In Handbook of physiology, Section 6 alimentary canal, Vol. V (ed. CF Code), pp. 26732694. American Physiological Society, Washington DC, USA.Google Scholar
Moir, RJ, Somers, M, Sharman, G, Waring, H 1954. Ruminant-like digestion in a marsupial. Nature 173, 269270.CrossRefGoogle Scholar
Morris, CA, Cullen, NG, Geertsema, HG 1997. Genetic studies of bloat susceptibility in cattle. Proceedings of the New Zealand Society of Animal Production 57, 1921.Google Scholar
Mortolaa, JP, Lanthier, C 2005. Breathing frequency in ruminants: a comparative analysis with non-ruminant mammals. Respiratory Physiology & Neurobiology 145, 265277.CrossRefGoogle Scholar
Müller, DWH, Bingaman, LL, Streich, WJ, Hatt, JM, Clauss, M 2010. Relevance of management and feeding regimes on life expectancy in captive deer. American Journal of Veterinary Research 71, 275280.CrossRefGoogle Scholar
Nehring, K 1965. Laub- und Reisigfutterstoffe. In Handbuch der Futtermittel Bd. 2 (ed. M Becker and K Nehring), pp. 127. Paul Parey, Hamburg, Germany.Google Scholar
Nehring, K, Schütte, J 1950. Über die Zusammensetzung und den Futterwert von Laub und Reisig. I. Über die Änderungen in der Zusammensetzung von Laub und Zweigen verschiedener Baumarten in Abhängigkeit von der Vegetationszeit. Archiv für Tierernährung 1, 151176.CrossRefGoogle Scholar
Nehring, K, Schütte, J 1951a. Über die Zusammensetzung und den Futterwert von Laub und Reisig. II. Über die Verdaulichkeit von Laub und Sommerreisig. Archiv für Tierernährung 1, 264289.CrossRefGoogle Scholar
Nehring, K, Schütte, J 1951b. Über die Zusammensetzung und den Futterwert von Laub und Reisig. III. Über den Futterwert von Fallaub und Winterreisig. Archiv für Tierernährung 1, 342360.CrossRefGoogle Scholar
Neuville, H, Derscheid, JM 1929. Recherches anatomiques sur l’okapi (Okapia johnstoni). IV. L’estomac. Revue de Zoologie et de Botanique Africaine 16, 373419.Google Scholar
Okine, EK, Mathison, GW, Hardin, RT 1989. Relations between passage rates of rumen fluid and particulate matter and foam production in rumen contents of cattle fed on different diets ad lib. British Journal of Nutrition 61, 387395.CrossRefGoogle ScholarPubMed
Ostrowski, S, Williams, JB 2006. Heterothermy of free-living Arabian sand gazelles (Gazella subgutturosa marica) in a desert environment. Journal of Experimental Biology 209, 14211429.CrossRefGoogle Scholar
Ostrowski, S, Williams, JB, Ismael, K 2003. Heterothermy and the water economy of free-living Arabian oryx (Oryx leucoryx). Journal of Experimental Biology 206, 14711478.CrossRefGoogle ScholarPubMed
Ostrowski, S, Williams, JB, Mésochina, P, Sauerwein, H 2006. Physiological acclimation of a desert antelope, Arabian oryx (Oryx leucoryx), to long-term food and water restriction. Journal of Comparative Physiology B 176, 191201.CrossRefGoogle ScholarPubMed
Owen-Smith, N 1988. Megaherbivores – the influence of very large body size on ecology. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Pagan, JD, Hintz, HF 1986. Equine energetics. I. Relationship between body weight and energy requirements in horses. Journal of Animal Science 63, 815821.CrossRefGoogle ScholarPubMed
Pérez-Barberìa, FJ, Gordon, IJ, Illius, A 2001a. Phylogenetic analysis of stomach adaptation in digestive strategies in African ruminants. Oecologia 129, 498508.CrossRefGoogle ScholarPubMed
Pérez-Barberìa, FJ, Gordon, IJ, Nores, C 2001b. Evolutionary transitions among feeding styles and habitats in ungulates. Evolutionary Ecology Research 3, 221230.Google Scholar
Pérez-Barberìa, FJ, Elston, DA, Gordon, IJ, Illius, AW 2004. The evolution of phylogenetic differences in the efficiency of digestion in ruminants. Proceedings of the Royal Society of London B 271, 10811090.CrossRefGoogle ScholarPubMed
Picard, K, Thomas, DW, Festa-Bianchet, M, Belleville, F, Laneville, A 1999. Differences in the thermal conductance of tropical and temperate bovid horns. Ecoscience 6, 148158.CrossRefGoogle Scholar
Piening, SY, Hammer, C, Clauss, M, Hammer, S 2009. Birth seasonality in captive bovids at Al Wabra Wildlife Preservation, Qatar. In Proceedings of the International Conference on Diseases of Zoo and Wild Animals (ed G Wibbelt, P Kretzschmar, H Hofer), vol. 1, pp. 297303. Leibniz Institute for Zoo and Wildlife Research (IZW), Berlin, Germany.Google Scholar
Prigge, E, Stuthers, B, Jacquemet, N 1990. Influence of forage diets on ruminal particle size, passage of digesta, feed intake and digestibility by steers. Journal of Animal Science 68, 43524360.CrossRefGoogle ScholarPubMed
Rhind, SM, Archer, ZA, Adam, CL 2002. Seasonality of food intake in ruminants: recent developments in understanding. Nutrition Research Reviews 15, 4365.CrossRefGoogle ScholarPubMed
Robbins, CT 1993. Wildlife feeding and nutrition. Academic Press, San Diego, CA, USA.Google Scholar
Robbins, CT, Spalinger, DE, Van Hoven, W 1995. Adaptations of ruminants to browse and grass diets: are anatomical-based browser-grazer interpretations valid? Oecologia 103, 208213.CrossRefGoogle ScholarPubMed
Rutter, SM 2006. Diet preference for grass and legumes in free-ranging domestic sheep and cattle: current theory and future application. Applied Animal Behaviour Science 97, 1735.CrossRefGoogle Scholar
Santiago-Moreno, J, Gómez-Brunet, A, Toledano-Díaz, A, Picazo, R, Gonzalez-Bulnes, A, López-Sebastián, A 2006. Seasonal endocrine changes and breeding activit in Mediterranean wild ruminants. Reproduction of Domesitc Animals 41 (suppl. 2), 7281.CrossRefGoogle Scholar
Savage, VM, Gillooly, JF, Woodruff, WH, West, GB, Allen, AP, Enquist, BJ, Brown, JH 2004. The predominance of quarter-power scaling in biology. Functional Ecology 18, 257282.CrossRefGoogle Scholar
Schwarm, A, Ortmann, S, Wolf, C, Streich, WJ, Clauss, M 2008. Excretion patterns of fluids and particle passage markers of different size in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis): two functionally different foregut fermenters. Comparative Biochemistry and Physiology. Part A, Molecular and integrative physiology 150, 3239.CrossRefGoogle Scholar
Schwarm, A, Ortmann, S, Wolf, C, Streich, WJ, Clauss, M 2009a. More efficient mastication allows increasing intake without compromising digestibility or necessitating a larger gut: comparative feeding trials in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis). Comparative Biochemistry and Physiology. Part A, Molecular and integrative physiology 152, 504512.CrossRefGoogle Scholar
Schwarm, A, Ortmann, S, Wolf, C, Streich, WJ, Clauss, M 2009b. 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 311, 647661.CrossRefGoogle ScholarPubMed
Schwarm, A, Schweigert, M, Ortmann, S, Hummel, J, Janssens, G, Streich, WJ, Clauss, M 2009c. No easy solution for the fractionation of faecal nitrogen in captive wild herbivores: results of a pilot study. Journal of Animal Physiology and Animal Nutrition 93, 596605.CrossRefGoogle ScholarPubMed
Schwitzer, C, Polowinsky, SY, Solman, C 2009. Fruits as foods – common misconceptions about frugivory. In Zoo animal nutrition IV (ed. M Clauss, AL Fidgett, JM Hatt, T Huisman, J Hummel, G Janssen, J Nijboer and A Plowman), pp. 131168. Filander Verlag, Fürth, Germany.Google Scholar
Shkolnik, A, Maltz, E, Chosniak, I 1980. The role of the ruminant’s digestive tract as a reservoir. In Digestive physiology and metabolism in ruminants (ed. Y Ruckebusch and P Thivend), pp. 731742. MT Press, Lancaster, UK.CrossRefGoogle Scholar
Silanikove, N 1994. The struggle to maintain hydration and osmoregulation in animals experiencing severe dehydration and rapid rehydration: the story of ruminants. Experimental Physiology 79, 281300.CrossRefGoogle ScholarPubMed
Soppela, P, Saarela, S, Heiskari, U, Nieminen, M 2008. The effects of wintertime undernutrition on plasma leptin and insulin levels in an arctic ruminant, the reindeer. Comparative Biochemistry and Physiology B 149, 613621.CrossRefGoogle Scholar
Stevens, CE, Hume, ID 1998. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiological Reviews 78, 393427.CrossRefGoogle ScholarPubMed
Stevens, CE, Argenzio, RA, Clemens, ET 1980. Microbal digestion: rumen versus large intestine. In Digestive physiology and metabolism in ruminants (ed. Y Ruckebusch and P Thivent), MTP Press, Lancaster, UK.Google Scholar
Sutherland, TM 1988. Particle separation in the forestomach of sheep. In Aspects of digestive physiology in ruminants (ed. A Dobson and MJ Dobson), pp. 4373. Cornell University Press, Ithaca, NY, USA.Google Scholar
Suzuki, M, Yokoyama, M, Onuma, M, Takahashi, H, Yamanaka, M, Okada, H, Ichimura, Y, Ohtaishi, N 2004. Significant relationships between the serum leptin concentration and the conventional fat reserve indices in a wildlife species, Hokkaido sika deer (Cervus nippon yesoensis). Wildlife Research 31, 97100.CrossRefGoogle Scholar
Taylor, CR 1969. The eland and the oryx. Scientific American 220, 8897.CrossRefGoogle ScholarPubMed
Tomkins, NW, McMeniman, NP, Daniel, RCW 1991. Voluntary feed intake and digestibility by red deer (Cervus elaphus) and sheep (Ovis ovis) of pangola grass (Digitaria decumbens) with or without a supplement of leucaena (Leucaena leucocephala). Small Ruminant Research 5, 337345.CrossRefGoogle Scholar
Tschuor, A, Clauss, M 2008. Investigations on the stratification of forestomach contents in ruminants: an ultrasonographic approach. European Journal of Wildlife Research 54, 627633.CrossRefGoogle Scholar
Valtorta, SE, Gallardo, MR, Sbodia, OA, Revelli, GR, Arakaki, C, Leva, PE, Gaggiotti, M, Tercero, EJ 2008. Water salinity effects on performance and rumen parameters of lactating grazing Holstein cows. International Journal of Biometereology 52, 239247.CrossRefGoogle ScholarPubMed
Van Saun, RJ 2006. Nutrient requirements of South American camelids: a factorial approach. Small Ruminant Research 61, 165186.CrossRefGoogle Scholar
Van Soest, PJ 1994. Nutritional ecology of the ruminant, 2nd editionCornell University Press, Ithaca, NY, USA.CrossRefGoogle Scholar
Van Soest, PJ, Dierenfeld, ES, Conklin, NL 1995. Digestive strategies and limitations of ruminants. In Ruminant physiology: digestion, metabolism, growth and reproduction (ed. W von Engelhardt, S Leonhard-Marek, G Breves and D Giesecke), pp. 581600. Ferdinand Enke, Stuttgart, Germany.Google Scholar
Van Wieren, SE 1996. Browsers and grazers: foraging strategies in ruminants. In Digestive strategies in ruminants and nonruminants (ed. SE Van Wieren), pp. 119146. Thesis Landbouw, University of Wageningen, NL.Google Scholar
Vermorel, M, Martin-Rosset, W, Vernet, J 1997. Energy utilization of twelve forages or mixed diets for maintenance by sport horses. Livestock Production Science 47, 157167.CrossRefGoogle Scholar
von Engelhardt, W, Wolter, S, Lawrenz, H, Hemsley, JA 1978. Production of methane in two non-ruminant herbivores. Comparative Biochemistry and Physiology 60, 309311.CrossRefGoogle Scholar
Webster, JR, Corson, ID, Littlejohn, RP, Martin, SK, Suttie, JM 2001. The roles of photoperiod and nutrition in the seasonal increases in growth and insulin-like growth factor-1 secretion in male red deer. Animal Science 73, 305311.CrossRefGoogle Scholar
White, CR, Seymour, RS 2005. Allometric scaling of mammalian metabolism. Journal of Experimental Biology 208, 16111619.CrossRefGoogle ScholarPubMed
Wiedmeier, RD, Arambel, MJ, Walters, JL 1987. Effect of orally administered pilocarpine on ruminal characteristics and nutrient digestibility in cattle. Journal of Dairy Science 70, 284289.CrossRefGoogle ScholarPubMed
Wolfe, BA, Sladky, KK, Loomis, MR 2000. Obstructive urolithiasis in a reticulated giraffe (Giraffa camelopardalis). Veterinary Record 146, 260261.CrossRefGoogle Scholar
Woodall, PF, Skinner, JD 1993. Dimensions of the intestine, diet and faecal water loss in some African antelope. Journal of Zoology 229, 457471.CrossRefGoogle Scholar
Zenker, W, Clauss, M, Huber, J, Altenbrunner-Martinek, B 2009. Rumen pH and hoof health in two groups of captive wild ruminants. In Zoo animal nutrition IV (ed. M Clauss, A Fidgett, JM Hatt, TR Huisman, J Hummel, G Janssens, J Nijboer and AB Plowman), pp. 247254. Filander Verlag, Fürth, Germany.Google Scholar