Macroecology of the host determines microecology of endobionts: Protozoal faunas vary with wild ruminant feeding type and body mass

Journal of Zoology

Volumn 283, Issue 3, 2011, Pages 169-185

  Clauss, M ^a   Muller K ^a   Fickel, J ^b   Streich, W J ^b   Hatt, J M ^a   Sudekum K H ^c  

^a UNIVERSITY OF ZURICH   (Switzerland)

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

^c UNIVERSITY OF BONN   (Germany)

Author keywords

Browser; Grazer; Rumen microbes; Rumen microbiology; Rumen physiology

Indexed keywords

BODY MASS; CORRELATION; DIET; FEEDING ECOLOGY; GRASS; MACROECOLOGY; PHYLOGENETICS; PHYLOGENY; PROTOZOAN; RUMINANT; SPECIES DIVERSITY; TAXONOMY; WILD POPULATION;

BOVIDAE; ISOTRICHIDAE; PROTOZOA;

EID: 79951798705     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2010.00759.x     Document Type: Article

References (134)

1. Abe, M. & Iriki, T. (1989). Mechanism whereby holotrich ciliates are retained in the reticulo-rumen of cattle. Br. J. Nutr. 62, 579-587.
2. Abe, M. & Kumeno, F. (1973). In vitro simulation of rumen fermentation: apparatus and effects of dilution rate and continuous dialysis on fermentation and protozoal population. J. Anim. Sci. 36, 941-948.
3. Abe, M., Nakagawa, Y. & Iriki, T. (1986). Comparison of the nature among different sites in the rumen of cows fed rations differing in hay-concentrate ratio. Jpn. J. Zootech. Sci. 57, 395-403.
4. Abe, M., Shibui, H., Iriki, T. & Kumeno, F. (1973). Relation between diet and protozoal population in the rumen. Br. J. Nutr. 29, 197-202.
5. Ankrah, P., Loerch, S.C. & Dehority, B.A. (1990). Sequestration, migration and lysis of protozoa in the rumen. J. Gen. Microbiol. 136, 1869-1875.
6. Bach, A., Calsamiglia, S. & Stern, M.D. (2005). Nitrogen metabolism in the rumen. J. Dairy Sci. 88 (Suppl. 1), E9-E21.
7. Behrend, A., Lechner-Doll, M., Streich, W.J. & Clauss, M. (2004). Seasonal faecal excretion, gut fill, liquid and particle marker retention in mouflon Ovis ammon musimon, and a comparison with roe deer Capreolus capreolus. Acta Theriol. 49, 503-515.
8. Bonhomme, A. (1990). Rumen ciliates: their metabolism and relationships with bacteria and their hosts. Anim. Feed Sci. Technol. 30, 203-266.
9. Borges, P.A., Dominguez-Bello, M.G. & Herrera, E.A. (1996). Digestive physiology of wild capybara. J. Comp. Physiol. B 166, 55-60.
10. Brüggemann, J., Giesecke, D. & Walser-Käst, K. (1967). Beiträge zur Wildbiologie und vergleichenden Tierphysiologie. II. Mikroorganismen im Pansen von Rothirsch (Cervus elaphus) und Reh (Capreolus capreolus). Z. Tierphysiol. Tierern. Futtermittelkd. 23, 143-151.
11. Buisson, J. (1923). Sur quelques infusoires nouveaux ou peu connus parasites des mammafières. Ann. Parasitol. Hum. Comp. 1, 209-246.
12. Buisson, J. (1924). Quelques infusoires parasites d'antelopes africaines. Ann. Parasitol. Hum. Comp. 2, 155-160.
13. Cameron, S.L. (2003). Taxonomy and phylogeny of endosymbiotic ciliates (Ciliophora: Litostomatea) associated with Australian herbivorous marsupials. Int. J. Parasitol. 33, 347-355.
14. Carl, G.R. & Brown, R.D. (1983). Protozoa in the forestomach of the collared peccary (Tayassu tajacu). J. Mammal. 64, 709.
15. Clarke, R.T.J. (1964). Studies on the flora and fauna of the bovine rumen. New Zealand: Massey University of Manawatu.
16. Clauss, M. & Dierenfeld, E.S. (2008). The nutrition of browsers. In Zoo and wild animal medicine. Current therapy 6: 444-454. Fowler, M.E. & Miller, R.E. (Eds). St Louis: Saunders Elsevier.
17. Clauss, M., Hofmann, R.R., Fickel, J., Streich, W.J. & Hummel, J. (2009). The intraruminal papillation gradient in wild ruminants of different feeding types: implications for rumen physiology. J. Morphol. 270, 929-942.
18. Clauss, M., Hofmann, R.R., Hummel, J., Adamczewski, J., Nygren, K., Pitra, C., Streich, W.J. & Reese, S. (2006a). 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. J. Zool. 270, 346-358.
19. Clauss, M., Hofmann, R.R., Streich, W.J., Fickel, J. & Hummel, J. (2008a). Higher masseter mass in grazing than in browsing ruminants. Oecologia 157, 377-385.
20. Clauss, M., Hofmann, R.R., Streich, W.J., Fickel, J. & Hummel, J. (2010a). Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of different feeding types and a new resulting hypothesis on reticular function. J. Zool. 281, 26-38.
21. Clauss, M., Hume, I.D. & Hummel, J. (2010b). Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4, 979-992.
22. Clauss, M. & Hummel, J. (2005). The digestive performance of mammalian herbivores: why big may not be that much better. Mammal. Rev. 35, 174-187.
23. Clauss, M., Hummel, J. & Streich, W.J. (2006b). 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. Eur. J. Wildl. Res. 52, 88-98.
24. Clauss, M., Kaiser, T. & Hummel, J. (2008b). The morphophysiological adaptations of browsing and grazing mammals. In The ecology of browsing and grazing: 47-88. Gordon, I.J. & Prins, H.H.T. (Eds). Heidelberg: Springer.
25. Clauss, M., Lechner, I., Barboza, P., Collins, W., Tervoort, T., Südekum, K.-H., Codron, D. & Hummel, J. (2010c). The effect of size and density on the mean retention time of particles in the reticulorumen of cattle (Bos primigenius f. taurus), muskoxen (Ovibos moschatus) and moose (Alces alces). Br. J. Nutr. (in press).
26. Clauss, M. & Lechner-Doll, M. (2001). Differences in selective reticulo-ruminal particle retention as a key factor in ruminant diversification. Oecologia 129, 321-327.
27. Clauss, M., Lechner-Doll, M. & Streich, W.J. (2003). Ruminant diversification as an adaptation to the physicomechanical characteristics of forage. A reevaluation of an old debate and a new hypothesis. Oikos 102, 253-262.
28. Codron, D., Brink, J.S., Rossouw, L., Clauss, M., Codron, J., Lee-Thorp, J.A. & Sponheimer, M. (2008). Functional differentiation of African grazing ruminants: an example of specialized adaptations to very small changes in diet. Biol. J. Linn. Soc. 94, 755-764.
29. Codron, D., Lee-Thorp, J.A., Sponheimer, M. & Codron, J. (2007a). Nutritional content of savanna plant foods: implications for browser/grazer models of ungulate diversification. Eur. J. Wildl. Res. 53, 100-111.
30. Codron, D., Lee-Thorp, J.A., Sponheimer, M., Codron, J., de Ruiter, D. & Brink, J.S. (2007b). Significance of diet type and diet quality for ecological diversity of African ungulates. J. Anim. Ecol. 76, 526-537.
31. Dehority, B.A. (1974). Rumen ciliate fauna of Alaskan moose (Alces americana), musk-ox (Ovibos moschatus) and Dall moutain sheep (Ovis dalli). J. Protozool. 21, 26-32.
32. Dehority, B.A. (1984). Evaluation of subsampling and fixation procedures used for counting rumen protozoa. Appl. Environ. Microbiol. 48, 182-185.
33. Dehority, B.A. (1986a). Microbes in the foregut of arctic ruminants. In Control of digestion and metabolism in ruminants: 307-325. Milligan, L.P., Grovum, W.L. & Dobson, A. (Eds). Englewoods Cliff: Reston Book, Prentice Hall.
34. Dehority, B.A. (1986b). Protozoa of the digestive tract of herbivorous mammals. Insect Sci. Appl. 7, 279-296.
35. Dehority, B.A. (1990). Rumen ciliate protozoa in ohio white-tailed deer (Odocoileus virginianus). J. Protozool. 37, 473-475.
36. Dehority, B.A. (1993). Laboratory manual for classification and morphology of rumen ciliate protoa, 1st edn. Florida: CRC Press.
37. Dehority, B.A. (1994). Rumen ciliate protozoa of the blue duiker (Cephalophus monticola), with observations on morphological variation lines within the species Entodinium dubardi. J. Euk. Microbiol. 41, 103-111.
38. Dehority, B.A. (2003). Rumen microbiology. Thrumpton: Nottingham University Press.
39. Dehority, B.A. (2004). In vitro determination of generation times for Entodinium exiguum, Ophryoscolex purkynjei and Eudiplodinium maggii. J. Euk. Microbiol. 51, 333-338.
40. Dehority, B.A. (2005). Effect of pH on viability of Entodinium caudatum, Entodinium exiguum, Epidinium caudatum, and Ophryoscolex purkynjei in vitro. J. Euk. Microbiol. 52, 339-342.
41. Dehority, B.A., Demarais, S. & Osborn, D.A. (1999). Rumen ciliates of white-tailed deer (Odocoileus virginianus), axis deer (Axis axis), sika deer (Cervus nippon) and fallow deer (Dama dama) from Texas. J. Euk. Microbiol. 46, 125-131.
42. Dehority, B.A. & Mattos, W.R. (1978). Diurnal changes and effect of ration on concentrations of the rumen ciliate Charon ventriculi. Appl. Environ. Microbiol. 36, 953-958.
43. Dehority, B.A. & Odenyo, A.A. (2003). Influence of diet on the rumen protozoal fauna of indigenous African wild ruminants. J. Euk. Microbiol. 50, 220-223.
44. Dehority, B.A. & Orpin, C.G. (1997). Development of, and natural fluctuations in, rumen microbial populations. In The rumen microbial ecosystem: 196-245. Hobson, P.N. & Stewart, C.S. (Eds). London: Chapman & Hall.
45. Dehority, B.A. & Tirabasso, P.A. (1989). Factors affecting the migration and sequestration of rumen protozoa in the family Isotrichidae. J. Gen. Microbiol. 135, 539-548.
46. Demment, M.W. (1982). The scaling of ruminoreticulum size with body weight in East African ungulates. Afr. J. Ecol. 20, 43-47.
47. Deutsch, A., Lechner-Doll, M. & Wolf, G.A. (1998). Activity of cellulolytic enzymes in the contents of reticulorumen and caecocolon of roe deer (Capreolus capreolus). Comp. Biochem. Physiol. A 119, 925-930.
48. Dogiel, V.A. (1925). Nouveaux infusoires de la familie des Ophryoscolecides parasites d'anilopes africaines. Ann. Parasitol. Hum. Comp. 3, 116-142.
49. Dogiel, V.A. (1927). Monographie der Familie Ophryoscolecidae. Arch. Protistenkd. 59, 1-288.
50. Dogiel, V.A. (1932). Beschreibung einiger neuer Vertreter der Familie Ophryoscolecidae aus afrikanischen Antilopen nebst Revision der Infusorienfauna afrikanischer Wiederkäuer. Arch. Protistenkd. 77, 92-107.
51. Dominguez-Bello, M.G., Ruiz, M.C. & Michelangeli, F. (1993). Evolutionary significance of foregut fermentation in the hoatzin (Opisthocomus hoazin; Aves: Opisthocomidae). J. Comp. Physiol. B 163, 594-601.
52. Drescher-Kaden, U. (1981). Vergleichende Untersuchungen in der Nahrungswahl von Gams- und Rotwild unter besonderer Berücksichtigung der mikrobiellen Besiedlung und der Verdauungsvorgänge im Pansen. Fortschr. Tierphysiol. Tierernaerung 12, 1-108.
53. Drescher-Kaden, U. & Seifelnasr, E.A. (1977). Untersuchungen am Verdauungstrakt von Reh, Damhirsch und Mufflon. Mitteilung 3: Mikroorganismen im Pansen von Reh, Damhirsch und Mufflon. Z. Jagdwiss. 23, 64-69.
54. Eugène, M., Archimède, H. & Sauvant, D. (2004). Quantitative meta-analysis on the effects of defaunation of the rumen on growth, intake and digestion in ruminants. Livest. Prod. Sci. 85, 81-97.
55. Ezenwa, V.O., Price, A., Altizer, S., Vitone, N.V. & Cook, K.C. (2006). Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla. Oikos 115, 526-536.
56. Fernandez, M.H. & Vrba, E.S. (2005). A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol. Rev. 80, 269-302.
57. Franzolin, R. & Dehority, B.A. (1996). Effect of prolonged high-concentrate feeding on ruminal protozoa concentrations. J. Anim. Sci. 74, 2803-2809.
58. Giesecke, D. (1970). Comparative microbiology of the alimentary tract. In Physiology of digestion and metabolism in the ruminant: 306-318. Phillipson, A.T. (Ed.). New Castle upon Tyne: Oriel Press.
59. Giesecke, D. & Van Gylswyk, N.O. (1975). A study of feeding types and certain rumen functions in six species of South African wild ruminants. J. Agri. Sci. 85, 75-83.
60. Goad, D.W., Goad, C.L. & Nagaraja, T.G. (1998). Ruminal microbial and fermentative changes associated with experimentally induced subacute acidosis in steers. J. Anim. Sci. 76, 234-241.
61. Grubb, J.A. & Dehority, B.A. (1975). Effects of an abrupt change in ration from all roughage to high concentrate upon rumen microbial numbers in sheep. Appl. Microbiol. 30, 404-412.
62. Hobson, P.N., Mann, S.O. & Summers, R. (1976). Rumen micro-organisms in red deer, hill sheep and reindeer in the Scottish highlands. Proc. Roy. Soc. Edinb.: Nat. Environ. 75, 171-180.
63. Hofmann, R.R. (1989). Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78, 443-457.
64. Hofmann, R.R. & Stewart, D.R.M. (1972). Grazer or browser: a classification based on the stomach-structure and feeding habit of East African ruminants. Mammalia 36, 226-240.
65. Hofmann, R.R., Streich, W.J., Fickel, J., Hummel, J. & Clauss, M. (2008). Convergent evolution in feeding types: salivary gland mass differences in wild ruminant species. J. Morphol. 269, 240-257.
66. Holechek, J., Pieper, R. & Herbel, C. (2004). Range management. Principles and practices, 5th edn. Upper Saddle River: Pearson/Prentice Hall.
67. Hoppe, P.P., Gwynn, M.D. & Van Hoven, W. (1981). Nutrients, protozoa and volatile fatty acids in the rumen of Harvey's duiker Cephalophus harveyi. S. Afr. J. Wildl. Res. 11, 110-111.
68. Hristov, A.N. & Jouany, J.P. (2005). Factors affecting the efficiency of nitrogen utilization in the rumen. In Nitrogen and phosphorus nutrition of cattle and environment: 117-166. Hristov, A.N. & Pfeffer, E. (Eds). Wallingford: CAB International.
69. Hummel, J., Clauss, M., Zimmermann, W., Johanson, K., Norgaard, C. & Pfeffer, E. (2005). Fluid and particle retention in captive okapi (Okapia johnstoni). Comp. Biochem. Physiol. A 140, 436-444.
70. Hummel, J., Nogge, G., Clauss, M., Norgaard, C., Johanson, K., Nijboer, J. & Pfeffer, E. (2006a). Energetic nutrition of the okapi in captivity: fermentation characteristics of feedstuffs. Zool. Biol. 25, 251-266.
71. Hummel, J., Südekum, K.-H., Streich, W.J. & Clauss, M. (2006b). Forage fermentation patterns and their implications for herbivore ingesta retention times. Funct. Ecol. 20, 989-1002.
72. Hungate, R.E. (1966). The rumen and its microbes. London: Academic Press.
73. Hungate, R.E. (1978). The rumen protozoa. In Parasitic protozoa: 655-695. Kreier, J.P. (Ed.). New York: Academic Press.
74. Ichimura, Y., Yamano, H., Takano, T., Koike, S., Kobayashi, Y., Ozaki, N., Suzuki, M., Okada, H. & Yamanaka, M. (2004). Rumen microbes and fermentation of wild sika deer on the shiretoko peninsula of Hokkaido Island, Japan. Ecol. Res. 19, 389-395.
75. Imai, S. & Rung, G. (1990). Rumen ciliates from the Mongolian gazelle, Procapra gutturosa. Nippon Juigaku Zasshi 52, 1063-1067.
76. Imai, S., Tsutsumi, Y., Yumura, S. & Mulenga, A. (1992). Ciliate protozoa in the rumen of Kafue lechwe, Kobus leche kafuensis, in Zambia, with the description of four new species. J. Protozool. 39, 564-572.
77. Ito, A., Imai, S. & Ogimoto, K. (1993). Rumen ciliates of Ezo deer (Cervus nippon yesoensis) with the morphological comparison with those of cattle. J. Vet. Med. Sci. 55, 93-98.
78. Jameson, A.P. (1925). A note on the ciliates from the stomach of the mouse deer (Tragulus meminna) with the description of Entodinium ovalis n. sp. Parasitology 17, 406-409.
79. Johnson, R.R. (1976). Influence of carbohydrate solubility on non-protein nitrogen utilization in the ruminant. J. Anim. Sci. 43, 184-191.
80. Jones, R.J., Meyer, J.H.F., Bechaz, F.M., Stolzt, M.A., Palmer, B. & van der Merwe, G. (2001). Comparison of rumen fluid from South African game species and from sheep to digest tanniniferous browse. Austr. J. Agric. Res. 52, 453-460.
81. Jouany, J.P., Demeyer, D.I. & Grain, J. (1988). Effect of defaunating the rumen. Anim. Feed Sci. Technol. 21, 229-265.
82. Kamler, J. (1999). Infusorial concentration in rumen fluid of red deer, fallow deer, roe deer and mouflon. Acta Vet. Brno 68, 247-252.
83. Kleynhans, C.J. & Van Hoven, W. (1976). Rumen protozoa of the giraffe with a description of two new species. East Afr. Wildl. J. 14, 203-214.
84. Kraschenninikow, S. (1955). Observations on the morphology and division of Eudiplodinium neglectum (Ciliata Entodiniomorpha) from the stomach of a moose (Alces americana). J. Protozool. 2, 124-134.
85. Kulkerni, V.D., Pant, H.C., Rai, G.S. & Rawat, J.S. (1971). The seasonal variation in the concentration of protozoa and Oscillospira guilliermondii organisms in the rumen fluid of grazing buffalo. Indian Vet. J. 48, 137-142.
86. Lanave, C., Preparata, G., Sacone, C. & Serio, G. (1984). A new method for calculating evolutionary substitution rates. J. Mol. Evol. 20, 86-93.
87. Lelkes, L. & Chang, C.L. (1987). Microbial dysbiosis in rabbit mucoid enteropathy. Lab. Anim. Sci. 37, 757-764.
88. Leng, R.A., Dellow, D. & Waghorn, G. (1986). Dynamics of large ciliate protozoa in the rumen of cattle fed on diets of freshly cut grass. Br. J. Nutr. 56, 455-462.
89. Leng, R.A., Gill, M., Kempton, T.J., Rowe, J.B., Nolan, J.V., Stachiw, S.J. & Preston, T.R. (1981). Kinetics of large ciliate protozoa in the rumen of cattle given sugar cane diets. Br. J. Nutr. 46, 371-384.
90. Levine, N.D. (Ed.) (1985). Ciliophora. In Veterinary protozoology: 334-364. Ames: Iowa State University Press.
91. Ley, R.E., Hamady, M., Lozupone, C., Turnbaugh, P.J., Ramey, R.R., Bircher, J.S., Schlegel, M.L., Tucker, T.A., Schrenzel, M.D., Knight, R. & Gordon, J.I. (2008). Evolution of mammals and their gut microbes. Science 320, 1647-1651.
92. Martins, E. (2004). COMPARE, version 4.6. Computer programs for the statistical analysis of comparative data. Bloomington: Department of Biology, Indiana University Distributed by the author at
93. Martins, E.P. & Hansen, T.F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into analysis of interspecific data. Am. Nat. 149, 646-667.
94. Moir, R.J. & Somers, M. (1956). A factor influencing the protozoal population in sheep. Nature 178, 1472.
95. Müller, K. (2010). Literaturübersicht zur Protozoenfauna im Vormagen von Wiederkäuern unter besonderer Berücksichtigung von Unterschieden zwischen den Äsungstypen. Zurich: Vetsuisse Faculty.
96. Nagaraja, T. & Towne, G. (1990). Ciliated protozoa in relation to ruminal acidosis and lactic acid metabolism. In The rumen ecosystem. 187-194. Hoshino, S., Onodera, R., Minato, H. & Itabashi, H. (Eds). Tokyo: Japan Scientific Societies Press.
97. Oshio, S. (1987). The effects of ratio of concentrate to roughage on the ciliate protozoa in the rumen heifers. Jpn. J. Zootech. Sci. 58, 36-43.
98. Owen-Smith, N. (1988). Megaherbivores - the influence of very large body size on ecology. Cambridge: Cambridge University Press.
99. Owen-Smith, N. (1997). Distinctive features of the nutritional ecology of browsing versus grazing ruminants. Z. Säugetierkd. 62 (Suppl. 2), 176-191.
100. Oxford, A.E. (1955). The bacteriology and protozoology of ruminant digestion. J. Sci. Food Agri. 6, 413-418.
101. Parra, R. (1978). Comparison of foregut and hindgut fermentation in herbivores. In The ecology of arboreal folivores: 205-230. Montgomery, G.G. (Ed.). Washington: Smithsonian Institution Press.
102. Pearson, H.A. (1965). Rumen organisms in white-tailed deer from South Texas. J. Wildl. Mgmt. 29, 493-496.
103. Pearson, H.A. (1969). Rumen microbial ecology in mule deer. Appl. Microbiol. 17, 819-824.
104. Pitra, C., Fickel, J., Meijaard, E. & Groves, P.C. (2004). Evolution and phylogeny of Old World deer. Mol. Phylogen. Evol. 33, 880-895.
105. Posada, D. (2008). jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253-1256.
106. Potter, E.L. & Dehority, B.A. (1973). Effects of changes in feed level, starvation, and level of feed after starvation upon the concentration of rumen protozoa in the ovine. Appl. Microbiol. 26, 692-698.
107. Prins, R.A. & Geelen, M.J.H. (1971). Rumen characteristics of red deer, fallow deer, and roe deer. J. Wildl. Mgmt. 35, 673-679.
108. Quinn, L.Y., Burroughs, W. & Christiansen, W.C. (1962). Continuous culture of ruminal microorganisms in chemically defined medium. II. Culture medium studies. Appl. Microbiol. 10, 583-592.
109. Robbins, C.T. (1993). Wildlife feeding and nutrition. San Diego: Academic Press.
110. Rodriguez, F., Oliver, J.F., Marin, A. & Medina, J.R. (1990). The general stochastic model of nucleotide substitution. J. Theor. Biol. 142, 485-501.
111. Rohlf, F. (2001). Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55, 2143-2160.
112. Rufener, H. Jr, Nelson, W.O. & Wolin, M.J. (1963). Maintenance of the rumen microbial population in continuous culture. Appl. Microbiol. 11, 196-201.
113. Schmidt, H.A., Strimmer, K., Vingron, M. & von Haeseler, A. (2002). TREEPUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502-504.
114. Silva, M. & Downing, J.A. (1995). CRC handbook of mammalian body masses. Bota Racon: CRC Press.
115. Singh, N., Iqbal, S. & Setia, M.S. (1993). Effect of diets on rumen ciliate protozoa in buffalo calves (Bubalus bubalis). Buffalo J. 9, 107-115.
116. Sládeček, F. (1946). Ophryoscolecidae from the stomach of Cervus elaphus, Dama dama, and Capreolus capreolus. Vestn. Cesk. Spol. Zool. 10, 201-231.
117. Slyter, L.L., Nelson, W.O. & Wolin, M.J. (1964). Modifications of a device for maintenance of the rumen microbial population in continuous culture. Appl. Microbiol. 12, 374-377.
118. Stevens, C.E. & Hume, I.D. (1998). Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Rev. 78, 393-427.
119. Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. Lect. Math. Life Sci. 17, 57-86.
120. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997). The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res. 15, 4876-4882.
121. Towne, G., Nagaraja, T.G., Brandt, R.T. Jr & Kemp, K.E. (1990a). Dynamics of ruminal ciliated protozoa in feedlot cattle. Appl. Environ. Microbiol. 56, 3174-3178.
122. Towne, G., Nagaraja, T.G., Brandt, R.T. Jr & Kemp, K.E. (1990b). Ruminal ciliated protozoa in cattle fed finishing diets with or without supplemental fat. J. Anim. Sci. 68, 2150-2155.
123. Towne, G., Nagaraja, T.G. & Kemp, K.K. (1988). Ruminal ciliated protozoa in bison. Appl. Environ. Microbiol. 54, 2733-2736.
124. Van Hoven, W. (1975). Rumen ciliates of the tsessebe (Damaliscus lunatus lunatus) in South Africa. J. Protozool. 22, 457-462.
125. Van Hoven, W. (1978). Development and seasonal changes in the rumen protozoan population in young blesbok (Damaliscus dorcasphillipsi). S. Afr. J. Wildl. Res. 8, 127-130.
126. Van Soest, P.J. (1994). Nutritional ecology of the ruminant, 2nd edn. Ithaca: Cornell University Press.
127. Van Wieren, S.E. (1996). Browsers and grazers: foraging strategies in ruminants. In Digestive strategies in ruminants and nonruminants: 119-146. Van Wieren, S.E. (Ed.). The Netherlands, University of Wageningen.
128. Varel, V.H. & Dehority, B.A. (1989). Ruminal cellulolytic bacteria and protozoa from bison, cattle-bison hybrids, and cattle fed three alfalfa-corn diets. Appl. Environ. Microbiol. 55, 148-153.
129. Weller, R. & Pilgrim, A. (1974). Passage of protozoa and volatile fatty acids from the rumen of the sheep and from a continuous in vitro fermentation system. Br. J. Nutr. 32, 341-351.
130. Wertheim, P. (1934). Ueber die Beschaffenheit der Infusorienmagenfauna von Capreolus capreolus. Zool. Anz. 106, 67-70.
131. Westerling, B. (1970). Rumen ciliate fauna of semi-domestic reindeer (Rangifer tarandus) in Finland: composition volume and some seasonal variation. Acta Zool. Fenn. 127, 1-76.
132. Wilkinson, R.C. & Van Hoven, W. (1976). Rumen ciliate fauna of the springbok (Antidorcas marsupialis) in southern africa. Zool. Afr. 11, 1-22.
133. Williams, A.G. (1986). Rumen holotrich ciliate protozoa. Microbiol. Rev. 50, 25-49.
134. Zielyk, M.W. (1961). Ophroscolecid fauna from the stomach of the white-tailed deer (Odocoileus virginianus borealis), and observations on the division of Entodinium dubardi (Ciliata Entodiniomorpha). J. Protozool. 8, 33-41.