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The Intraruminal Papillation Gradient in Wild Ruminants of Different Feeding Types: Implications for Rumen Physiology

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The Intraruminal Papillation Gradient in Wild Ruminants of Different Feeding Types: Implications for Rumen Physiology JOURNAL OF MORPHOLOGY 270:929–942 (2009) The Intraruminal Papillation Gradient in Wild Ruminants of Different Feeding Types: Implications for Rumen Physiology Marcus Clauss,1* Reinhold R. Hofmann,2 Jo¨ rns Fickel,2 W. Ju¨ rgen Streich,2 and Ju¨ rgen Hummel3 1Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland 2Research Group for Evolutionary Genetics, Leibniz-Institute for Zoo and Wildlife Research (IZW), Berlin, Germany 3Department of Animal Nutrition, Institute of Animal Science, University of Bonn, Bonn, Germany ABSTRACT Browsing and grazing ruminants are species between seasons (Hofmann, 1973; Langer, thought to differ in the degree their rumen contents are 1974; Ko¨nig et al., 1976; Hofmann, 1982; Hofmann stratified—which may be due to different characteristics and Schnorr, 1982; Hofmann, 1984, 1985; Smolle- of their respective forages, to particular adaptations of Wieszniewski, 1987; Hofmann et al., 1988a; Hofmann the animals, or both. However, this stratification is diffi- and Nygren, 1992; Josefsen et al., 1996; Forsyth and cult to measure in live animals. The papillation of the rumen has been suggested as an anatomical proxy for Fraser, 1999; Mathiesen et al., 2000; Kamler, 2001), stratification—with even papillation indicating homoge- or between free-ranging and captive individuals (Hof- nous contents, and uneven papillation (with few and mann and Matern, 1988; Marholdt, 1991; Hofmann small dorsal and ventral papillae, and prominent papil- and Nygren, 1992; Lentle et al., 1996). lae in the atrium ruminis) stratified contents. Using the Differences in the degree of papillation among surface enlargement factor (SEF, indicating how basal different rumen regions in the same animal have mucosa surface is increased by papillae) of over 55 rumi- been recognized for a long time in cattle, where nant species, we demonstrate that differences between especially the dorsal rumen wall completely lacks the SEFdorsal or SEFventral and the SEFatrium are signifi- papillae. In contrast, Martin and Schauder (1938) cantly related to the percentage of grass in the natural noted that the rumen of some deer species is diet. The more a species is adapted to grass, the more distinct this difference, with extreme grazers having evenly papillated. Differences in the papillation unpapillated dorsal and ventral mucosa. The relative among different rumen regions in different rumi- SEFdorsal as anatomical proxy for stratification, and the nant species were noted repeatedly (Garrod, 1877; difference in particle and fluid retention in the rumen as Langer, 1973), and put into a systematic perspec- physiological proxy for stratification, are highly corre- tive by Hofmann (1973), with extensive photo- lated in species (n 5 9) for which both kind of data are graphic documentation. Examples of papillation available. The results support the concept that the strat- extremes are given in Figure 1, where the rumina ification of rumen contents varies among ruminants, of roe deer (Capreolus capreolus), steenbok (Raphi- with more homogenous contents in the more browsing cerus campestris) and gerenuk (Litocranius wal- and more stratified contents in the more grazing species. leri) display a comparatively even papillation in all J. Morphol. 270:929–942, 2009. Ó 2009 Wiley-Liss, Inc. regions, whereas the rumina of hartebeest (Alcela- KEY WORDS: grazer; browser; rumen; rumen papillae; phus buselaphus), gemsbok (Oryx gazella) and surface enlargement factor reedbuck (Redunca redunca) show a papillation INTRODUCTION R. R. Hofmann is currently at: Trompeterhaus, 15837 Baruth/ Mark, Germany. In ruminants (Hofmann, 1969; Langer, 1973), hip- popotamids (Langer, 1975), and several rodent spe- Contract grant sponsor: German Wildlife Foundation (Deutsche cies (Vorontsov, 2003), the portion of the forestomach Wildtierstiftung e.V.). where bacterial fermentation occurs, and hence vola- *Correspondence to: Marcus Clauss, Clinic for Zoo Animals, tile fatty acids (VFA) are produced, is characterized Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, by an absorptive mucosa whose surface is consider- Winterthurerstr. 260, 8057 Zurich, Switzerland. ably enlarged by papillae. In ruminants, it was dem- E-mail: [email protected] onstrated that the development of these papillae is stimulated by the presence of VFA (Warner et al., Received 14 September 2008; Revised 17 December 2008; 1956; Sander et al., 1959; Sakata and Tamate, 1978, Accepted 19 December 2008 1979). Because VFA production is also a function of Published online 26 February 2009 in diet quality, the number and size of forestomach pap- Wiley InterScience (www.interscience.wiley.com) illae reflect variation in diet quality, e.g., within a DOI: 10.1002/jmor.10729 Ó 2009 WILEY-LISS, INC. 930 M. CLAUSS ET AL. Fig. 1. Papillation of the rumen (A: atrium ruminis, D: dorsal rumen, V: ventral rumen) of six ruminant species fixed in situ: on the left side, from top to bottom, the browsers roe deer (Capreolus capreolus), steenbok (Raphicerus campestris; rod indicating the cardia) and gerenuk (Litocranius walleri) show a comparatively even papillation in all regions of the rumen; on the right side, from top to bottom, hartebeest (Alcelaphus buselaphus), gemsbock (Oryx gazella) and reedbock (Redunca redunca) show an uneven ruminal papillation, with large papillae in the atrium and smaller papillae and even unpapillated areas in the dorsal or ventral rumen. Magnification adapted for qualitative comparison; historical photographs, no scale bars available (from Hofmann, 1969; Hofmann et al., 1976; Hofmann and Schnorr, 1982). anterior 5 left side of photographs. that is distinct in the Atrium ruminis and around cific ruminal areas, such as the dorsal rumen wall, the Ostium intraruminale (i.e., in the middle the atrium, or the ventral rumen wall, reflect dif- rumen layer), less distinct towards the more dorsal ferences in the degree of ingesta stratification in and ventral layers, and even completely absent in the rumen (Hofmann, 1973; Langer, 1974; Hof- the most dorsal and ventral regions. It has been mann, 1989; Josefsen et al., 1996; Mathiesen proposed that differences in the papillation of spe- et al., 2000). Actually, differences the stratification Journal of Morphology PAPILLATION PATTERNS IN RUMINANTS 931 of rumen contents have been found in parallel to 2008a; Schwarm et al., 2008), and has been pro- differences in papillation in several wild ruminant posed to be a major driver of particular anatomical species (Clauss et al., 2009, in press). adaptations in grazers, such as strong rumen pil- In cattle and other grazing ruminants, the lars (Clauss et al., 2003) and large omasa (Clauss rumen contents are stratified, with a distinct gas et al., 2006a). dome of CO2 and methane above the ‘‘fiber mat,’’ However, the presence or absence of a rumen which itself floats on the liquid layer, at the very contents stratification is actually difficult to inves- bottom of which very dense, fine sedimented par- tigate in live animals. Recently, the use of ultraso- ticles form a ‘‘sludge’’ layer (Grau, 1955; Capote nography has been shown to facilitate the differen- and Hentges, 1967; Hofmann, 1973; Tschuor and tiation between a gas dome and a fiber mat in the Clauss, 2008; Hummel et al., in press). In con- rumen of cattle, and allowed to demonstrate the trast, the rumen contents of several browsing spe- absence of a gas dome in a browse-fed captive cies anecdotally appeared rather homogenous, moose (Tschuor and Clauss, 2008), but this tech- ‘‘frothy,’’ without a distinct separation of gas, par- nique has obvious limitations in terms of applic- ticles, fluids, and sludge (Hofmann, 1969, 1973; ability over a wide range of species; the same is Nygren and Hofmann, 1990; Renecker and Hud- true for comparative measurements of fluid and son, 1990; Clauss et al., 2001). As papillation particle passage through the gastrointestinal tract. growth is induced by VFA, the presence of a dor- In contrast, using the rumen mucosa papillation sal gas dome and a ventral sludge layer could pre- as a surrogate measure for the stratification of the vent papillae formation in these locations, rumen contents is an attractive alternative. The because gas and sludge will displace any VFA papillation of a certain rumen region can be easily that could accumulate in these regions. Actually, quantified by the use of the ‘‘surface enlargement differences in VFA content between different factor’’ (SEF; Schnorr and Vollmerhaus, 1967), rumen ingesta layers have been measured in which represents the factor by which the absorp- domestic cattle (Smith et al., 1956; Tafaj et al., tive surface of the rumen mucosa is increased due 2004). In contrast, in homogenous rumen con- to the papillae in comparison to the basal rumen tents, VFA can be assumed to be relatively evenly area; an unpapillated region of the rumen, thus, distributed throughout the ingesta, leading to an has a SEF of 1.0. For rumen contents stratifica- even ruminal papillation. tion, three rumen regions are of particular inter- Hofmann (1969, 1973, 1989) first proposed that est: the atrium ruminis which usually shows the the difference in rumen contents stratification was most distinct papillae development and hence the one of many differences between grazing and highest SEF (Hofmann, 1973; Langer, 1973), and browsing ruminants. When comparing different both the dorsal and the ventral rumen wall. The ruminant species according to the macroscopic difference between
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