The Intraruminal Papillation Gradient in Wild Ruminants of ...faculty.weber.edu/rmeyers/CVA/Ruminant...

The Intraruminal Papillation Gradient in WildRuminants of Different Feeding Types: Implicationsfor Rumen Physiology

Marcus Clauss,1* Reinhold R. Hofmann,2 Jörns Fickel,2 W. Jürgen Streich,2 and Jürgen Hummel3

1Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland2Research Group for Evolutionary Genetics, Leibniz-Institute for Zoo and Wildlife Research (IZW), Berlin, Germany3Department of Animal Nutrition, Institute of Animal Science, University of Bonn, Bonn, Germany

ABSTRACT Browsing and grazing ruminants arethought to differ in the degree their rumen contents arestratified—which may be due to different characteristicsof their respective forages, to particular adaptations ofthe animals, or both. However, this stratification is diffi-cult to measure in live animals. The papillation of therumen has been suggested as an anatomical proxy forstratification—with even papillation indicating homoge-nous contents, and uneven papillation (with few andsmall dorsal and ventral papillae, and prominent papil-lae in the atrium ruminis) stratified contents. Using thesurface enlargement factor (SEF, indicating how basalmucosa surface is increased by papillae) of over 55 rumi-nant species, we demonstrate that differences betweenthe SEFdorsal or SEFventral and the SEFatrium are signifi-cantly related to the percentage of grass in the naturaldiet. The more a species is adapted to grass, the moredistinct this difference, with extreme grazers havingunpapillated dorsal and ventral mucosa. The relativeSEFdorsal as anatomical proxy for stratification, and thedifference in particle and fluid retention in the rumen asphysiological proxy for stratification, are highly corre-lated in species (n 5 9) for which both kind of data areavailable. The results support the concept that the strat-ification of rumen contents varies among ruminants,with more homogenous contents in the more browsingand more stratified contents in the more grazing species.J. Morphol. 270:929–942, 2009. � 2009 Wiley-Liss, Inc.

KEY WORDS: grazer; browser; rumen; rumen papillae;surface enlargement factor

INTRODUCTION

In ruminants (Hofmann, 1969; Langer, 1973), hip-popotamids (Langer, 1975), and several rodent spe-cies (Vorontsov, 2003), the portion of the forestomachwhere bacterial fermentation occurs, and hence vola-tile fatty acids (VFA) are produced, is characterizedby an absorptive mucosa whose surface is consider-ably enlarged by papillae. In ruminants, it was dem-onstrated that the development of these papillae isstimulated by the presence of VFA (Warner et al.,1956; Sander et al., 1959; Sakata and Tamate, 1978,1979). Because VFA production is also a function ofdiet quality, the number and size of forestomach pap-illae reflect variation in diet quality, e.g., within a

species between seasons (Hofmann, 1973; Langer,1974; König et al., 1976; Hofmann, 1982; Hofmannand Schnorr, 1982; Hofmann, 1984, 1985; Smolle-Wieszniewski, 1987; Hofmann et al., 1988a; Hofmannand Nygren, 1992; Josefsen et al., 1996; Forsyth andFraser, 1999; Mathiesen et al., 2000; Kamler, 2001),or between free-ranging and captive individuals (Hof-mann and Matern, 1988; Marholdt, 1991; Hofmannand Nygren, 1992; Lentle et al., 1996).

Differences in the degree of papillation amongdifferent rumen regions in the same animal havebeen recognized for a long time in cattle, whereespecially the dorsal rumen wall completely lackspapillae. In contrast, Martin and Schauder (1938)noted that the rumen of some deer species isevenly papillated. Differences in the papillationamong different rumen regions in different rumi-nant species were noted repeatedly (Garrod, 1877;Langer, 1973), and put into a systematic perspec-tive by Hofmann (1973), with extensive photo-graphic documentation. Examples of papillationextremes are given in Figure 1, where the ruminaof roe deer (Capreolus capreolus), steenbok (Raphi-cerus campestris) and gerenuk (Litocranius wal-leri) display a comparatively even papillation in allregions, whereas the rumina of hartebeest (Alcela-phus buselaphus), gemsbok (Oryx gazella) andreedbuck (Redunca redunca) show a papillation

R. R. Hofmann is currently at: Trompeterhaus, 15837 Baruth/Mark, Germany.

Contract grant sponsor: German Wildlife Foundation (DeutscheWildtierstiftung e.V.).

*Correspondence to: Marcus Clauss, Clinic for Zoo Animals,Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich,Winterthurerstr. 260, 8057 Zurich, Switzerland.E-mail: [email protected]

Received 14 September 2008; Revised 17 December 2008;Accepted 19 December 2008

Published online 26 February 2009 inWiley InterScience (www.interscience.wiley.com)DOI: 10.1002/jmor.10729

JOURNAL OF MORPHOLOGY 270:929–942 (2009)

� 2009 WILEY-LISS, INC.

that is distinct in the Atrium ruminis and aroundthe Ostium intraruminale (i.e., in the middlerumen layer), less distinct towards the more dorsaland ventral layers, and even completely absent inthe most dorsal and ventral regions. It has beenproposed that differences in the papillation of spe-

cific ruminal areas, such as the dorsal rumen wall,the atrium, or the ventral rumen wall, reflect dif-ferences in the degree of ingesta stratification inthe rumen (Hofmann, 1973; Langer, 1974; Hof-mann, 1989; Josefsen et al., 1996; Mathiesenet al., 2000). Actually, differences the stratification

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 indicatingthe 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 unevenruminal papillation, with large papillae in the atrium and smaller papillae and even unpapillated areas in the dorsal or ventralrumen. 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.

930 M. CLAUSS ET AL.

Journal of Morphology

of rumen contents have been found in parallel todifferences in papillation in several wild ruminantspecies (Clauss et al., 2009, in press).

In cattle and other grazing ruminants, therumen contents are stratified, with a distinct gasdome of CO2 and methane above the ‘‘fiber mat,’’which itself floats on the liquid layer, at the verybottom of which very dense, fine sedimented par-ticles form a ‘‘sludge’’ layer (Grau, 1955; Capoteand Hentges, 1967; Hofmann, 1973; Tschuor andClauss, 2008; Hummel et al., in press). In con-trast, the rumen contents of several browsing spe-cies anecdotally appeared rather homogenous,‘‘frothy,’’ without a distinct separation of gas, par-ticles, fluids, and sludge (Hofmann, 1969, 1973;Nygren and Hofmann, 1990; Renecker and Hud-son, 1990; Clauss et al., 2001). As papillationgrowth is induced by VFA, the presence of a dor-sal gas dome and a ventral sludge layer could pre-vent papillae formation in these locations,because gas and sludge will displace any VFAthat could accumulate in these regions. Actually,differences in VFA content between differentrumen ingesta layers have been measured indomestic cattle (Smith et al., 1956; Tafaj et al.,2004). In contrast, in homogenous rumen con-tents, VFA can be assumed to be relatively evenlydistributed throughout the ingesta, leading to aneven ruminal papillation.

Hofmann (1969, 1973, 1989) first proposed thatthe difference in rumen contents stratification wasone of many differences between grazing andbrowsing ruminants. When comparing differentruminant species according to the macroscopicappearance of their mucosa of ruminal regionssuch as the dorsal rumen, the atrium and the ven-tral rumen (Fig. 2), it is evident that in speciesincreasingly specialized in grass forage, the differ-ences among the rumen regions become morepronounced. The stratification of rumen contentsaccording to updrift and sedimentation into a ‘fibermat’ with the larger, lighter particles above a fluidphase containing the smaller, denser particles, isregarded as the main mechanism responsible forthe sorting of particles in the reticulorumen indomestic ruminants (Sutherland, 1988; Beaumontand Deswysen, 1991; Lechner-Doll et al., 1991b;Dardillat and Baumont, 1992; Kaske et al., 1992).Additionally, the continuous mixing of the rumencontents, which forces small particles through thefiber mat, where they may also be retained (the‘filter bed effect’) (Poppi et al., 2001; Faichney,2006) is also considered an important mechanismresponsible for the selective particle retention inthis organ. A well-developed stratification (with anaccording filter-bed effect) was suggested to causethe differential outflow of fluids and particles ingrazing wild ruminant species (Clauss and Lech-ner-Doll, 2001; Behrend et al., 2004; Hummelet al., 2005; Clauss et al., 2006b; Hummel et al.,

2008a; Schwarm et al., 2008), and has been pro-posed to be a major driver of particular anatomicaladaptations in grazers, such as strong rumen pil-lars (Clauss et al., 2003) and large omasa (Clausset al., 2006a).

However, the presence or absence of a rumencontents stratification is actually difficult to inves-tigate in live animals. Recently, the use of ultraso-nography has been shown to facilitate the differen-tiation between a gas dome and a fiber mat in therumen of cattle, and allowed to demonstrate theabsence of a gas dome in a browse-fed captivemoose (Tschuor and Clauss, 2008), but this tech-nique has obvious limitations in terms of applic-ability over a wide range of species; the same istrue for comparative measurements of fluid andparticle passage through the gastrointestinal tract.In contrast, using the rumen mucosa papillationas a surrogate measure for the stratification of therumen contents is an attractive alternative. Thepapillation of a certain rumen region can be easilyquantified by the use of the ‘‘surface enlargementfactor’’ (SEF; Schnorr and Vollmerhaus, 1967),which represents the factor by which the absorp-tive surface of the rumen mucosa is increased dueto the papillae in comparison to the basal rumenarea; an unpapillated region of the rumen, thus,has a SEF of 1.0. For rumen contents stratifica-tion, three rumen regions are of particular inter-est: the atrium ruminis which usually shows themost distinct papillae development and hence thehighest SEF (Hofmann, 1973; Langer, 1973), andboth the dorsal and the ventral rumen wall. Thedifference between either the dorsal or the ventralrumen wall SEF and the SEF of the atrium rumi-nis thus becomes, in theory, a measure of thedegree of rumen contents stratification, with asmall difference indicating homogenous, and alarge difference comparatively stratified rumencontents.

For this contribution, published SEF data forthese three rumen regions were collated from theliterature, and supplemented with hitherto unpub-lished data of the second author (RRH). The fol-lowing predictions were made

1. There is no correlation between body mass(BM) and the SEF of the atrium ruminis, thedorsal or the ventral rumen wall, because theSEF is a measure of diet quality, which we didnot assume to be correlated to BM in such abroad-scale data collection.

2. There is a negative correlation of both the abso-lute SEF of the dorsal and the ventral rumenwall, as well as of the relative SEF of theseregions (in % of the Atrium ruminis SEF), withthe percentage of grass (%grass) in the naturaldiet of the respective species, indicating anincrease in rumen contents stratification withincreasing adaptation to a grass diet.

PAPILLATION PATTERNS IN RUMINANTS 931


3. There is a positive correlation between the rela-tive SEF (in % of the Atrium SEF) of the dorsaland the ventral rumen wall, indicating that themechanism responsible for rumen contentsstratification is effective throughout the wholerumen.

4. There is a negative correlation between the rel-ative SEF (in % of the Atrium SEF) of the dor-sal rumen wall, as an anatomical measure ofrumen contents stratification, and the selectiveparticle retention (as compared to the fluidretention) in the reticulorumen (Clauss et al.,2006b) as a physiological measure; in otherwords, the more the rumen mucosa reflects con-tents stratification, the larger the differencebetween fluid and particle passage from therumen in the same species.

METHODS

The SEF is calculated as the sum of surface of the papillaeand the basal area divided by the basal area. Data on the SEFof the dorsal rumen wall, the ventral rumen wall, and theatrium ruminis were collated from both the literature and hith-erto unpublished observations. When data was available fromboth the literature and the second author, data from the secondauthor was preferred for a maximum of data consistency. Forthis data collection, only measurements from free-ranging ani-mals were used, because the diets fed in captivity may lead to

important changes in the ruminal mucosa papillation (Hofmannand Matern, 1988; Marholdt, 1991). The only exception wereanimals kept in a semi-natural setting on large pastures fromWhipsnade Wild Animal Park, such as Chinese water deer (Hof-mann et al., 1988a), Père David’s deer, axis deer, hog deer,blackbuck, and nilgai. The SEF measurements were performedon formalin-fixed samples by counting the number of papillaefor a given basal area, and measuring their height and width,as described in the literature (Hofmann, 1973; Langer, 1973).When data on BM were available, it was directly taken fromthe sources; if only SEF but no BM data was available, BMdata was taken from Clauss et al. (2002). All data representmeans calculated on the basis of individual measurements, or,in the case of many publications, on the basis of average valuesper season. The number of individuals investigated per speciesis given in Table 1.

As in more recent evaluations of the influence of adaptationto the natural diet in ruminants (Clauss et al., 2008a), the per-centage of grass in the natural diet (%grass) was used to char-acterize species on a continuous scale. The bulk of the respec-tive data was taken from Van Wieren (1996) and from the datacollection that formed the basis of Owen-Smith [(1997), datakindly provided by the author], which were supplemented byseveral other publications (Table 1). Whenever seasonal datawas available, the %grass used to characterize a species repre-sents the mean of the values from different seasons. It shouldbe noted that this literature data was collated using a varietyof sources and methods, and does not represent the actual dietingested by the individuals measured in this study.

Data on the ratio between the mean retention time of par-ticles: fluids in the reticulorumen were taken from Clauss et al.(2006b). Data for both papillation and this ratio were availablefor cattle, sheep, goat, giraffe, moose, roe deer, wapiti, ibex, andmouflon.

Fig. 2. Samples of mucosa from the dorsal rumen (top set), the atrium ruminis (middle set), and the ventral rumen (bottom set)of nine ruminant species (Giraffidae: Giraffe Giraffa camelopardalis; Cervidae: White-tailed deer Odocoileus virginianus, Fallowdeer Dama dama, Père David’s deer Elaphurus davidianus; Bovidae: Bushbuck Tragelaphus scriptus, Thomson gazelle Gazellathomsoni, Goat Capra hircus, Blackbuck Antilope cervicapra, African buffalo Syncerus caffer). Note that although the atrium rumi-nis is always heavily papillated, papillation of the dorsal and ventral wall appears to decrease from the browsing species (left) tothe intermediate feeders (center) and the grazers (right). Magnification adapted for qualitative comparison: magnification was keptconstant within but not between species; apparent differences in papilla size between species do not necessarily reflect real size dif-ferences; historical photographs, no scale bars available (from Hofmann, 1973; Hofmann et al., 2005; and previously unpubl. photo-graphs).



TABLE 1. Mean body mass (BM) and surface enlargement factors of ruminant species of different feeding type collatedfrom different sources, and an estimation of the percentage of grass (% grass) in the natural diet of the species

according to literature sources

SpeciesBM(kg)

SEFSEF in %atrium

Source%

Grass SourceDorsal Ventral Atrium Dorsal Ventral

Impala Aepyceros melampus 55 3.9 5.0 15.3 25 32 A (25) 60.0 1Hartebeest Alcelaphus buselaphus 174 1.0 1.8 19.0 5 9 A (9) 96.7 2Moose Alces alces 258 9.6 9.5 15.3 63 62 J (25) 2.0 1Springbok Antidorcas marsupialis 41 2.6 3.0 14.8 17 20 K (7) 30.0 4Pronghorn Antilocapra americana 40 4.5 5.2 9.0 50 58 B (2) 15.0 1Blackbuck Antilope cervicapra 33 1.7 2.3 6.3 27 37 B (1) 75.0 1Axis deer Axis axis 85 1.5 1.9 7.0 22 27 B (2) 70.0 1Hog deer Axis porcinus 45 1.9 3.1 6.0 32 52 B (1) 50.0 5Bison Bison bison 335 1.0 2.1 15.9 6 13 B (1) 84.0 1Cattle Bos taurus 600 1.0 1.5 14.2 7 11 L (1) 79.0 2Nilgai Boselaphus tragocamelus 220 2.4 2.6 8.8 28 30 B (3) 59.5 2Domestic goat Capra hircus 31 2.5 2.6 6.7 37 38 H (53) 28.0 1Alpine ibex Capra ibex 60 3.1 3.7 14.7 21 25 B (1) 60.0 1Roe deer Capreolus capreolus 25 6.2 6.5 9.0 69 72 C, D, E,

F (58)9.0 1

Serau Capricornis crispus 37 3.6 3.6 12.5 29 29 O (10) 70.0 1Red duiker Cephalophus harveyi 16 4.5 7.5 11.0 41 68 A (2) 1.0 3Red deer Cervus elaphus 170 3.7 3.7 19.0 19 19 C (12) 47.0 1Wapiti Cervus elaphus canadensis 300 2.9 3.4 8.8 33 39 B (1) 64.0 1Sika deer Cervus nippon 70 1.9 3.3 12.6 15 26 B (14) 50.0 1Sambar Cervus unicolor 200 4.0 4.7 14.8 27 32 M (12) 45.0 1Wildebeest Connochaetes taurinus 182 1.0 7.5 36.5 3 21 A (5) 90.0 1Fallow deer Dama dama 60 2.4 4.3 16.2 15 27 G (11) 46.0 1Tsessebe Damaliscus lunatus 119 1.0 1.0 16.0 6 6 A (5) 99.3 2Pere Davids Deer Elaphurus davidianus 120 1.2 2.3 13.3 9 17 B (3) 75.0 7Grant’s gazelle Gazella granti 55 3.7 5.5 20.0 19 28 A (13) 50.0 1Thomson’s gazelle Gazella thomsoni 21 2.5 2.5 16.5 15 15 A (15) 85.5 2Giraffe Giraffa camelopardalis 750 24.0 18.0 30.0 80 60 A (4) 0.2 2Himalayan tahr Hemitragus jemlahicus 55 2.5 3.0 9.9 25 30 P (39) 75.0 8Chinese water deer Hydropotes inermis 11 3.3 3.7 6.7 50 55 I (58) 50.0 7Waterbuck Kobus ellipsiprymnus 201 1.0 1.0 32.0 3 3 A (5) 80.0 2Uganda kob Kobus kob 79 1.0 1.0 19.0 5 5 A (5) 95.0 9Gerenuk Litocranius walleri 43 7.5 12.0 19.0 39 63 A (8) 0.0 2Günther’s dikdik Madoqua guentheri 4 7.5 16.5 19.0 39 87 A (6) 5.0 10Kirk’s dikdik Madoqua kirki 5 6.5 12.5 17.5 37 71 A (6) 17.0 3Muntjac Muntiacus reveesi 15 4.5 4.8 6.9 65 69 N (33) 10.0 1Suni Neotragus moschatus 6 7.3 9.0 11.5 63 78 A (4) 0.0 6Mule deer Odocoileus hemionus 80 5.1 6.9 10.7 48 65 B (4) 11.0 1White-tailed deer Odocoileus virginianus 70 4.0 4.6 7.0 57 65 B (3) 9.0 1Klipspringer Oreotragus oreotragus 11 10.5 10.0 17.5 60 57 A (3) 5.0 1Beisa oryx Oryx beisa 145 1.7 2.5 11.0 16 23 B (2) 83.0 12Gemsbok Oryx gazella 182 1.0 1.5 12.5 8 12 A (3) 82.0 2Oribi Ourebia ourebi 16 1.0 — 15.0 7 — A (5) 48.5 2Sheep Ovis ammon domesticus 31 2.1 2.2 6.5 33 34 H (14) 50.0 1Mouflon Ovis ammon musimon 40 2.6 3.5 8.6 30 41 G (10) 69.0 11Dall’s sheep Ovis dalli dalli 56 2.2 6.1 19.4 11 32 B (2) 56.0 1Mongolian gazelle Procapra gutturosa 29 4.2 4.5 15.5 27 29 R (38) 28.0 13Reindeer Rangifer tarandus 62 9.5 11.6 9.5 99 122 Q (36) 36.0 1Steenbok Raphicerus campestris 11 6.0 6.0 18.0 33 33 A (18) 10.0 1Mountain reedbuck Redunca fulvolufula 24 1.0 1.0 16.0 6 6 A (6) 99.0 2Bohor Reedbuck Redunca redunca 45 1.0 1.0 20.0 5 5 A (3) 80.0 1Barasingha Rucervus duvauceli 200 1.7 2.4 9.0 19 26 B (2) 80.0 1Chamois Rupicapra rupicapra 50 3.5 4.3 15.5 22 28 B (16) 74.0 1Grey duiker Sylvicapra grimmia 14 11.0 11.0 23.5 47 47 A (6) 5.0 2African buffalo Syncerus caffer 599 1.0 2.0 35.0 3 6 A (4) 90.0 1Eland Taurotragus oryx 465 3.8 8.0 35.0 11 23 A (4) 50.0 3Bongo Tragelaphus euryceros 250 4.1 — 11.1 37 — B (3) 20.0 14Lesser Kudu Tragelaphus imberbis 91 8.0 9.5 31.0 26 31 A (4) 10.0 2Bushbuck Tragelaphus scriptus 50 7.0 9.0 24.5 29 37 A (4) 10.0 1Greater Kudu Tragelaphus strepsiceros 214 9.0 13.5 40.0 23 34 A (3) 5.0 1

Sources for SEF data (number of individuals investigated in parentheses): A, (Hofmann, 1973); B, (Hofmann, unpubl.); C, (Hof-mann et al., 1976); D, (König et al., 1976); E, (Hofmann et al., 1988b); F, (Wen-Jun and Hofmann, 1991); G, (Geiger et al., 1977);H, (Hofmann et al., 1987); I, (Hofmann et al., 1988a); J, (Hofmann and Nygren, 1992); K, (Hofmann et al., 1995); L, (Schnorr andVollmerhaus, 1967); M, (Stafford, 1995); N, (Pfeiffer, 1993); O, (Jiang, 1998); P, (Forsyth and Fraser, 1999); Q, (Mathiesen et al.,2000); R, (Jiang et al., 2003).Sources for %grass data: 1, (Van Wieren, 1996); 2, (Owen-Smith, 1997); 3, (Gagnon and Chew, 2000); 4, (Bigalke, 1972); 5, (Dhungeland O’Gara, 1991); 6, (Heinichen, 1972); 7, (Geist, 1999); 8, (Schaller, 1973); 9, (Field, 1972); 10, (Hofmann and Stewart, 1972); 11,(Stubbe, 1971); 12, (Skinner and Chimimba, 2005); 13, (Campos-Arceiz et al., 2004); 14 (Kingdon, 1982).

Relationships among species were inferred from a phyloge-netic tree based on the complete mitochondrial cytochrome bgene. Respective DNA sequences were available from GenBank(http://www.ncbi.nlm.nih.gov) for all ruminant species investi-gated (except for Gazella thomsoni, which was therefore omittedfrom the analyses). Sequences were aligned using CLUSTALX(Thompson et al., 1997), visually controlled and trimmed toidentical lengths (1,143 bp). To select the best-fitting nucleotidesubstitution model for the data, a combination of the softwarepackages PAUP* (v.4.b10; Swofford, 2002) and MODELTEST(v.3.7; Posada and Crandall, 1998) was used. Analysis wasbased on a hierarchical likelihood ratio test approach imple-mented in MODELTEST. The model selected was the generaltime-reversible (GTR) model (Lanave et al., 1984; Tavaré, 1986)with an allowance both for invariant sites (I) and a gamma (G)distribution shape parameter (a) for among-site rate variation(GTR1I1G) (Rodriguez et al., 1990). The nucleotide substitu-tion rate matrix for the GTR1I1G model was similarly calcu-lated using MODELTEST. Parameter values for the modelselected were: -lnL 5 15642.5273, I 5 0.4613, and a 5 0.8093(eight gamma rate categories). The phylogenetic reconstructionbased on these parameters was then performed using the maxi-mum likelihood (ML) method implemented in TREEPUZZLE(v.5.2; Schmidt et al., 2002). Support for nodes was assessed bya reliability percentage after 100,000 quartet puzzling steps;only nodes with more than 50% support were retained. Theresulting tree is displayed in Figure 3. The basal polytomy forfamilial relationships (Bovidae, Cervidae, Giraffidae and Antilo-capridae) was resolved assuming it to be a soft polytomy (Purvisand Garland, 1993). To meet the input requirements for thephylogenetic analysis implemented in the COMPARE 4.6 pro-gram (Martins, 2004), we resolved the remaining polytomies tofull tree dichotomy by introducing extreme short branch lengths(l 5 0.00001) at multifurcating nodes. Taxa grouping in thebifurcating process followed the phylogenies proposed by Pitraet al. (2004) for Cervidae and by Fernandez and Vrba (2005) forall other taxa.The subjects of the comparative analyses were individual spe-

cies, each characterized by its respective SEF as describedabove. To achieve normal data distribution, data for BM,SEFdorsal, SEFatrium and SEFventral were ln-transformed. Statis-tical analyses were performed with and without accounting forphylogeny, to test for the validity of a general, functionalhypothesis, and to then discriminate between convergent adap-tation and adaptation by descent. Data were analyzed by corre-lation and partial correlation analysis (controlling for theinfluence of body mass). To additionally include phylogeneticinformation, we used the Phylogenetic Generalized Least-Squares approach (Martins and Hansen, 1997; Rohlf, 2001) inwhich a well-developed standard statistical method wasextended to enable the inclusion of interdependencies amongspecies due to the evolutionary process. To test the robustnessof the results, the comparative analysis was performed for botha set of phylogenetic trees involving branch lengths (tree 1) andanother set with equal branch lengths (tree 2). As there wereno relevant differences in the results, only the tests using tree1 are given here. The COMPARE 4.6 program (Martins, 2004)served for the phylogenetically controlled calculations. Theother statistical calculations were performed with the SPSS12.0 software (SPSS, Chicago, IL). The significance level wasset to a 5 0.05.

RESULTS

In this dataset, there was a significant, positivecorrelation between body mass and %grass in thenatural diet (Table 2). On average, grazing rumi-nants are larger than browsing ruminants (Bell,1971; Case, 1979; Bodmer, 1990; Van Wieren,1996; Pérez-Barberı̀a and Gordon, 2001), but corre-lations between BM and the proportion of grass in

the natural diet are usually not found (Van Wie-ren, 1996; Clauss et al., 2003; Sponheimer et al.,2003) or very weak (Gagnon and Chew, 2000),because browsers are found across the body sizerange (Sponheimer et al., 2003). In our case, thesignificance was retained even if phylogeny wastaken into account (Table 2).

There were significant correlations between BMand all parameters investigated (Table 2). Signifi-cant correlations were also evident for %grass withall parameters except SEFatrium. Similarly, VanWieren (1996) already had not found a significantcorrelation between %grass and the SEFatrium.Phylogenetic control generally did not change theresults (Table 2). Correlations of %grass with SEFparameters generally had markedly higher corre-lation coefficients than the rather weak correla-tions with BM (Table 2; compare Fig. 4a–d). Thereindeer (Rangifer tarandus) was an evident out-lier to the general pattern, showing an unusuallyhigh degree of papillae uniformity in its rumen forits feeding type as intermediate feeder.

Partial correlations (controlling for BM) between%grass and SEF parameters (except SEFatrium)were highly significant (Table 2), indicating thatthe correlations between %grass and the SEF pa-rameters were not caused by a mediating effect ofBM. The relative SEFdorsal and the SEFventral (in %of the SEF of the atrium) were positively corre-lated to each other (Fig. 4e), with a generallyhigher value (by 6% of the SEFatrium) in the rela-tive SEFventral (raw data: R 5 0.909, P < 0.001;phylogenetically controlled: R 5 0.857, P < 0.001;n 5 56). The three species that appeared to devi-ate the most from this pattern were the giraffe,with a higher relative SEFdorsal, and the two dik-dik species (Madoqua guentheri and M. kirki), inwhich the relative SEFdorsal was disproportionatelylower than the relative SEFventral.

Among the few species (n 5 9) for which com-parative data on both the relative SEFdorsal andthe passage characteristics (SF 5 selectivity factor,mean retention time of particles/mean retentiontime of fluids in the reticulorumen) were available,there was a significant, negative correlationbetween these parameters both for the raw data(R 5 20.917, P < 0.001) and the phylogeneticallycontrolled test (R 5 20.922, P < 0.001) (Fig. 4f).

DISCUSSION

In general, the hypotheses concerning the corre-lation of the patterns of the ruminal papillationwith the %grass in the natural diet were con-firmed. If the ruminal papillation pattern isaccepted as a proxy for the stratification of rumencontents, the results therefore indicate that thecontents of more grazing wild ruminants tend tobe more stratified than those of more browsingruminants.



Large interspecific comparisons such as this oneare, by necessity, limited by certain factors thatneed to be stated: The data on the natural dietcomposition was not generated from the same ani-mals, or not even the same animal populations,that were used for the papillation measurements;the same limitation applies to the use of bodyweight data derived from other individuals.Whether the habitat from which the individualsused for this study were taken was representativefor the ‘‘typical’’ habitat of the species could not beassessed. The fact that papillation characteristicsas well as the natural diet are subject to seasonalvariation could have introduced a source of inac-

curacy in the results of our analysis. Finally, dif-ferences in the handling of rumen samples (mea-surements on fresh samples or after storage in for-malin of varying concentrations) will influence theresults (Lentle et al., 1997). Some of these varia-tions may have been attenuated by the use ofratios (SEF dorsal in % of SEF atrium). However,our study was not concerned with the detailedpositioning of individual species in the comparison,but with a broad general pattern that is clearlyevident across the wide range of species fromdifferent taxonomic groups.

The results confirm that the rumen contents offree-ranging wild ruminants induce a more pro-

Fig. 3. Fifty percent majority rulemaximum likelihood tree (100,000puzzling steps), depicting the phyloge-netic relationships among completemitochondrial cytochrome b sequencesfrom 58-ruminant taxa as used in thephylogenetically controlled statisticsin this study (accession codes fromGenBank available at: http://www.ncbi.nlm.nih.gov). The families of theGiraffidae, Antilocapridae, Cervidae,and Bovidae (from Hippotraginae toBovinae) are represented.



TABLE 2. Results of statistical analyses for correlations and partial correlations (controlling for body mass) between the surfaceenlargement factors (SEF) of different areas of the rumen mucosa, the proportion of grass (%grass) in the natural diet, and body

mass, using either raw data from Table 1 or phylogenetically controlled statistics

%Grass SEFdorsal SEFventral SEFatrium SEFdorsal (% SEFatrium) SEFventral (% SEFatrium)

n 58 58 56 58 58 56Raw data

Body mass R 0.401 20.281 20.281 0.289 20.323 20.487P 0.002 0.032 0.036 0.028 0.013

nounced difference in the intraruminal papillationpattern in those species that are characterized by ahigher proportion of grass in their natural diet. Inaddition to the quantitative findings collated in thisstudy, there are qualitative observations on addi-tional species that are in accord with the patternobserved here. For example, Agungpriyono et al.(1992) observed that the rumen of the lesser mouse-deer (Tragulus javanicus) was completely evenlypapillated, and Clauss et al. (2006c) observed thesame in captive okapi (Okapia johnstoni). Both spe-cies are known to avoid grass consumption in thewild (Nordin, 1978; Hart and Hart, 1988). In con-trast, the rumen of three more recently domesti-cated bovini, the gaur (Bos frontalis), the yak (Bosgrunniens) and the zebu (Bos indicus) were reportedto resemble that of domestic cattle (Sarma et al.,1996), presumably indicating an absence of papillaein the dorsal area. Similar observations were madein other bovini such as water buffalo (Bubalus buba-lis) (Hemmoda and Berg, 1980), lowland anoa(Bubalus depressicornis) (Clauss et al., 2008b), ban-teng (Bos javanicus) and European bison (Bisonbonasus) (Clauss, pers. obs.), the puku (Kobus var-doni) (Stafford and Stafford, 1990) and the lechwe(Kobus leche) (Stafford and Stafford, 1991). All theseanimals are assumed to ingest high proportions ofgrass in their natural diet. Similar to our study,Enzinger and Hartfiel (1998) demonstrated quanti-tatively that the rumen mucosa of captive roe deerwas evenly papillated, in contrast to that of fallowdeer, sheep and goats. The most prominent outlierin our data collection, the reindeer, has beenreported to have homogenous rumen contents(Westerling, 1970; Hobson et al., 1976) and a veryeven rumen papillation (Soveri and Nieminen,1995; Josefsen et al., 1996; Mathiesen et al., 2000;Soveri and Nieminen, 2007). Whether this is causedby the peculiar diet of reindeer, or by an exceptionalrumen physiology, remains to be elucidated. In thehippopotamids, which also have a voluminous for-estomach lined with a papillated mucosa, the ab-sence of differential particle retention contrastswith the selective large particle retention in rumi-

nants (Schwarm et al., 2008); correspondingly, noelaborate stratification of contents would beexpected in this group, and reports on the papilla-tion of the hippopotamus do not indicate a stratifica-tion as seen in grazing ruminants (Langer, 1988).We propose that it is a higher fluid content in thegrazing ruminant forestomach as compared to thehippopotamids (Thurston et al., 1968) that facili-tates the stratification of the contents by allowingparticle movements according to density.

One obvious explanation for differences in papil-lation between ruminant species is the sheer effectof body size and hence rumen size—the larger arumen, the more distinct the characteristics of itscontents’ different layers could be. The significantcorrelations between BM and SEF parameters,which had not been expected, would support thishypothesis. However, these findings can probablybe explained by the fact that BM was correlated to%grass in this dataset. Low proportions of grass inthe natural diet, and SEF parameters indicatingunstratified rumen contents, do occur across thewhole body size range (up to the largest ruminant,the giraffe), indicating that the consistency of therumen contents itself, irrespective of its volume,must be considered responsible for the demon-strated effects. Similarly, the physiological measureof rumen contents stratification, which is the differ-ence between particle and fluid retention in therumen, also does not follow a strict pattern withbody size, either (Clauss and Lechner-Doll, 2001).

But is this consistency of the rumen contents aneffect of the ingested forage, or of physiologicaladaptations of the different animal species? Intra-specific comparisons of SEF data, from individualsof different intermediate feeder species ingesting abrowse- or a grass-dominated diet (Table 3) suggesta diet component in the formation of a stratifiedrumen. In addition, Hofmann (1973) observed thata group of zebus—a species with an usually unpa-pillated dorsal area—had a completely papillatedrumen when kept on lucerne pasture; similarly, heobserved that an oribi kept on a diet of concentrateand occasional browse had a completely papillated

TABLE 3. Surface enlargement factor in the rumen of several wild intermediate feeding ruminants in relation tothe predominant composition of their actual diet

Species Diet

SEFSEF in % SEF

atrium

Dorsal Ventral Atrium Dorsal Ventral

Impala Aepyceros melampus Browse 6.0 6.5 18.0 33 36Grass 1.8 3.4 12.5 14 27

Thomson’s gazelle Gazella thomsoni Browse 3.5 3.5 16.5 21 21Grass 1.5 1.5 16.5 9 9

Eland Taurotragus oryx Browse 6.0 12.0 35.0 17 34Grass 1.7 4.0 35.0 5 11

Grant’s gazelle Gazella granti Browse 5.5 7.0 20.0 28 35Grass 1.9 4.0 20.0 10 20

Data from Hofmann (1973).



rumen, in contrast to free-ranging specimens.Therefore, it can be suspected that certain charac-teristics of dicotyledonous forage, which need to befurther elucidated, induce less stratification in therumen than monocotyledonous forage. Actually, indomestic ruminants, certain secondary plant com-pounds in some dicotyledonous forages (lucerne, clo-ver) have been identified as the cause of ‘‘frothybloat’’ or ‘‘legume bloat,’’ a disease of domestic cattlewhich is characterized by an absence of rumen con-tents stratification (Clarke and Reid, 1970). On theother hand, passage trials in a moose did not showa difference in the pattern of particle and fluidretention between diets including browse, legume,or grass hay (Renecker and Hudson, 1990), andthus suggest independence of rumen contents strat-ification from dietary factors at least in this species.Maybe this is an indication that at least moose haveevolved physiological adaptations that, directly orindirectly, prevent the formation of rumen contentsstratification.

The fact that both, the dorsal as well as the ven-tral rumen region show a difference in SEF ascompared with the atrium (Fig. 4e) supports ourhypothesis that a mechanism leading to this strati-fied papillation must be operative throughout thewhole rumen. The most probable mechanismappears to be rumen content and rumen fluid vis-cosity (Clauss et al., 2006b). Actually, rumen fluidof roe deer or moose was found to be of a higherviscosity than that of mouflon, bison (Clauss et al.,2009, in press) or that of cattle (Hummel et al., inpress). However, this hypothesis has to be testedin a larger number of species. Reasons forthe deviation of giraffe (with an unusually highSEFdorsal) and dikdik (with unusually low SEFdorsalas compared to the SEFventral) cannot be given here.

One of the consequences of a higher fluid viscos-ity would be the entrapment of gas bubbles in therumen contents, rather than the formation of a dis-tinct dorsal gas dome. This would explain the‘‘frothy’’ appearance of browsers’ rumen contents(see Introduction), and the absence of a distinct dor-sal gas dome observed in a moose (Tschuor andClauss, 2008). McCauley and Dziuk (1965) foundthat in resting goats only little gas accumulated inthe dorsal rumen, and suggested that the gas wastrapped as ‘‘numerous bubbles’’ in the rumen con-tents instead. The frothy appearance of the rumencontents of browsers suggests that the pathologicprocess of ‘‘frothy bloat,’’ seen in domestic rumi-nants fed fresh legume forages (Clarke and Reid,1970), may offer some comparative potential for theunderstanding of the differences in rumen physiol-ogy between browsing and grazing ruminants(Clauss et al., 2006b). Interestingly, domestic sheepare less susceptible to legume-caused frothy bloatthan cattle (Olson, 1940; Colvin and Backus, 1988).Given the papillation pattern (Table 1) and the dif-ferential passage of fluid and particles from the

rumen (Clauss et al., 2006b; Fig. 3f), sheep rumencontents are naturally less distinctively stratifiedthan those of cattle. Additionally, in direct compari-sons of animals feeding on the same pastures,sheep ingest a higher proportion of browse thancattle (Sanon et al., 2007). Given these observa-tions, we hypothesize that sheep—and the zebu cat-tle mentioned above—are better adapted to lessstratified rumen contents, and that cattle, asextreme grazers with a very distinct rumen contentstratification and a distinct difference in particleand fluid passage from the rumen, have lost theability to cope with frothy rumen contents, mostlikely due to less flexible rumen motility patterns(Colvin and Backus, 1988).

The question arising from these observations isabout the adaptive value of the described differen-ces. Evidently, given the proportion of areas thatare un-papillated or only lined with small papillae,the total absorptive surface of the whole rumen isless in grazers than in browsers of similar rumensize. This trend is most likely not countered by anincrease in SEF in the papillated rumen areas ofgrazers, as there was no significant increase inSEFatrium with increasing %grass in the naturaldiet (Table 2). This difference in absorptive area inthe rumen puts measurements on the concentra-tion of volatile fatty acids (VFA) (Hoppe, 1977;Clemens and Maloiy, 1983; Hoppe, 1984; Prinset al., 1984) and on VFA production rates (Gordonand Illius, 1994) in the rumen contents of wildruminants into a new perspective. Most of thesestudies had not found a statistical difference intheir measurements between grazers and brows-ers. The concentration of VFA depends on produc-tion and absorption rate across the epithelium ofthe fermentation chamber (Lechner-Doll et al.,1991a). Because a rise in VFA concentration trig-gers an increase in the epithelial growth in therumen (Nocek and Kesler, 1980; Goodlad, 1981;Dirksen et al., 1984), the absorption capacity forVFA will increase and hence actual VFA concentra-tions measured after this adaptation period will beleveled. Thus, large differences in VFA productionrates may be masked and reflected by only verysmall differences in VFA concentrations (Lechner-Doll et al., 1991a). Higher VFA production rates,which may be demonstrated in natural forages ofbrowsing ruminants (Hummel et al., 2006), there-fore need not necessarily translate into higherVFA concentrations in the rumen of these animalsbecause of their larger absorptive surface.

Ruminal VFA concentrations also depend onrumen fluid volume and fluid outflow rate(Lechner-Doll et al., 1991a). Some large grazingruminants, such as cattle (Clauss et al., 2006b;Schwarm et al., 2008), are characterized by a par-ticularly fast fluid passage through the rumen,which might reduce VFA concentrations. Theseanimals might compensate for their comparatively



lower absorptive surface in the rumen by anincreased absorption of VFA in their comparativelylarger omasum (Clauss et al., 2006a). This fastthroughput might additionally have the advantageof maximal use of microbial protein produced inthe rumen (as suggested by Hummel et al., 2008a).The distinct stratification induced by this highfluid throughput could also render the ruminationprocess more efficient, so that only such materialfrom the fiber mat is regurgitated that needs fur-ther comminution. In two white-tailed deer (Odo-coileus virginianus) (a browser, with a presumedlack of a distinct rumen contents stratification),Dziuk et al. (1963) observed regurgitation and re-swallowing of ingesta without rumination and sus-pected that further mastication had been unneces-sary for the respective regurgitated bolus. Theauthors noted that such observations (of ‘vain’regurgitations) had not been made in cattle orsheep. However, detailed studies on differences inregurgitation frequency and rumination in differ-ent ruminant species are mostly lacking.

At least two different extremes of rumen physi-ology are thus proposed by the observed differen-ces in rumen mucosa papillation and hence rumencontents stratification:

1. Browsers, ingesting a faster-fermenting forage,have more viscous rumen contents and fluid,either due to forage or saliva characteristics,and a comparatively slow fluid throughput; thewhole rumen acts as an absorptive organ, andshows no particular adaptations to a contentsstratification with a fiber mat. This physiologytype is a consequence of the fact that the forageinduces high viscosity contents, or necessitatesa high-protein and hence high-viscosity salivadue to the forage’s content of secondary com-pounds (Hofmann et al., 2008).

2. Grazers, ingesting a slower-fermenting forage,have a less viscous rumen fluid, also due to ei-ther forage or saliva characteristics, probablysupported by a comparatively high fluidthroughput; the whole rumen acts as a storageorgan, with absorption occurring at more lim-ited areas, and shows particular adaptations toa contents stratification with a fiber mat. Thisphysiology type is a consequence of the fact thatmonocot forage induces less viscous contents,does not necessitate high-protein saliva, andmight tend to form a more efficient fiber mat.

These findings are independent of phylogeneticrelatedness between ruminant species; e.g., parallelobservations were made in cervids and bovids ofdifferent feeding type. The more pronounced rumencontents stratification could be a reason why graz-ing ruminants digest fiber more efficiently thanbrowsing ruminants (Pérez-Barberı̀a et al., 2004).But whether stratification is actually a relevant ad-

aptation in itself (in the sense of a convergent evo-lution) would have to be studied in in vitro diges-tion models in which important characteristics ofthe modeled ingesta—such as its viscosity—aremanipulated. Note that our study does not claimthat the stratification of rumen contents itself is anadaptation; it merely describes a notable differencein the degree of stratification between the ruminantfeeding types that happens, that is reflected in therumen papillation pattern, and to which the ani-mals adapt by various anatomical and physiologicalmeans. To which degree these adaptations are ge-netically fixed or subject to modification due to theingested forage remains to be demonstrated. Cur-rent evidence suggests that both extremes—theextreme grazers as well as the extreme browsers—are derived from more rudimentary intermediatefeeding types (Codron et al., 2008; DeMiguel et al.,2008). The extremes in rumen contents stratifica-tion and papillation therefore describe opposingrumen physiologies and emphasize the general flex-ibility of the ruminant digestive system.

ACKNOWLEDGMENTS

The authors thank the numerous hunters andzoological institutions that helped collecting mate-rial. Norman Owen-Smith kindly provided thedata collection from his 1997 publication. Theauthors also thank A. S. Hug for assistance in thepreparation of photographic material and B.Schneider for support in literature acquisition.They thank anonymous reviewers for their usefulcomments.

LITERATURE CITED

Agungpriyono S, Yamamoto Y, Kitamura N, Yamada J, Sigit K,Yamashita T. 1992. Morphological study on the stomach ofthe Lesser mouse deer (Tragulus javanicus) with special ref-erence to the internal surface. J Vet Med Sci 54:1063–1069.

Beaumont R, Deswysen AG. 1991. Mélange et propulsion ducontenu du réticulo-rumen. Reprod Nutr Dev 31:335–359.

BehrendA, Lechner-DollM, StreichWJ, ClaussM. 2004. Seasonalfaecal excretion, gut fill, liquid, and particle marker retention inmouflon (Ovis ammon musimon), and a comparison with roedeer (Capreolus capreolus). Acta Theriol 49:503–515.

Bell RHV. 1971. A grazing ecosystem in the Serengeti. Sci Am225:86–93.

Bigalke RC. 1972. Observations on the behavior and feedinghabits of the springbok (Antidorcas marsupialis). Zool Afr7:333–359.

Bodmer RE. 1990. Ungulate frugivores and the browser-grazercontinuum. Oikos 57:319–325.

Campos-Arceiz A, Takatsuki S, Lhagvasuren B. 2004. Foodoverlap between Mongolian gazelles and livestock in Omno-gobi southern Mongolia. Ecol Res 19:455–460.

Capote FA, Hentges JF. 1967. Diet effect on ruminant forestom-ach structure. Ceiba 13:9–37.

Case TJ. 1979. Optimal body size and an animal’s diet. ActaBiotheor 28:54–69.

Clarke TJ, Reid CSW. 1970. Legume bloat. In: Philipson AT,editor. Physiology of Digestion and Metabolism in the Rumi-nant. Newcastle Upon Tyne, England: Oriel Press. pp 599–606.



Clauss M, Lechner-Doll M. 2001. Differences in selective retic-ulo-ruminal particle retention as a key factor in ruminantdiversification. Oecologia 129:321–327.

Clauss M, Lechner-Doll M, Behrend A, Lason K, Lang D,Streich WJ. 2001. Particle retention in the forestomach of abrowsing ruminant, the roe deer (Capreolus capreolus). ActaTheriol 46:103–107.

Clauss M, Lechner-Doll M, Streich WJ. 2002. Faecal particlesize distribution in captive wild ruminants: An approach tothe browser/grazer-dichotomy from the other end. Oecologia131:343–349.

Clauss M, Lechner-Doll M, Streich WJ. 2003. Ruminant diversi-fication as an adaptation to the physicomechanical character-istics of forage. A reevaluation of an old debate and a newhypothesis. Oikos 102:253–262.

Clauss M, Hofmann RR, Hummel J, Adamczewski J, Nygren K,Pitra C, Reese S. 2006a. The macroscopic anatomy of theomasum of free-ranging moose (Alces alces) and muskoxen(Ovibos moschatus) and a comparison of the omasal laminalsurface area in 34 ruminant species. J Zool (Lond) 270:346–358.

Clauss M, Hummel J, Streich WJ. 2006b. The dissociation ofthe fluid and particle phase in the forestomach as a physio-logical characteristic of large grazing ruminants: An evalua-tion of available, comparable ruminant passage data. Eur JWildl Res 52:88–98.

Clauss M, Hummel J, Völlm J, Lorenz A, Hofmann RR. 2006c.The allocation of a ruminant feeding type to the okapi(Okapia johnstoni) on the basis of morphological parameters.In: Fidgett A, Clauss M, Eulenberger K, Hatt JM, Hume I,Janssens G, Nijboer J, editors. Zoo Animal Nutrition III.Fürth, Germany: Filander Verlag. pp 253–270.

Clauss M, Kaiser T, Hummel J. 2008a. The morphophysiologicaladaptations of browsing and grazing mammals. In: GordonIJ, Prins HHT, editors. The Ecology of Browsing and Grazing.Heidelberg: Springer. pp 47–88.

Clauss M, Reese S, Eulenberger K. 2008b. Macroscopic digestiveanatomy of a captive lowland anoa (Bubalus depressicornis).5th European Zoo Nutrition Conference. Abstract Book:42.

Clauss M, Fritz J, Bayer D, Nygren K, Hammer S, HattJM, Südekum KH, Hummel J. 2009. Physical characteris-tics of rumen contents in four large ruminants of differentfeeding type, the addax (Addax nasomaculatus), bison (Bi-son bison), red deer (Cervus elaphus) and moose (Alcesalces). Comp Biochem Physiol A 152:398–406.

Clauss M, Fritz J, Bayer D, Hummel J, Streich WJ, SüdekumKH, Hatt JM. Physical characteristics of rumen contents intwo small ruminants of different feeding type, the mouflon(Ovis ammon musimon) and the roe deer (Capreolus capreo-lus). Zoology (in press). doi:10.1016/j.zool.2008.1008.1001(online).

Clemens ET, Maloiy GMO. 1983. Digestive physiology of EastAfrican wild ruminants. Comp Biochem Physiol A 76:319–333.

Codron D, Brink JS, Rossouw L, Clauss M. 2008. The evolutionof ecological specialization in southern African ungulates:Competition or physical environmental turnover? Oikos 117:344–353.

Colvin HW, Backus RC. 1988. Bloat in sheep (Ovis aries). CompBiochem Physiol A 91:635–644.

Dardillat C, Baumont R. 1992. Physical characteristics of retic-ular content in the bovine and consequences on reticular out-flow. Reprod Nutr Dev 32:21–36.

DeMiguel D, Fortelius M, Azanza B, Morales J. 2008. Ancestralfeeding state of ruminants reconsidered: Earliest grazing ad-aptation claims a mixed condition for Cervidae. BMC EvolBiol 8:13.

Dhungel SK, O’Gara BW. 1991. Ecology of the hog deer in RoyalChitwan National Park. Nepal. Wildl Monogr 119:1–40.

Dirksen G, Liebich HG, Brosi G, Hagemeister H, Mayer E.1984. Morphologie der Pansenschleimhaut und Fettsäurepro-duktion beim Rind - bedeutende Faktoren für Gesundheitund Leistung. J Vet Med Ser A 31:414–430.

Dziuk HE, Fashingbauer BA, Idstrom JM. 1963. Ruminoreticu-lar pressure patterns in fistulated white-tailed deer. Am J VetRes 24:772–783.

Enzinger W, Hartfiel W. 1998. Auswirkungen gesteigerteerEnergie- und Proteingehalte des Futters auf Fermentation-sprodukte. Fauna und Schleimhaut des Pansens von Wildiwe-derkäuern (Darmhirsch/Reh) im Vergleich zu Hauswieder-käuern (Schaf/Ziege). Eur J Wildl Res 44:201–220.

Faichney GJ. 2006. Digesta flow. In: Dijkstra J, Forbes JM,France J, editors. Quantitative Aspects of Ruminant Diges-tion and Metabolism. Wellingford, UK: CAB International. pp49–86.

Fernandez MH, Vrba ES. 2005. A complete estimate of the phy-logenetic relationships in Ruminantia: A dated species-levelsupertree of the extant ruminants. Biol Rev 80:269–302.

Field CR. 1972. The food habits of wild ungulates in Uganda byanalysis of stomach contents. East Afr Wildl J 10:17–42.

Forsyth DM, Fraser KW. 1999. Seasonal changes in the rumenmorphology of Himalyan tahr (Hemitragus jemlahicus) in thetwo thumb range. South Island, New Zealand. J Zool (Lond)249:241–248.

Gagnon M, Chew AE. 2000. Dietary preferences in extant Afri-can bovidae. J Mammal 81:490–511.

Garrod AH. 1877. Notes on the visceral anatomy and osteologyof the ruminants, with a suggestion regarding a method ofexpressing the relations of species by means of formulae. ProcZool Soc Lond 1877:2–18.

Geiger G, Hofmann RR, König R. 1977. Vergleichend-anatomi-sche Untersuchungen an den Vormägen von Damwild (Cervusdama) und Muffelwild (Ovis ammon musimon). SäugetierkdlMitt 25:7–21.

Geist V. 1999. Deer of the World. Their Evolution, Behaviour,and Ecology. Shrewsbury, England: Swan Hill Press.

Goodlad RA. 1981. Some effects of the diet on the mitotic indexand the cell cycle of the ruminal epithelium of sheep. Q JExp Physiol 66:487–499.

Gordon IJ, Illius AW. 1994. The functional significance of thebrowser-grazer dichotomy in African ruminants. Oecologia98:167–175.

Grau H. 1955. Zur Funktion der Vormägen, besonders des Netz-magens, der Wiederkäuer. Berl Munch Tierärztl Wochenschr15:271–275.

Hart JA, Hart TB. 1988. A summary report on the behaviour,ecology and conservation of the okapi (Okapia johnstoni) inZaire. Acta Zool Pathol Antverp 80:19–28.

Heinichen IG. 1972. Preliminary notes on the suni (Neotragusmoschatus) and the red duiker (Cephalophus natalensis). ZoolAfr 7:157–165.

Hemmoda ASK, Berg R. 1980. Gross-anatomical studies on theruminal pillar system of the Egyptian water buffalo (Bosbubalis). Anat Histol Embryol 9:148–154.

Hobson RN, Mann SO, Summers R. 1976. Rumen function inred deer, hill sheep and reindeer in the Scottish Highlands.Proc R Soc Edinb B 75:181–198.

Hofmann RR. 1969. Zur Topographie und Morphologie des Wie-derkäuermagens im Hinblick auf seine Funktion (nach ver-gleichenden Untersuchungen an Material ostafrikanischerWildarten). J Vet Med Suppl 10:1–180.

Hofmann RR. 1973. The Ruminant Stomach. Nairobi: East Afri-can Literature Bureau.

Hofmann RR. 1982. Zyklische Umbauvorgänge am Verdauung-sapparat des Gamswildes als Ausdruck evolutionärer Anpas-sung an extreme Lebensräume. Allg Forest Ztg 51/52:1562–1564.

Hofmann RR. 1984. Feeding habits of mouflon (Ovis ammonmusimon) and chamois (Rupicapra rupicapra) in relation tothe morphophysiological adaptation of their digestive tracts.In: Hoefs M, editor. Proceedings of the Fourth Biennial Sym-posium of the Northern Wild Sheep and Goat Council. White-horse, Yukon: Yukon Wildlife Branch. pp 341–355.

Hofmann RR. 1985. Digestive physiology of deer—Their mor-phophysiological specialisation and adaptation. R Soc N ZBull 22:393–407.



Hofmann RR. 1989. Evolutionary steps of ecophysiological adap-tation and diversification of ruminants: A comparative viewof their digestive system. Oecologia 78:443–457.

Hofmann RR, Stewart DRM. 1972. Grazer or browser: A classi-fication based on the stomach-structure and feeding habit ofEast African ruminants. Mammalia 36:226–240.

Hofmann RR, Schnorr B. 1982. Die funktionelle Morphologiedes Wiederkäuer-Magens. Stuttgart: Ferdinand Enke Verlag.

Hofmann RR, Matern B. 1988. Changes in gastrointestinal mor-phology related to nutrition in giraffes (Giraffa cameloparda-lis): A comparison of wild and zoo specimens. Int Zoo Yb27:168–176.

Hofmann RR, Nygren K. 1992. Ruminal mucosa as indicator ofnutritional status in wild and captive moose. Alces Suppl1:77–83.

Hofmann RR, Geiger G, König R. 1976. Vergleichend-anatomi-sche Untersuchungen an der vormagenschleimhaut vonrehwild (Capreolus capreolus) und rotwild (Cervus elaphus). ZSäugetierkd 41:167–193.

Hofmann RR, Schwartz HJ, Schwartz M. 1987. Morphologicaladaptation of the forestomach of small East African goats toseasonal changes of forage quality. Proc Int Conf Goats 4:1–14.

Hofmann RR, Kock RA, Ludwig J, Axmacher H. 1988a. Sea-sonal changes in rumen papillary development and body con-dition in free-ranging Chinese water deer (Hydropotes iner-mis). J Zool (Lond) 216:103–117.

Hofmann RR, Knight MH, Skinner JD. 1995. On structuralcharacteristics and morphophysiological adaptation of thespringbok (Antidorcas marsupialis) digestive system. Trans RSoc S Afr 50:125–142.

Hofmann RR, Fassbender M, Kock R. 2005. Structural charac-teristics and morphophysiological adaptations of the digestivesystem of Père David’s deer, the milu (Elaphurus davidia-nus). In: Jingshi X, editor. The 20th Anniversary of Milu’sReturn to Home. Bejing: Milu Ecological Research Centre. pp108–118.

Hofmann RR, Saber AS, Pielowski Z, Fruzinski B. 1988b. Com-parative morphological investigations of forest and field eco-types of roe deer in Poland. Acta Theriol 33:103–114.

Hofmann RR, Streich WJ, Fickel J, Hummel J, Clauss M. 2008.Convergent evolution in feeding types: Salivary gland massdifferences in wild ruminant species. J Morphol 269:240–257.

Hoppe PP. 1977. Rumen fermentation and body weight in Afri-can ruminants. In: Peterle TJ, editor. 13th Congress of GameBiology. Washington DC: The Wildlife Society. pp 141–150.

Hoppe PP. 1984. Strategies of digestion in African herbivores.In: Gilchrist FMC, Mackie RI, editors. Herbivore Nutrition inthe Subtropics and Tropics. Craighall, South Africa: SciencePress. pp 222–243.

Hummel J, Clauss M, Zimmermann W, Johanson K, NorgaardC, Pfeffer E. 2005. Fluid and particle retention in captiveokapi (Okapia johnstoni). Comp Biochem Physiol A 140:436–444.

Hummel J, Südekum KH, Streich WJ, Clauss M. 2006. Foragefermentation patterns and their implications for herbivoreingesta retention times. Funct Ecol 20:989–1002.

Hummel J, Steuer P, Südekum KH, Hammer S, Hammer C,Streich WJ, Clauss M. 2008a. Fluid and particle retention inthe digestive tract of the addax antelope (Addax nasomacula-tus)—Adaptations of a grazing desert ruminant. Comp Bio-chem Physiol A 149:142–149.

Hummel J, Südekum KH, Bayer D, Ortmann S, Hatt JM,Clauss M. Physical characteristics of reticuloruminal contentsof cattle in relation to forage type and time after feeding.J Anim Physiol Anim Nutr (in press). DOI: 10.1111/j.1439-0396.2008.00806.x (online).

Jiang Z. 1998. Feeding Ecology and Digestive Systems of Rumi-nants: A Case Study of the Mongolian Gazelle (Procapra gut-turosa) and the Japanese Serow (Capricornis crispus). Tokyo,Japan: University of Tokyo.

Jiang Z, Takatsuki S, Wang W, Li J, Jin K, Gao Z. 2003. Sea-sonal changes in parotid and rumen papillary development inMongolian gazelle (Procapra gutturosa). Ecol Res 18:65–72.

Josefsen TD, Aagnes TH, Mathiesen SD. 1996. Influence of dieton the morphology of the ruminal papillae in reindeer calves(Rangifer tarandus). Rangifer 16:119–128.

Kamler J. 2001. Morphological variability of forestomach muco-sal membrane in red deer, fallow deer, roe deer and mouflon.Small Rumin Res 41:101–107.

Kaske M, Hatiboglu S, von Engelhardt W. 1992. The influenceof density and size of particles on rumination and passagefrom the reticulo-rumen of sheep. Br J Nutr 67:235–244.

Kingdon J. 1982. East African Mammals, Vol. 3. London: Aca-demic Press.

König R, Hofmann RR, Geiger G. 1976. Differentiell-morpholo-gische Untersuchungen der resorbierenden schleimhauto-berfläche des pansens beim rehwild (Capreolus capreolus) imsommer und winter. Eur J Wildl Res 22:191–196.

Lanave C, Preparata G, Sacone C, Serio G. 1984. A new methodfor calculating evolutionary substitution rates. J Mol Evol20:86–93.

Langer P. 1973. Vergleichend-anatomische untersuchungen ammagen der artiodactyla. II. Untersuchungen am magen dertylopoda und ruminantia. Gegenbaurs Morphol Jb 119:633–695.

Langer P. 1974. Oberflächenmessungen an der Innenausklei-dung des Ruminoreticulums von Rehwild (Capreolus capreo-lus) und Damwild (Cervus dama). Z Säugetierkd 39:168–190.

Langer P. 1975. Macroscopic anatomy of the stomach of theHippopotamidae GRAY, 1821. Anat Histol Embryol 4:334–359.

Langer P. 1988. The Mammalian Herbivore Stomach. Stuttgart/New York: Gustav Fischer Verlag.

Lechner-Doll M, Becker G, von Engelhardt W. 1991a. Short-Chain Fatty Acids in the Forestomach of Indigenous Camels,Cattle, Sheep, and Goats and in the Caesum of DonkeysGrazing a Thornbush Savanna Pasture. Vienna, Austria:International Atomic Energy Association. pp 253–268.

Lechner-Doll M, Kaske M, von Engelhardt W. 1991b. Factorsaffecting the mean retention time of particles in the forestom-ach of ruminants and camelids. In: Tsuda T, Sasaki Y, Kawa-shima R, editors. Physiological Aspects of Digestion andMetabolism in Ruminants. San Diego: Academic Press. pp455–482.

Lentle RG, Henderson IM, Stafford KJ. 1996. A multivariateanalysis of rumen papillary size in red deer (Cervus elaphus).Can J Zool 74:2089–2094.

Lentle RG, Stafford KJ, Henderson IM. 1997. The effect of for-malin on rumen surfac area in red deer. Anat Histol Embryol26:127–130.

Marholdt F. 1991. Fütterungsbedingte, Morphologische Verän-derungen der Vormagenschleimhaut von 67 Zoo-Wieder-käuern im Vergleich mit Wildlebenden Wiederkäuern. Gies-sen: Justus-Liebig-Universität Giessen.

Martin P, Schauder W. 1938. Lehrbuch der Anatomie der Haus-tiere III (Anatomie der Hauswiederkäuer). Stuttgart, Ger-many: Schickhardt and Ebner.

Martins E. 2004. COMPARE, version 4.6. Computer programsfor the statistical analysis of comparative data. Available at:http://compare.bio.indiana.edu/. Department of Biology, Indi-ana University, Bloomington, IN.

Martins E, Hansen T. 1997. Phylogenies and the comparativemethod: A general approach to incorporating phylogeneticinformation into analysis of interspecific data. Am Nat149:646–667.

Mathiesen SD, Haga OE, Kaino T, Tyler NJC. 2000. Diet com-position, rumen papillation and maintenance of carcass massin female Norwegian reindeer (Rangifer tarandus) in winter.J Zool (Lond) 251:129–138.

McCauley EH, Dziuk HE. 1965. Correlation of motility and gascollection from goat rumen. Am J Physiol 209:1152–1154.



Nocek JE, Kesler EM. 1980. Growth and rumen characteristicsof Holstein steers fed pelleted or conventional diets. J DairySci 63:249–254.

Nordin M. 1978. Voluntary food intake and digestion by thelesser mousedeer. J Wildl Manag 42:185–186.

Nygren K, Hofmann RR. 1990. Seasonal variations of food par-ticle size in moose. Alces 26:44–50.

Olson TM. 1940. Bloat in dairy cattle. J Dairy Sci 23:343–353.Owen-Smith N. 1997. Distinctive features of the nutritional

ecology of browsing versus grazing ruminants. Z Säugetierkd62 (Suppl 2):176–191.

Pérez-Barberı̀a FJ, Gordon IJ. 2001. Relationships between oralmorphology and feeding style in the Ungulata: A phylogeneti-cally controlled evaluation. Proc R Soc Lond B 268:1023–1032.

Pérez-Barberı̀a FJ, Elston DA, Gordon IJ, Illius AW. 2004. Theevolution of phylogenetic differences in the efficiency of diges-tion in ruminants. Proc R Soc Lond B 271:1081–1090.

Pfeiffer C. 1993. Vergleichend-Morphologische Untersuchungemam Verdauungstrakt des Chinesischen Muntjak (Muntiacusreevesii) Einschliesslich Saisonaler Veränderungen an derVormagenschleimhaut [Diss]. University of Giessen, Giessen,Germany. 95 p.

Pitra C, Fickel J, Meijaard E, Groves PC. 2004. Evolution andphylogeny of old world deer. Mol Phylogenet Evol 33:880–895.

Poppi DP, Ellic WC, Matis JH, Lascano CE. 2001. Marker con-centration patterns of labeled leaf and stem particles in therumen of cattle grazing bermuda grass (Cynodon dactylon)analysed by reference to a raft model. Br J Nutr 85:553–563.

Posada D, Crandall KA. 1998. Modeltest: Testing the model ofDNA substitution. Bioinformatics 14:817–818.

Prins RA, Lankhorst A, van Hoven W. 1984. Gastrointestinalfermentation in herbivores and the extent of plant cell-walldigestion. In: Gilchrist FMC, Mackie RI, editors. HerbivoreNutrition in the Subtropics and Tropics. Craighall, SouthAfrica: Science Press. pp 403–434.

Purvis A, Garland T. 1993. Polytomies in comparative analysesof continous characters. Syst Biol 42:569–575.

Renecker LA, Hudson RJ. 1990. Digestive kinetics of moose,wapiti, and cattle. Anim Prod 50:51–61.

Rodriguez F, Oliver JF, Marin A, Medina JR. 1990. The generalstochastic model of nucleotide substitution. J Theor Biol142:485–501.

Rohlf F. 2001. Comparativemethods for the analysis of continuousvariables: Geometric interpretations. Evolution 55:2143–2160.

Sakata T, Tamate H. 1978. Rumen epithelial cell proliferationaccelerated by rapid increase in intraruminal butyrate.J Dairy Sci 61:1109–1113.

Sakata T, Tamate H. 1979. Rumen epithelial cell proliferationaccelerated by propionate and acetate. J Dairy Sci 62:49–52.

Sander EG, Warner RG, Harrison HN, Loosli JK. 1959. Thestimulatory effect of sodium butyrate and sodium propionateon the development of the rumen mucosa in the young calf.J Dairy Sci 42:1600–1605.

Sanon HO, Kaboré-Zoungrana C, Ledin I. 2007. Behavior ofgoats, sheep and cattle and their selection of browse specieson natural pasture in a Sahelian area. Small Rumin Res67:64–74.

Sarma K, Bhattacharya M, Bordoloi CC, Kalita SN. 1996. Mac-roanatomy of rumen of mithun (Bos frontalis), yak (Bos grun-niens), and zebu (Bos indicus). Indian J Anim Sci 66:705–706.

Schaller GB. 1973. Observations on Himalayn Tahr (Hemi-tragus jemlahicus). J Bombay Nat Hist Soc 70:1–24.

SchmidtHA, StrimmerK,VingronM, vonHaeseler A. 2002. TREE-PUZZLE:Maximum likelihood phylogenetic analysis using quar-tets and parallel computing. Bioinformatics 18:502–504.

Schnorr B, Vollmerhaus B. 1967. Das Oberflächenrelief derPansenschleimhaut bei Rind und Ziege [The surface relief ofthe ruminal mucosa in the ox and goat]. J Vet Med Ser A14:93–104.

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 hippopot-amus (Hexaprotodon liberiensis): Two functionally differentforegut fermenters. Comp Biochem Physiol A 150:32–39.

Skinner J, Chimimba CT. 2005. The Mammals of the SouthernAfrican subregion. Cambridge: Cambridge University Press.

Smith PH, Sweeney HC, Rooney JR, King KW, Moore WEC.1956. Stratifications and kinetic changes in the ingesta of thebovine rumen. J Dairy Sci 39:598–609.

Smolle-Wieszniewski E. 1987. Morphologische Untersuchungenan der Pansenwand von Gemsen (Rupicapra rupicapra).Wien Tierärztl Monatsschr 74:74.

Soveri T, Nieminen M. 1995. Effects of winter on the papillarmorphology of the rumen in reindeer calves. Can J Zool 73:228–233.

Soveri T, Nieminen M. 2007. Papillar morphology of the rumenof forest reindeer (Rangifer tarandus fennicus) and semido-mesticated reindeer (R. t. tarandus). Anat Histol Embryol36:366–370.

Sponheimer M, Lee-Thorp JA, DeRuiter D, Smith JM, Vander Merwe NJ, Reed K, Grant CC, Ayliffe LK, Robinson TF,Heidelberger C, Marcus W. 2003. Diets of Southern Africanbovidae: Stable isotope evidence. J Mammal 84:471–479.

Stafford KJ. 1995. The stomach of the sambar deer (Cervus uni-color). Anat Histol Embryol 24:241–249.

Stafford KJ, Stafford YM. 1990. Stomach of the puku. Afr JEcol 28:250–252.

Stafford KJ, Stafford YM. 1991. The stomach of the Kafuelechwe (Kobus leche kafuensis). Anat Histol Embryol 20:299–310.

Stubbe C. 1971. Zur Ernährung des Muffelwildes (Ovis ammonmusimon) in der DDR. Beitr Jagd Wildforschg 7:103–125.

Sutherland TM. 1988. Particle separation in the forestomach ofsheep. In: Dobson A, Dobson MJ, editors. Aspects of DigestivePhysiology in Ruminants. Ithaca, NY: Cornell UniversityPress. pp 43–73.

Swofford DL. 2002. PAUP*: Phylogenetic Analyses Using Parsi-mony (and Other Methods), Version 4.0 Beta. WashingtonDC: Smithsonian Institition.

Tafaj M, Junck B, Maulbetsch A, Steingass H, Piepho HP,Drochner W. 2004. Digesta characteristics of dorsal, middleand ventral rumen of cows fed with different hay qualitiesand concentrate levels. Arch Anim Nutr 58:325–342.

Tavaré S. 1986. Some probabilistic and statistical problems inthe analysis of DNA sequences. Lect Math Life Sci 17:57–86.

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, HigginsDG. 1997. The CLUSTAL_X windows interface: Flexible strat-egies for multiple sequence alignment aided by quality analy-sis tools. Nucl Acids Res 15:4876–4882.

Thurston JP, Noirot-Timothée C, Arman P. 1968. Fermentativedigestion in the stomach of Hippopotamus amphibius andassociated ciliate protozoa. Nature 218:882–883.

Tschuor A, Clauss M. 2008. Investigations on the stratificationof forestomach contents in ruminants: An ultrasonographicapproach. Eur J Wildl Res 54:627–633.

Van Wieren SE. 1996. Browsers and grazers: Foraging strategiesin ruminants. In: Van Wieren SE, editor. Digestive Strategiesin Ruminants and Nonruminants: Thesis Landbouw. TheNetherlands: University of Wageningen. pp 119–146.

Vorontsov NN. 2003. Macromutations and evolution: Fixation ofGoldschmidt’s macromutations as species and genus charac-ters. Papillomatosis and appearance of macrovilli in therodent stomach. Russ J Genet 39:422–426.

Warner RG, Flatt WP, Loosli JK. 1956. Dietary factors influenc-ing the development of the ruminant stomach. Agric FoodChem 4:788–792.

Wen-Jun L, Hofmann RR. 1991. Stomach wall samples as indi-cators of nutritional status in Chinese and European roe deer(Capreolus capreolus). Acta Zool Sin 37:193–197.

Westerling B. 1970. Rumen ciliate fauna of semi-domestic rein-deer (Rangifer tarandus) in Finland: Composition, volume,and some seasonal variations. Acta Zool Fenn 127:1–76.



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