Quarterly Journal of Experimental Physiology (1984), 69, 615-625 Printed in Great Britain

COMPARATIVE ANATOMY OF THE STOMACH IN MAMMALIAN HERBIVORES

PETER LANGER Institut fur Anatomie und Zytobiologie, Justus-Liebig-Universitat Giessen, Aulweg 123, D-6300 Giessen, F.R.G.

INTRODUCTION The aims of this paper are to review data on the comparative anatomy of the stomach in mammalian herbivores and to refer to some structural adaptations that can be identified as serving specialized functions. Reference will be made to the three main digestive functions of the stomach: secretion, absorption and motility, but most attention will be paid to the adaptations of the stomach that serve to ensure the storage of the digesta for microbial degradation, the delay in transit of digesta and the physical separation of constituents of digesta.

COMPARATIVE ANATOMY OF THE STOMACH IN RELATION TO GASTRIC FUNCTION Secretion The gastric secretion of proteolytic enzymes, hydrochloric acid and mucus has been associated with characteristic types of cells and glands in the gastric mucosa; these cells and endocrine cells present in the glandular gastric mucosa are not distributed uniformly throughout the stomach. Thus, in the glandular unilocular stomach (terminology, Langer, 1984) such as that of man, three main areas of the mucosa are identified: cardiac, oxyntic or fundic and pyloric (Ito, 1968). The exocrine secretions of the cardiac and pyloric glands are alkaline with a high mucus content, those of the oxyntic area may contain acid, enzyme and mucin. The areas differ in extent in the unilocular stomach, with the cardiac gland area being relatively narrow in the stomachs of cat, dog and human. In animals in which a multilocular stomach has developed, these glandular areas are commonly situated most caudally in the stomach lying between sometimes capacious non-glandular gastric compartments and the duodenum. In Sirenia, however, oxyntic cells are concentrated in a pouch or diverticulum set off from the main gastric lumen (Marsh, Spain & Heinsohn, 1978; Reynolds, 1980). The stomach of the pig presents, in some respects, a form intermediate between the uni- and multi-locular types of stomach because it has a small gastric diverticulum and stratified epithelium at the cardia; there is an extensive cardiac zone with glandular epithelium extending into the diverticulum (Sloss, 1954) and discrete oxyntic and pyloric gland areas. Radiological studies show that the diverticulum always contains gas and occasionally ingesta and is motile (Wood & Kidder, 1982). The status of the diverticulum and its functions are not clear. Gastric development and microbialfermentation Microbial degradation of the structural carbohydrates in plants is vital to digestion in mammals. It can be argued that the development of this type of digestion has been of great evolutionary advantage, enabling some mammalian herbivores to occupy nutritional niches free, in many instances, of competitors (Kinnear &Main, 1979). 616 P. LANGER

B (lstric tloi-ini anid muinldosal liniinge in tile Artiodact\via ( ,astric t'orini and nniLcosal fi nine in differenit herbivores

Pe nora rumlain,inlts wNith 1io1( Ots and anj tlers) Potoroillnac cx (rdt-kaniiaroos) Tra 'llII 11.11 ci rotains M\acropodiMICt Iltre kano.aroos)

T lopoda carnlel-like Colobidac naminals ) (Iclea nonkke---)-v liip1popotarnmidac Bradypodidac (hippopotanmns anid ( tree} slortlis ) < py'g111' flipploprotamu s )

as Sirensia U4 It+a. nisa) (sea cow\s)

ti 9 BabYroisa babiX rnissa b-ihiriisal _r.

Fig. 1. Gastric form and mucosal lining in the Artiodactyla (A) and in other herbivores (B). The different mucosal types were differentiated as follows: LI: non-glandular squamous; : cardial glands; E: HCl-producing fundic' glands; 1111: pyloric glands.

Microbial fermentation in the forestomach occurs in the Pecora, Tragulina, Tylopoda, Hippopotamidae, Macropodidae, Colobidae, Bradypodidae (Bauchop, 1977), Tayassuidae (Shively, 1979) and Potoroinae (Kinnear, Cockson, Christensen & Main, 1979; Kinnear & Main, 1979). No comparable investigations have been made in Babyrousa babyrussa in which conditions are comparable to those in the domestic pig and fermentation is of minor significance as in other species with a unilocular stomach (Bauchop, 1977; Kidder & Manners, 1978). In Sirenia, microbial gastric fermentation is not developed to any extent: the sea-cows are hind-gut fermenters (Marsh et al. 1978). Where microbial fermentation takes place in the stomach, a voluminous' fermentation-vat' is differentiated (Figs. 1 A and B and 2A and B). This provides a gastric capacity to hold food for fermentation which may be 'in-line' between the cardia and the pylorus or can be 'set-off' in a cul-de-sac (Hungate, 1976) where a portion of the gastric contents is stored for a longer time allowing it to be more thoroughly degraded microbially. A consequence is to slow transit of digesta through the stomach as a whole. Increase of transit time In all forestomach fermenters there is an increased cross-sectional diameter of the stomach, increased volume of digesta in the stomach and increased time for transit of digesta through the stomach. However, in the Sirenia, the transit time of digesta through the total digestive tract might be increased by the fact that a 'double volume' is developed, i.e. the capacity of the duodenal ampulla that follows the stomach, is similar to that of the total stomach (Fig. 1 B). This 'double-volume' effect does not occur in the forestomach STOMACH IN MAMMALIAN HERBIVORES 617

A B Terminology and relative volumes of the stomach Terminology and relative volumes of the stomach regions in the Artiodactyla regions in different herbivores Terninology (%) Terminology (%) Potoroinae (a) sacciform Pecora (a) ruminoreticulum 88 b a (rat kangaroos) forestomach 77 (ruminants (b) omasum 6 (b) tubiform I 9 with horns (c) abomasum 6 forestomach and antlers) a (c) hind stomach 4 b a Tragulina (a) ruminoreticulum 95 Macropodinae (a) sacciform (chevrotains) (b) abomasum 5 (true kangaroos) forestomach 31 (b) tubiform a forestomach 60 c b a Tylopoda (a) ruminoreticulum 89 (c) hind stomach 9 (camel-like (b) tubiform c b Colobidae (a) saccus gastricus mammals) forestomach 9 (leaf monkeys) and praesaccus 73 - (c) hind stomach 2 a (b) tubus gastricus 24 c Hippopotamidae (a) blind-sacs and (c) pars pylorica 3 (hippopotamus vestibulum 42 a and pygmy (b) connecting hippopotamus) compartment Bradypodidae (a) diverticulum (c) hind stomach 6 (tree sloths) and fundus 29 / (b) central pouch 31 -.- Tayassuidae (a) blind-sacs 40 (c) connecting pouch 36 d L., (peccaries) (b) gastric pouch 45 b (d) prepyloric stomach 4 c b a (c) hind stomach 15 T a a Sirenia (a) stomach 32 d/b Babyrousa (a) diverticulum (sea cows) (b) cardiac gland 9 babyrussa (b) fornix (c) duodenal ampulla 47 (babirusa) (c) corpus and 63S (d) pyloric blind-sacs 12 pylorus 63 C b__ a d b Fig. 2. Terminology and relative volumes of the stomach regions in the Artiodactyla (A) and in other herbivores (B). The gastric groove is represented schematically as a horizontal filled bar and the apertures between gastric regions are also represented. The variability within the Macropodinae is not considered in this Figure. Dotted structures in the Potoroinae, Macropodinae, and Colobidae represent the functionally changing semilunar folds.

fermenters considered here. The different types of gastric forms show a variable array of folds that may act to regulate digesta transit. A complex system of anatomical differen- tiations directing digesta through the forestomach regions of the Hippopotamidae, includes extensive folds that probably function like valves and help to transport the digesta unidirectionally from the oesophagus via the viscera blind-sac and the vestibulum into the parietal blind-sac and from there further into the connecting compartment (Langer, 1975, 1976). Such a 'detour' via the forestomach blind-sacs would increase transit time of digesta from cardia to pylorus. The long connexion chamber with transverse folds also might have the same general effect. The transit time ofdigesta in an aborad direction may be influenced by small apertures between different stomach compartments such as those in the ruminants (ostium reticulo-omasicum in the Pecora and ostium reticulo-abomasicum in the Tragulina), the Tylopoda, Bradypodidae, Colobidae, and Potoroinae, but not in Macropodinae or Tayassuidae (Fig. 1 A and B). A complex mechanism affecting digesta transit is present in the stomachs of the Macropodidae and the Colobidae. Both have a stomach with taeniae, haustra, and semilunar folds; structures generally found in the large intestine of herbivorous or omnivorous hind-gut fermenters, where digesta transit is slow in taxonomically unrelated mammalian groups (Fig. 3) (Langer, 1982). In the large intestine of these animals, as well as in the stomach of Macropodidae and Colobidae, the external layer of the tunica 618 P. LANGER

Ott reta&:eous/ O. e 65 % Palacen 5 .3 % E3cene OMigocene 26 IPliocene-Recent Fig. 3. Mammals with taeniae, haustra, and semilunar folds (filled areas) in the hind gut and/or the stomach. Abbreviations refer to regions where taeniae, haustra, and semilunar folds are differentiated: Ce: caecum; Co: colon; Ve: ventriculus = stomach. muscularis is reduced to longitudinal muscular bands or taeniae (Fig. 4). In the areas of the gastrointestinal wall between these taeniae the cross-sectional diameter can increase and form voluminous dilations, or haustra, as well as functionally mobile semilunar folds. The semilunar folds are 'anchored' on two taeniae. The haustra lie between two semilunar folds (Fig. 4). In these folds the internal circular musculature of the tunica muscularis is contracted, whereas in the haustra it is dilated. In both cases there is a change from an originally circular cross-section to a more polygonal one during contraction or a change to a form with 'bubble-like' outgrowths during dilation. It can be argued that such arrangements favour less muscular effort to achieve a given reduction in cross-sectional surface than in regions of the gut lacking the developments. Physical separation of constituents of digesta An important aspect of gastric function is the retention of coarse particles which ensures that digesta leave the stomach in solution or in a finely divided form. The fine division results in part from mastication when food is eaten and in ruminants from further mastication in the course of rumination in addition to the mechanical breakdown of food in the stomach. Within the stomach itself, there is a gradient in the distribution of particles, with larger particles being fewer in more aboral regions. The mechanisms contributing to differences in particle distribution have not been defined although indications of their nature have been inferred. STOMACH IN MAMMALIAN HERBIVORES 619

Changes in cross-section geometry in an intestinal tube with three taeniae (T)

Circular cross-section Haustrum Semilunar fold A

-80 -40 0 40 80 .-Contraction Dilation Changes in circumference (%) Fig. 4. Changes in cross-section geometry in an intestinal tube with three taeniae (T). Changes in circumference of an intestinal tube are plotted against changes in cross-sectional area. A circular cross-section is considered as the starting point and the changes are represented as percentages of the circular cross-section data. The upper dashed curve represents circular cross-sections with changing diameters, the lower dashed curve represents triangles of different sizes. The continuous curve shows the relation between changes in cross-sectional area and changes in circumference in an intestinal tube with three taeniae and with haustra and semilunar folds. The dot, triangle, and diamond on the full curve represent conditions indicated by the same symbols in the upper semi-schematic drawing of a tube with taeniae, haustra, and semilunar folds.

In the ruminant few coarse particles leave the rumen and reticulum, thus Trudell-Moore & White (1983) reported that in the reindeer the majority of particles passing aborally were 2 mm diameter or less. How such a selection of food particles is achieved is not clear (Phillipson & Ash, 1965) although Grau (1955) and Schels (1956) advanced hypotheses invoking particle size, specific gravity and the cellular form ofthe reticular epithelial surface. According to Schels (1956) particles of a specific gravity greater than those of the rest of the contents ofthe reticulum and rumen become trapped in the dilated cells ofthe reticulum. Relations have been established between reticular contractions and closure and opening of the reticulo-omasal orifice (Bost, 1970) and flow ofdigesta into the omasum (Stevens, Sellers & Spurrell, 1960); it is clear that the activity and condition of these structures contribute importantly in determining what material enters the omasum and when it does so. The sensory innervation ofthe ruminant stomach includes mechano- and chemoreceptors (Iggo & Leek, 1970) which probably contribute to the control of the movements of these structures during responses to changes in conditions within them. 620 P. LANGER Gradations in the numbers ofparticles retained by a 1 mm2 sieve between the forestomach and hind stomach were reported in the similar stomachs of Thylogale thetis and Thylogale stigmata. In those species, the large numbers of micro-organisms present in the sacciform stomach presumably contribute significantly to the breakdown ofdigesta in thiscompartment of the stomach (Dellow & Hume, 1982). Similarly in Macropus robustus, the highest proportion of coarser particles is in the tubiform stomach. In M. robustus, in contrast to the situation in Thylogales, the oesophagus opens into a gastric groove in its stomach; it is supposed that in M. robustus food passes into the tubiform stomach whence coarser particles are selectively transported into the sacciform forestomach where they are subjected to microbial digestion. Dellow (1982) showed that a separation of liquid and particulate components of digesta occurred in the haustrated stomach of the Macropodinae and considered from a review of the passage of markers of liquid and particles, that this separation occurred more efficiently than it does in the stomach of the sheep. The South American Tylopoda are interesting because they are ruminating herbivores lacking an abomasum and having a discrete ostium between the reticulum and gastric tube. Vallenas & Stevens (1971) and Langer (1973) examined the glandular saccules ofthe camelid rumen and the arrangement of their muscle. These saccules can be everted into the forestomach lumen (Vallenas & Stevens, 1971; Ehrlein & Engelhardt, 1971) and their muscle is well disposed to contribute to changes in the height of the glandular cells and may have a function in retention of food particles. Examination of the contents of the stomachs of three collared peccaries (Langer, 1978, 1979 a) suggested that, in these animals also, specific gravity and particle size are important in determining passage ofdigesta as Schels (1956) had suggested in cattle. In these peccaries, particles of 0 25-1 mm diameter with a density of above 1 were found only in small quantities in the ventral part of the gastric pouch: their number increases towards the distal part of the glandular stomach; the upper blind-sac contained a greater proportion of these particles than were present in the gastric pouch. Cineradiographic evidence of alternate contractions of the upper and anterior blind-sacs and the gastric pouch of the peccary stomach (R. S. Wynburn, personal communication) and evidence that the aperture between this pouch and the fourth or last compartment of the stomach changes in diameter suggest that these movements may be associated with mechanisms sorting or selecting material passing aborally in the peccary's stomach. The same oral-aboral gradient of larger and smaller particles in gastric contents has been demonstrated in the Hippopotamidae (Langer, 1975, 1976). It is not known whether the complex folding in its stomach contributes to the maintenance of this gradient. Diversion of liquid digesta and the sulcus ventriculi A gastric groove or sulcus ventriculi (Fig. 2) is a well-developed feature in the reticulum (hence sulcus reticuli) of Ruminantia. It functions at least in young sucking ruminants to direct sucked liquid from the cardia through the reticulum, by-passing the rumen, towards the abosum (Hill, Noakes & Lowe, 1970). The groove is stimulated to contract as part of a complex response in which oesophageal and reticulo-omasal orifice activity areco-ordinated by their vagal innervation (Titchen & Newhook, 1975). Whilst there is no doubt of the functional importance of the reticular groove (Black, 1970) it has not been established that it is an obligatory adaptation for forestomach fermentation (Black & Sharkey, 1970). Arman & Field (1973) discussed the lack ofevidence ofa functioning gastric sulcus (or 'Oesophageal groove' as they referred to it, using older functionally derived terminology) in the hippopotamus. Similarly, Langer (1979c, dand 1980a, b) has drawn attention to the absence of a sulcus ventriculi in some kangaroos: T. thetis is an example. STOMACH IN MAMMALIAN HERBIVORES 621

Absorption An important function in the forestomach is absorption which takes place in the omasum and ruminoreticulum of the Pecora. Absorption of organic products of fermentative digestion, inorganic ions and water have been extensively studied (see Phillipson, 1970) and defined as occurring across the squamous epithelium which lines the entire forestomach of the Ruminantia and Hippopotamidae. In these the epithelial surface is increased by papillae and other developments. The Ruminantia and Hippopotamidae are the only groups considered here where papillae increase the surface area ofthe forestomach. Macroscopically visible papillae are not very common in mammalian forestomachs and their architecture varies. In the white-tailed rat (Mystromys albicaudatus) papillae are completely made up by the horny layer (stratum corneum, Maddock & Perrin, 1981, 1983). The vascularity of papillae have been recognized as important factors in their absorptive function (Comline, Silver & Steven, 1968). Features of the architecture of papillae have also been discussed by Schnorr & Vollmerhaus (1967) who applied a factor ofthe increase in surface area (f.i.s.a.) to make comparisons of surface areas of different regions of the stomach and differences between species. This factor was derived from considerations of the simple surface area (basal surface) and the measured surface of papillae as follows: - Basal surface + 2 x measured surface of papillae f.i.s.a. - Basal surface

Schnorr & Vollmerhaus (1967) concluded papillation accounted for increases ofup to 21-fold in the surface area of the rumen in cattle and up to 13-fold in the goat. The development of papillae varies according to seasonal and biotic influences as Langer (1974b) showed in European roe deer and fallow deer and Hofmann and his colleagues in a number of European game ruminants (Hofmann, Geiger & K6nig, 1976; Konig, Hofmann & Geiger, 1976; Geiger, Hofmann & Kbnig, 1977). In these studies in ruminants, the major increase in surface area in the rumen arises from the presence ofpapillae in the antrum of the rumen. Increases in surface area of over four times have been detected in tragulids and more than 7-fold in the musk ox. Papillae account for lesserincreases in surface area in Hippopotamidae: about 3-fold were reported by Langer (1975) whose studies included the pygmy hippopotamus (Choeropsis liberiensis). Morphological changes in the epithelium in the rumen occur rapidly with changes in the quality offood. Hofmann (1973) noted increases in density and changes in shape ofpapillae within two weeks after better quality food becomes available at the start of the rainy season in East Africa: at this time there are increases in the rumen of substances such as ammonia and volatile fatty acids which are subject to absorption and stimulate papillary development and epithelial growth (Candau, 1973). Such changes, characterized by increased mitosis, have been shown to be stimulated by butyrate, propionate and acetate (Sakata & Tamate, 1978, 1979). In a recent study (P. Langer, unpublished observation) a comparison was made off.i.s.a. and the mitotic index (m.i.) ofthe basal stratum ofepithelium ofthe ruminal atrium of three species of deer obtained with the help of Professor Prins from the Netherlands. Four specimens each of European roe deer (Capreolus capreolus), of European red deer (Cervus elaphus), and five specimens of the fallow deer (Cervus dama) were available. In the roe deer and the red deer, but not in the fallow deer, significant correlations between the factor of increase in surface area and the mitotic index could be found. Both f.i.s.a. and m.i. were highest in the largest species, the red deer, and much lower in the two other deer species. The large species has large papillae with intensive mitotic activity. Nutritional 622 P. LANGER

Thylogale

Mucosal lining of the stomach in nine species of the Macropodinae The schematic illustrations are grouped according to similarities T thetis 11 T stigmatica

L = =JL- J - = -

D. muelleri P. penicillata

L - - JL - - - - J r |I Macropus

M. giganteus i M robustus ILI M. eugenii M. rufus L. conspicillatus L------JL- --J L Fig. 5. Mucosal lining of the stomach in nine species of the Macropodinae. Continuous lines represent species of the same genus, dashed lines represent one species. In M. eugenii and M. giganteus intraspecific differences in mucosal lining have been demonstrated. The three species on the bottom (M. eugenii, M. rufus, and L. conspicillatus) show relatively simple conditions where the immediate surrounding of the cardia is covered with non-glandular squamous epithelium. The other types of gastric forms are considered to be more complex. Those species that are grouped in a horizontal line are considered similar. For explanation of different mucosal types, see the legend to Fig. 1. differences between the three species (Hofmann & Schnorr, 1982) may have been important. The relationship between f.i.s.a. and m.i. needs more detailed investigation in more species to obtain a better understanding of epithelial modifications and their possible importance in absorption. In other forestomach fermenters the epithelium may have glandular characteristics and little is known of what structures are concerned in the absorptive process. In the llama, a zone of cardiac glands might contribute to absorption (Ruibsamen, 1976). Such an idea is not necessarily generally applicable as Gemmell & Engelhardt (1977) indicated, because evidence is not available to indicate similar functions of cardiac glands in different species. It is not possible to relate epithelial structure to absorptive function in a general way. For example in the Potoroinae (the rat kangaroos) the sacciform stomach has a cardiac glandular mucosa whereas in the relatively closely related Macropodinae ('true' kangaroos) the epithelium in the sacciform forestomach is completely squamous (as it is in Thylogale thetis and T. stigmatica, Dorcopsis muelleri and Petrogale penicillata) whilst it is completely glandular in Macropus ru/us and Lagorchestes conspicillatus (Fig. 5). Fuller studies, incorporating work on absorption, are needed to achieve an understanding of the significance in absorption of these features of development of the gastric epithelial surface. STOMACH IN MAMMALIAN HERBIVORES 623

CONCLUSIONS The majority of the information available on anatomical features and functional activities of the stomach of animals in which forestomach fermentation occurs has been obtained from relatively few species. Difficulties such as those related to gaining access to animals because of their small numbers (e.g. Bradypodidae), problems in handling them (Hippo- potamidae) and pressures arising from greater economic importance ofdomesticated species, have dictated the pattern of work on those species. It is clear that it is not appropriate to speak of 'ruminant-like' herbivores in considering Hippopotamidae, Tayassuidae, Macro- podidae, Colobidae and Bradypodidae. Even in the Tylopoda, which are taxonomically relatively close to the Ruminantia and have a forestomach that shows similarities with the ruminoreticulum of ruminants (Langer, 1974a), there are also remarkable differences not only ofphysiological, but also ofmorphological characteristics (Herre, 1982; von Engelhardt & Holler, 1982). In spite of the many dissimilarities between the different types of stomachs in forestomach fermenters indicated in this paper, it is nevertheless also possible to see similarities in the many different morphological and functional differentiations developed by forestomach fermenters. It remains to be demonstrated how to assess, order and interpret these differences. Help received from many colleagues who contributed most useful discussion and criticism is gratefully acknowledged.

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