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Comparative Anatomy of the Stomach in Mammalian Herbivores

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Comparative Anatomy of the Stomach in Mammalian Herbivores 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
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