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Morphology of the Gastrointestinal Tract in Primates : Comparisons with Other Mammals in Relation to Diet David J Chivers, Claude Marcel Hladik

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Morphology of the Gastrointestinal Tract in Primates : Comparisons with Other Mammals in Relation to Diet David J Chivers, Claude Marcel Hladik Morphology of the gastrointestinal tract in primates : Comparisons with other mammals in relation to diet David J Chivers, Claude Marcel Hladik To cite this version: David J Chivers, Claude Marcel Hladik. Morphology of the gastrointestinal tract in primates : Com- parisons with other mammals in relation to diet. Journal of Morphology, Wiley, 1980, 166, pp.337-386. hal-00561758 HAL Id: hal-00561758 https://hal.archives-ouvertes.fr/hal-00561758 Submitted on 16 Mar 2013 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. CHIVERS D.J. & HLADIK C.M. (1980) — Morphology of the gastrointestinal tract in primates : Comparisons with other mammals in relation to diet. Journal of Morphology, 166 : 337-386. Flattened pieces of intestinal tract in a dissecting tray, for the actual measurement of mucosal area. 338 DAVID J. CliiVERS AND C. M. HLADIK G 'I' ~IOI!PIIOI.OGY Ai\llDIET I ~li\~ 1\ I AI.S 339 '67) showed interesting relationsh ips among available in limited qua ntity (fruit), to t hose reductions are clearly specializations, rather a "muscular tooth" compensating fo r the lack primates, but data on diet were st ill inade­ that are widely abundant bui relatively diffi­ than representing the prim it ive condition. of oral teeth <Grasse, '55). A s im ilar muscular tjuate. cult to digest (leaves). Hence the need fo r Specia lizations of faunivores may a lso in­ specialization is found in pholidotcs, such as Our aims in this paper arc I l to describe marked differentiation of feed ing strategy a nd volve the stomach. Some ani-eating edentaLes the termite-eating pangolin, Manis (F'ig. ll, various fea t ures of gut moq>hology with gui morphology. A classification in terms of a lso lack a caecum and the gut is only seven s upplemented by a keratinized area in the greater precision and quantificntion, 21 to three dietary grades (H iadik, '78al, wi th ap­ times body length, but t he stomach contains pylorus and by the pr·esence of s mall stones. present datn from our field and laboratory pr·opriate subdivis ions, allows greater fl exibil­ st udies, 3) to account fo r allometric factors in ity, a nd seems to represent s uccessive evol u­ the d iscussion of intcrspecific differences, and tionary stages of greater admixture of the 4 l to compm·c these datn on mo rphology wi th diflerent types of food. what is now known nbout the feed ing ecology of the species concerned. COMPARATI VE ANATOMY 0~' T ilE GASTRO­ The combination of data on primates wi th INTESTINAL TRACT those on domestic and other mamma ls is use­ T he structure of the wal l of the gasiro-in­ • ful, because it a llows n group of closely-related testinal iraci fo llows a pattern common to all species with considcrnble d ictnry fl exibility to vertebrates: the inner li ning of mucous mem­ be contrasted with others which have become brane is separated by connective tissue from highly specialized for markedly different diets. a n outer cylinder of ai least two layers of While the structure of the gastro-intestinal muscle. Variation in histological structure ef­ tract is fai r·l y homogeneous nmong the differ­ fects divisions into stomach , .~ mall intestine ent orders of mammals, there have been pm·­ (duodenu m, jejunum, ileum), and large intes­ allel develop m cnL~ of different parts of the gut tine (caecum and colon). Br ief reference will in various evolutionary lineages. These refl ect be made to various configurutions of the mu­ adaptations to different food s, which can be cosa a nd underlyi ng connective tissue, which classified into three major groups, according apparently assist digestion mecha nically, by to structur·e and biochemical composition, a nd m ixing or slowing the passage of food or by the resulting digestive requirements: increasing the surface area for digestion and 1> " Animal matte r," incl uding inverte­ absorption, e.g., papi llae, rugae tfoldsl, ha us­ brates, fish, and other small ve rtebr·ates fro m trae <saccula tionsl, vill i. the secondary production of the ecosystem, In this section we s hall try to identify those which provide sources of protein and fat that structures relating to each of ihe three main a re easily digested a nd, therefore, requi re a dietary adaptations by suppl ementing pre­ relatively short and simple gut. vious knowledge with new observations. The 21 " F' ruits," incl uding um·i pe (e.g., flowers) latter are made from relaxed guts immersed and ripe (fl eshy) pm·ts, seeds, and tubers ­ in water a nd positioned io show the main most ly the reproductive p:u ts of plants ­ features clearly; a complete reconstruction, which <We foods containing short-cha in sugars impossible by photograph, is achieved by mov­ that are hydrolyzed r-ap idly in tracts of large ing par·ts of the tract while drawing, and intestinal area fo r rapid absorption and im­ adjusting the dimensions of each region after mediate use. dissection and meas urement. 3) "Leaves,'' including young and matur·c leaves, grasses, stems, as well as barks a nd Fauniuores gums - the vegetative parts of plants- which The bas ic pattern of gut structure among a rc foods usually containing pr·otein and long­ faunivores consists of a simple globular stom­ cha in sugars that require fer·mentation in an ach, tortuous s mall intestine, s hort conical enla rged stomach or large intestine. caecum, and simple s mooth-wa lled colon. This According to the predominant items con­ pattern is exh ib ited by pr·imates feeding main­ sumed, three categories of dietary adaptation ly on invertebrates, such as Arctocebus (Fig. may be recognized, a nd in this paper they a re 1), Loris, and Tarsi us. ln other mammals there referred to hereafter as (aunivore, {rugivore, may be structural specialization in one direc­ and (olivore respectively (recognition of insec­ tion or another. The s mallest ma mmalian gut tivore, camivore, and herbivor·e, with their known is found in the insectivorous bat, Rhin­ Fig. l. Gastro.intcst.inal_t rac~. of faunivores, drawn by C.M.H., with accurate scaling of proportions, main taxonomic and other connotations , contributes opom.e; its tract is only four·-fifths of body b lood vessels t.o show the d•spos1Uon of mesenteries, and conventional shading of lhe different morpho l o~,~ cal little to this a na lysis). These categor·ies rep­ length (Grasse, '55). Simplification of the gut ~eat.ures . The angwanttbo, Arctocebus calabarensis (Specimen FC, see t.able 5) is one of the most unspecialized resent a gradation, for a generalized mamma l, is extreme in haemophagous bats, such as m terms of morphology. The pangolin, Ma11is giga11tea Ispecimen MR, juven ile) is presented below with an open stomach to show the muscular ''tooth:'' the arrow marks the junction of il eum and colon determined from from food s that a re relatively difficult io col­ Desmodus, with the stomach as a blind-ending microscopiC examination or lhe mucosal wall; lhe extreme length of lhe small inlesline did 'not a ll ow itlo be lect but easy to digest (prey), through those tube, a very short colon, and no caecum. Such drawn completely unfolded, as in other drawings. 340 DAVID J . CHIVERS AND C. M. IILADIK GUT \IOili'IIOI.OGY AND DII·:T I ~11\ ,\ 1 ~1 1\ I. S 341 Ln cetaceans t he stomach has tht·ee mai n distinctive structural specialization in the gut, marmosets, and hook-shaped in cebids; in ca­ into bands) m·e lacking in Saimiri, Cebus, a nd co mpa rtments ( Harrison et al., '70). The first although its morphology may show consider­ tarrhines the base is globu lat·, the body short most pros imians, but there may be one or two and largest is covered by folds of th ick, kera­ able variation between species. a nd capacious, a nd the apex blunt and conica l, in Nycticebus, Perodicticus CFig. 6l, Lemur, tinized epithelium, the second by spira lly ar­ Some Carnivora also have this mixed diet, with a termina l venn iform appendix in hom­ and callitrichids, a nd cebids and most catar­ ranged folds of thick, glandular epithelium but retain the structural features of fauni­ inoids IHill '58!. rhines otherwise have three, except for gib­ (making a dit·ect cha nnel a long t he lesser vores, e.g., t he palm civet Nandinia feeds The colon is s imple and s traight in cebids bons with fow· <H ill , '58). The ansa coli loop curvature), and the thit·d , tubular compat·i­ heavily on fruit (Cha rles-Dominique, '78), but such as Saimiri; there is a tt·ansvet-se colon in in the trans vet·se colon is common in prosi­ ment has a s imple pyloric muco a and s tr·ong has no caecum a nd a reduced colon CFig. 6). Cebus and Aotus, and a r ight colon as wel l in mians <Pig. 6l; this part of the colon is also s phincten; at both ends, e.g., the porpoise Myoxid rode nts a lso have no caecum Ca/licehus, Cacajao, a nd Pithecia.
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