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

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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

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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 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 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 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· duodenum, is very long a supplement to seeds and fruit , places them Logolhrix, a nd a ll cata nhines Taenia coli (reduction of longitudinal muscle tentia l for fermentation. very short colon (only 10 cm , identified under vores. In the stomachs of cricetine rodents, the the dissecting microscope by the abrupt tran fundus a nd enlarged cardia ! gland region vary sition from vill i to crypts). in theit· dimens ions, separated by a fold of In the lnscctivora the s impl e stomach is varying shape (Carleton , '73). In frug ivorous followed by a very short small intestine a nd, bats the stomach is relatively complex, with usually, no caecum- as ill ustrated by Polo· a dist inct cardia! region, a long pyloric diver mogale Wig. 3l, which is adapted for feeding ticu lum fo lded back on itself, and a lateral on freshwater fi sh and crustaceans. 1n Sorex "caecum"; the true caecum is present in sev the tract is only 2.6 ti mes body length, and eral genera (Grasse, '55). some faeces arc rcingcsted to permit a second Among a rtiodactyls, the pigs have a stom opportunity fo r digestion. This phenomenon of ach that is clearly di vided into zones, and in refl ection CCrowct·oll., '52) helps to explain the some cases into compa rtments; they have an reduction in gut s ize as a phys iologicaVbehav especially long sma ll intestine, a IMge cae ioral specialization. 1n one species of Tenrec, cum, and a relatively complex colon, so that which eats foods other than insects, the tract the whole tract is about 20 times body length. may be seven times body length. Tree s hrews, These elabora tions •·elate to the inclus ion of Tupaia, which also supplement their inverte mots and other vegetative parts of plants in brate diet with fruit, have a s lightly larger their diet. co lon than other insectivores and a small Gut structure is more homogeneous among caecum CGrasse, '55). Some rodents subsist on frugivorous primates (Figs. 7, 8, 9). The stom a diet composed entir·ely of insects or other ach is essentially s imple a nd globular in struc a nimal prey. In the African murid Lophuro ture (Hill, '58). Ma rmosets show some elon mys, for example, special ization to such a diet gation of the fundus, whereas those of cebids includes a change in the di stribution of gastric are more specialized with a globular fundus, glands CGenes t-Villard, 1968). conical body, a nd cyli ndrical pylorus. Alouat Other mammals, such as some feeding on ta, wh ich also eats many leaves C4 cat Profelis cF'ig. 4). The shape, inter stones, has a n enlat·ged J -shaped stomach. Old nal features, a nd relat ive s i7..CS of fundus and World primates, other than colobine monkeys, pylorus vary slightly among such mammals, have a single smooth-walled sac; among the as described by Ellenbet·ger a nd Baum ('21) a pes it is more globular and man-like in gib a nd illustrated here by the domestic dog, Can bons, even more globular in gorillas, and more is !Fig. 5). elongated in chimpanzees and orangutans (Hill, '58). Frugiuores The duodenum is commonly C-shaped, in Fig. 2 .. The _compound stomach of t he harbor I>Orpoi S(l, Plwcaena plrocaena (035), is shown open a nd This group contains most primates, but none contrast to the elongated U-shape of other flaU.enoo m a d1ssectmg t ray. The oesophagus (cent.er) leads right into the fi rst compartment, which in turn of them subs ists entirely on fruit. All frugi mammals; in some cebids a nd all catarrhines opens mto the glandula r chamber ening into the pyloric tube, is j ust visible vores supple ment their diets wit h varying it is rett·operitoneal. The caecum is large in Oo-:ver centcrl leadmg up to the pyloric sphincter and thence into the duodenal diverticulum· the mucosal folds wh1ch ~un the _l ength of the intestine, can be seen (upper left). Photo by D.J.C. a nd Department of Anatomy' a mounts of insects and/or leaves, but have no frug ivorous prosimia ns, s hort and wide in Cambr1dge Umvers•ty. ' 342 DAVIO J . C l-l iVERS AND C. M. II LADI K GUT MORPHOLOGY AND D I ET IN MAMM A LS 343

Fig. 3. Gastro-intcstinal tract of Potamogale velox (MXJ presented as in Figure I , with the arrow marking the junction of small intest ine and colon. In Poiana riclwrdsoni (MS), to the r ight, the limit of the colon is clearly marked by a short caecu m. Drawings by C. M. H.

Fig. 5. Internal view of the stomach of the domestic dog, opened around the greater curvature, showing the oesophageal ope ning intact (at top), the extensive folded fu ndic region, and the paler pyloric region (lower). Photo by Department of Anatomy, Cambridge University.

Folivores Lepilemur a mechanism similar to refection The long-chain !3-linked carbohydrates pre (see above) allows efficient use of a diet very dominant in the leaves, grasses, stems, barks, high in fiber content (Hladik and Charles a nd gums cons umed by these an imals require Dominique, '74). This case of caecotrophy is considerable degradation by symbiotic micro unique a mong primates, a nd helps to explain bial organisms. The most conspicuous adap why the small intestine is one of the shortest tat ions are chambers for t he bacterial fermen among mammals (Fig. 11). An equally elon tation of cellulose and for the absor·ption of gated and coiled caecum is found in Phaner volatile fatty acids a nd other metabolites, and E uoticus. S ince gums r·equire fermenta either in the stomach or in t he large intestine. t ion for digestion they are classified with fol This d ichotomy might mask further diversifi ivores, a long with lndri, which shows similar cation as shown by the expansion of t he right features (Fig. 11) a nd is a true folivore. colon as well as, or instead of, t he caecum, the The rabbit provides the classic case of cae presence or absence of caecotrophy, and vari cotrophy (Mor·ot, 1882; Taylor, '40). ln !ago ation in stomach structure. morphs and myomorph rodents some faeces Fig. 4. Gastro-intcst ina l tracts of Atilax paludinosus (MW) and: on the right: Profelis aurata (MZ). Drawings by C.M.H. The large intestine is enlarged in those are r·eingested after fermentation in the ca pr·osimians which feed on leaves or gums. ln pacious caecum, so that metabolites from the GUT J\ IO I! I'IIOLOCiY AND D IET I 'I/ ~ I AM~IA I .S 345 344 0 1\ VIO J. CHIVERS AND C. M. H LADIK

Fig. 6. GasLro-i ntcstinal Lracts of frugivores. On _the left.. from Perooicticus poll~ (FM), a frugivorous pro~hnian feedi~g panly on animal matLer. On the righL, Lh c palm covet, Nandrma bmotata (MY) os a carmvore feedmg maon ly on fruot, lacking a caecum. Lhe juncLion of colon and small inLcstinc is marked by an arrow. Orawmgs by C.M.II.

herbivorous diet can be absor·bed in the s mall tion to the huge sacculated caecum for the intestine. breakdown of their fibrous diet. As in other The caecum is very coiled a nd elongated in mammals which cope with this kind of diet, specialized folivorcs, such as the "gliding" the horse has a large area of keratinized squirrel Anomalurus ruminants). Among the ruminants, the migr·ation of the ileo-caeco-colic junction ln contrast to perissodactyls, proboscids tiodactyl ruminants. Macr·opod ma r·supials, for example, there a re pure frugivores, such can be traced from the left cranial pa rt of the have a large folded stomach and a short small some edentates, hippopotami, camels, a nd co as Cephaloplws a nd Hyemoschus (chevrotain), abdominal cavity round to the righ t caudal intestine of large internal ar·ea. Sirenia ns, lobine monkeys show evolutionary conver intermediate types such as the spotted deer aspect, so tha t the caecum comes to poi nt such as the dugong, ha ve a complex two-cham gence wit h ru minants in the ir ada ptations of Axis, a nd pure fol ivores, such as Neotragus, or caudally rather than cranially (Hill, '58). ln bered stomach, with one part fulfi lling the stomach structure for folivory

Fig. 9. Gastro-intestinal tract of the barbary macaque, Macaca sylvatw (F'Ol,_ showing a rather la rger colon t.han occurs in .other frugivorous primates, which carrelales w 1lh a d1et mcludmg large Fig. 8. The disposition of the gastro-int.estinal tract within the abdomen of the long-tailed amounts of plant matter. Drawing by C.M.H. macaque. Macacu fuscicularis abomasum m·e merged into a sac is roughly sphe•·oidal (Fig. 15, cf. Kuhn, '64). The colon is long and sacculated, and the muscular wall . single tube. cu•·vature, with an oesophageal groove (rum Colobine monkeys have a similarly large caecum is of mode.-ate size (Fig. 15), as in inant feature linking oesophagus with omas The hippopotamus has the oesophagus open a nd complex stomach, with much distension other Old World primates. um) (Grasse, '55). The stomach leads into a ing into a vestibule, into which open two a nd sacculation proximally and a U-shaped The artiodactyl ruminants are well known long intestine with a wide caecum. Among unequal diverticula, and which leads into a tube distally, sacculated a long the proximal for their fo ur-chambered stomach (Comline et folivorous edentates, such as the s loth Bra third t ubula1· chamber; a ll three ch ambers part of the greater curvature (Hill, '58). These al., '68), which is dominated by the vast ru dypus, there is a keratinized cm·dial region, a have stmtified epithelium thrown into pro sacculations are produced by the reduction of men, divided into dorsal and ventral sacs by small "rumen" with two diverticula a nd an jecting fo lds with numerous papillae. There is longitudinal muscle into two or more bands muscular pillars, and covered by kerat inized oesophageal groove, and an "abomasum" wi th a very long intest ine, but no caecum. Camels (taen ia). The stomach of African colobines is squamous epithelium with papillae of varying an expanded pyloric region with a very thick have a stomach that is smooth and ovoid in more elongated, wi th the tube bent back on size and shape (Fig. 16). The oesophagous 348 DAVID J. CHIVERS AND C. M. HLADIK GUT MOIWIIOLO(;Y AND D IET IN MAMM ALS 349

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Fig. 11. Gastro-intestinal tracts of folivorous prosimians (iefl.) and a rode nt with e xtreme development of the caecum F'ig. 10. O n the left, a n internal view of the stomach of the siamang, Hylobates sy,uiactylus (P27l, opened around re lated to their specialized diets. The sportive lemur, Lepilenwr leucopus ( 00), upper Jell, has the shortest small intestine lesser (to le ft) and greater curvatures and laid out in a dissect ing tray; the oesophagus open s at the upper le ft, with a dark of all primates; it is the only genus in which caecotroph y occurs and the ileo-caeco-colic .. plate" (a rrowed) probably plays region of cardia) gland s, and the pyloric sphincter is at the lower left. On the right, an external view of the s iamang's a n importa nt role in regulating this behavior sheep, pentagonal in ments, with the ventricula r groove running vegetation at high altitudes, where cattle and dist ingu ishing features in t he mammalian goats) and is covered by small conical papillae. from the first to the last; only the terminal goats cannot graze. gastro-i ntestina l t ract has empha sized the The rumen connects with the glandular part fi fth of the third, tubular compartment has J anis ('76) suggests that horses also have simple stomach and long small intestine of of the stomach through the sma ll ovoid omas true fundic and pyloric g lands (Val lenas et al., a n advantage over cattle in their abil ity to mammals known to subsist mainly on a nimal um, wh ich is part itioned by many leaves of '71 ). While th is chamber has mucosal pleats use a more fi brous diet of low protein content, matter, and the elaboration of the stomach varying s ize for water absorption. The inter over much of the rest of its length, the first by taking in la rger quantities which pass and/or sma ll intestine in leaf- or grass-eating na l surface of the glandula r abomasum is two sac-l ike compartments have areas of large through more rapidly, rat her than developing for ms, with frug ivores showing an intermedi t hrown into fol ds throughout the fundic region gla ndular saccules, which not only contain a more efficient d igest ion of cellulose. In dis ate morphology (Table 1). Most mammalian (Fig . 16). The intestine is again very long, the considerable amounts of ingesta, but are ca cussing the evolut iona r·y strategy of equids, feat ures of gut morphology, except fo r t he caecum is relatively short, and the colon is pa ble of frequent eversion. Thus, they seem in terms of physiology and ecology, she con more specialized, occur among primates, long a nd ela borately flexed and coil ed. more likely to contribute secretions to buffer trasts their digestive system with that of ru m which form a n array derived from primitive Effo rts at demonstrating homologies with inants, and refers to t he greater extension of unspecia lized forms and which have not at stomach con tents, rathe r t han to absorb caecum and colon in those nonrumina nt her the rumina nt stomach of bovids ha ve had tained the extreme adaptations found in other water. It is claimed that such str uctures a id bivores tha t do not practice caecotrophy. orders. Didelphid m arsupials, adapted to a sim- 350 DAVID J . CH! VERS AND C. M. I·!LADIK

Fig. 12. Gastro·•nt.cstina l tract of the tree hyrax, Dendrohyrax d orsalrs (MU>. showing the most complex arrangement of cncca and colon. l hc exuct functions of which a rc not yet known. Drawing by C. M. H.

ordeL Didelphia marsupials, ada pted to a sim QUANT ITATIVE ANALYSIS OF GUT MORPHOLOGY ilar ra nge of d iets, show even less mor·phol ogica l speciali zation than loris id a nd cheiro Methods galeid pr-imates (Char les-Dominique and Hladik, Gastro-i ntestina l tracts were taken from unpubl. observ.); this supports the idea that 180 indiv iduals of 78 ma mmalian s pecies in the gastm-intestinal tract has para ll eled other England, Fra nce, Morocco, Gabon, Madagas aspect.<; of ma mmalian evolution . ca r, Sri Lanka, Malaysia, and Panama. There It has been seen how variations in propor a re 117 pr imates of 48 species, 13 temperate tions of di fferent parts of the tract, wit h cer mamma ls of 7 species (2 aquatic), and 24 tain structural peculiar ities, can often be re tropical nonprimate mammals of 17 species. lated to difTe r·ent as pects of diet. [n some cases One-hundred forty-eight specimens were caught the correspondence is not obvious; references in their natural habitat by hunters dur ing to the lengths of various regions are inade pest control operations or by local people for quate for a full functional interpretation. A food; 29 a nimals, mostly pr imates, died in fuller quantitative analysis is necessary to captivity, from illness or old age. In addition, investigate the relationships wi thin a nd be 26 domest ic ma mmals of six species were put tween dietary groups. Ha ving set the scene down during routine marketing, research, or a nd illustrated the problems in this survey, teaching operations. we can now proceed with this more detailed Larger sampl es of certain species indicate evalua tion. the level of intraspecific variation, and the f'ig. 13. T he large in test ines of the domestic horse <0141 showing, above, external shape and large size of the caecum ICenterl surrounded by dorsal and ventral loops of the primitive right colon, with ster na I and diaphragmatic flexures (lower) and the s ma ller s ize of the trans verse and left colons, also with taenia coli (lower left corner). Below, the internal appea rance uf the caecum after opening and washing , befor e c utting the t.a en io coli, which increases the length from 80 to 240 cm. Photos hy the Department of Anatomy, Cambridge University. 352 DAVID J. CHIVERS AND C. M. HLADIK GUT MOitPIIOLOGY AND DIET IN MAMMALS 353

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Fig. l4. Internal aspect ~ f the stomach of the domestic horse

reliability of small samples. Thirty-seven of a nalysis, because of the distortion introduced t he 78 species a re represented by only one by varying lengths of muzzle, especially when specimen, 15 species by only two, and 10 contrasting primates with other mammals. species by three individuals. There a re four The guts of most specimens were examined speci mens of Galago (Euoticus) elegantulus, a nd measured in the fresh state (or were G. alieni, G. demidouii, Alouatta palliata, Cer preserved in a saturated saline and then copithecus cephus, C. nictitans, Presbytis ob washed in water); seven had to be fixed for scura, and the domest ic goat; five specimens later study in 10% formal sal ine, but meas of Arctocebus, Cheiroga.leus, M iopithecu.s, urements under these conditions are affected Vulpes, a nd Dendroh.yrax; six specimens of adversely by contraction at the time of fixa Presbytis melalophos and the domestic cat; tion. Many specimens were examined, drawn, and nine domestic dogs. a nd photographed with the guts in situ and/or Specimens were weighed intact, which was displayed under water in a large dissecting Fig. 15 . . The gastro-intestinal tract of the dusky leaf monkey, Presbytis obscura (P l9). Upper r ight, the disposit ion within not a lways possible in the fie ld, and their tray. The dimensions of each region were then t~e abdommal cav1ty; note the large s1ze of the stomach occupying the upper half of t he view, and the coils of colon below (cf. lengths were measured from bregma to is measured, for calculations of area and volume, ~ ~~- 8). Upper left, t he stomach (part1ally d1stended w1th water) displayed to show the large sac, the gastric tube (on t he n ght), and the pylorus (lower left). Below, the complete abdomma l part of the tract, with a different aspect of the stomach on chium a nd from tip of nose to base of tail. The and weighed a fter the removal of excess mois the left .. and the cotls of small mtestme, caecum (dJrected downwards ), and colon leading around into the rectum success· 1 latter measure of length was not used in this tUJ-e. to the nght. Photos by D.J.C. ' lve Y ~~C!~ c.> __ o 3"" ~ -e a~~ ~ "'... 3 ~ ? ::... ;:: c Cl:l :J 0) '<3<:lQ.' ·~ fas ~;;-~~ :!. ?n; .. ~ 0 - ~; ~ - ~ ~...:a2 :r <> " ~~~~ ~~::=~ ""=~~ ~ g_ -· ~ - " c: 0 "' ., ~- g g- ~ c 3=.,2, > ~ g~-g . g- c ~ ~:... ~ ' ~ c: z. s () ;:-c" 3_ ., 3 :t ~-c - · n ~ =:IJQ· ;r < tt~;-:ro ~~ .... -, ;:l Ill"' 3 :;·~ ;. :> ., ., .. z =;.~ . Q. ~tO =o c E:o~~ 0 Gel 3 0 CfJ 5:~ ;~· ~ ';-3?.;"c§ = ;; 0~- ~ f;: 2 ~ =-~ 6 :>; s 2~-g tJ'J. (:1 ':"""' ~~~c 0 ~ Q.:g ~ 0 Cl/ ctl 'O:::I:r., Q)~ ~ - ~ ~-g? g~~;. ;;2,3tt~ ....,..,._a.:T' > :r - · 0 :I 0 ~ = ~ ?~~ 3E.!Sa '<• n-· "0 a" ~'g ~ -g 3 ., tll ... .,c:r ....,....,.,~ob Q..,...,...:J (IQ :r :::r 0 ct1 RI RI-,

TABLE J. ~ u mmary o{ adilptationo of the ga>lru> order> of mammal, arrordmR to tho predomman reduced z Artiodactyla zones, even chambers very long large rei. complex ..., Rodentia extensive cardial glands, none ;:; separated from fundus by fold ....;~ Folivores long, tubular, sacculated, z Marsupalia, macropod long wide ::: grooved > Primates ;:: lemurid caecotrophy si mple very short elongated, coiled ~ colobine sacs and tu be > Proboscides large, folded short, capacaous huge, saccul. large loops en Sirenia 2-chambered very wide Hyracoidca 3 caeca most complex Perissodactyla cornified area huge, saccul. large loops Artiodactyla hippopotamid 3 chambers very long none NW camelid 3 chambers OW camelid 2 sacs, smooth, ovoid bovid most elaborate 4 chambers, huge elaborate long large long, folded and coiled Edentate cornified cardia, 'rumen', groove, 'abomasum' Rodentia caecotrophy cornified variably capacious v. coiled, long w Lagomorpha caecotrophy ,,"' ' BL ~ Body length. 356 OAVIOJ. CHIVERS AND C.M. HLADIK GUT ~IOI! I'II OI.OGY A:-

Techniques wer·e standardized throughout calculation from the weight of unit area; this stomach, where the whole clearly does not between the two authors, on occasions when pr·ovided a means of checking the accuracy of V = = 4.19 . ( fable 3). appr·oximate a sphere. While some compart they worked together, so as to obtain compa length and breadth measurements. Error re 3"4 (217L )" (6 283L )'· ments resemble spheres (the ruminant retic rable accuracy. Severa l hou rs were allowed to sulti ng from the different methods, or from ulum, rumen a nd omasum, a nd the colobine elapse a fter· t he death of the individual to repeated measurement s, amounted to less Vo lumes calculaled from s urface a rea are presaccus a nd saccus), others approximate cyl permit complete relaxation of muscle tone in Uwn 5'!1-. about 1 ~ less on average than those fro m inders (the ruminant abomasum and the co the gut wal l. Measurements of length a nd Little merit was pl aced on measuring vol greater curvature or water·-filling (Tables 2 Jobine gastric and pyloric lubesl. Thus, vol breadth of stomach, small intestine, caecum, umes by distending parts of the gut with water and 3l. umes have been recalculated along these lines and colon wer·e then made without str·etching, (even if the pressure could be controlled), if While a ll species can be compared against

t.,,oJ '" plots on a logarithmic scale represent species • <11 ,;.,., I •Jit~J.OMo '" culations, are displayed in ta bles 5-8 for pro 0 Hl" ti•J,..., fr 1 II.IL't I Ill" s imia ns, New Wor ld monkeys, Old Wor ld means, with the range of variation ma rked for monkeys (cercopitheci ne a nd colobinel, apes, those species with four or more s pecimens. ~ ~~~; Ji)[)[filll]Ji[l[f]ft][illi(Jf][IJ]ill}:;::~~ ~~~][ffi][§~~ f[;~~~~j[-~~ [[~I.: Ji::}lm [][[JJJ[[][J[f:;{ :;{ :;~~~p~~;~=:::~~:~ .. ·~~r! "'/~~·:"'''~' ~' ~--- domestic ma mmals, a nd wild mammals (tem Wh ile t he va lues of the coefficients appear 0 perate and tropica l). Emphasis is placed on generally to represent structura l adaptations "'~ A luu.. tto.~ 1"" 111<11-' adult animals taken from their natura l habi ind icative of the relat ive proportions of animal .:! .::•: Cf"I"COC'ct.u"' • 1111•·1• • a nd pla nt mat ter in t he diet, only those below ~s ','jj:' -:_:j:,~::!:i!:!!i!!::.!':!ii!:::::·!·l!lllijj:jjj:!:!:jj:jj!jjjjjj!ji·j:jjj:!!i!j!:_:j,j:j:·j,\:!i!:i:i!!:,j.jj.jji!!i!.:j:!::i::i:·:~~@tt@rutl:l:.l!i!:ii:j!i~l:l:::!l! ili!!:!::j::!.:: ;~;Prt!Sbytr":;:.:·;., r 1-.t ol.,. tat, since cons iderable changes in gross d i I'W<.. d ..;ol "'""'""" 0.2 can be regarded as true faunivores a nd P~S short pe1·iods, e.g., from a 33'/f reduction to an only those above 3.0 as exclus ive fol ivores. PTN>byt I' I•" Ut .,I l OOK increase in the surface a rea of the small lnterspeci fic variation may be app1·eciated intestine in some cercop ithecines (H ladik, '67). more clearly by compa ring coefficients within Prt·~b'/ f 1"' '"''l" lopho.h . '""""'"' Immature individuals a re pa rticularl y suscep (a nd between) the various taxonomic or eco '<1 t1 troylu dytcs logical groups of mammal (Fig. 18). In each of Av .th l ldnHICT t ible to dieta ry effects on gut proportions, and Ct!n.-opttik· ":u~ n1.. c I(.,, their measurements should be treated with the ·e groups dietary categories, as suggested ---:1-- f're«:~:'" rub1.un·l • by st ructure, are separated , albeit in d ifferent • I ~~~"' ., z., ,-v.,tu caut ion; the stomach and colon a re relatively • I f'VIloJ pclq -..Jt:'bHI"'S J•l H'diU a lso liable to distortion from the functional 0 I Afk»U lllt U .. t t I.J~I dominated by stomach a nd/or large intestine e I ,l!f.l,;.J d a..~J .. tt<.l state. I 5<~o•t .. t t odl I (for digesting leaves), and the few lower ones, 1f i Op ~tht.-cu~o :.tl.•t• •" Gut Differentiation. The sizes of stomach a mong prosimians a nd ceboids, where the 0 Ht'J t<><;C l UtU rufc1t't I ·IJJUIII CO! r cops tht••.:v.9 o11 thtOp , a nd la rge intestine relative to small intesti ne, small intestine predominates (for digesting • AO ttJ «: tt lVI t'I'CfiiC'UlU"' in terms of su rface area, weight, and vol ume, animal ma tter). The categories of "faunivore," __:_ HyloboH f>"l "'lljM 1<1 tt~lu-. provide a s imple qua ntitative index of gut "f1·ugivore," and "fo livore" are esta blished ac Citid'i .J llt>fll tnr 1 s t .. rd•qr.JdoJ .. different iat ion, wi thout regard to the s ize of cording to str uctural discontinuities, and at • Fl"'liS the animal. These coefficients of gut differen this stage they can be no more than suggestive 0 scau,- u· ~·uJv<~ra -- Vul pe!> vul IX''~ --<>- tiation va ry cons idera bly in the ma mma ls of diet. The overlap between them would seem • A l,P/f>'S f\<.I OJSC'U'i to result from inters pecifi c variation in the W90 t hru i 4 10ll"lo.:h4 s tudied, f1·om t1·acts t ha t m·e dominated by 0 • I'UillS CriCu:.piS s mall intestine in faunivo1·es to those that are deg1·ee of admixture of animal , fru it, and leaf C.tJt~qO d efltldOVl I • P4plo P

~}:~ ? ;~:ff! J IS .JU r dt.J TABLE 4. Estimation of stomach uolume.OJ: complex stomachs# treated (a) a.'i a \::~ ~ ~: ::: J ., NIUilt'd smglf sphere arrd (b) as a combination of spheres and cylinders P• nther.a pdtdu~

Volume, cm1 Cf!nl"'ttfl "lf"I"V fl l lrw ---- \:~ }~j ~~~~~:u~ : s: :~vtll r u -: S pheres :)f~t=~ Uoonto..·t>t.us mtdd:. & % reduct.ion Spec:1es Single s phere CylinderS of laU

F1g. 17. Coefficients of gut differentiation from surface area plotted in order of magnit ude (smallest ''alues below) on a lo,.;:uri thmic scale, ind icating by arrows and stippling the t hree main morphological die1.ary categories and the overlap between them, which may or may not incl ude s pecies with intermediate diet. Range of values are denoted by horizontal lines for species with more than one specimen. w TABLE 5 . Measurements of body length and we1ght, and of surface area, u:e~ght and volume of stomach, smollmtestine, caecum , and colon 111 0> prosimians a ne/ New \Vorld monkeys 0

Body Body Surface area, cm' We1ght. g m Volume, cm' ldent . length we1ght Species no.' Sex cm gm Stom. S.I. Cacc. Colon Stom. S.I. Caec. Colon Stom. S.I. Caec. Colon Prosi mians AY2 M 22 220 14 146 10 29 5 21 3 OT M 22 160 30 126 9 36 15 18 7 Arctocebus ER F 22 190 24 110 10 38 11 15 I 5 calabarensrs EV ~1 21 160 26 Ill 10 4 1 5 6 0 3 13 17 2 6 FC ~I 21 180 12 88 6 29 5 I 3 4 11 I 4 BP ~I 24 34 337 165 165 19 39 87 26 Avah1 BQ J-1 25 56 309 107 95 39 43 40 12 0 laniger > BR F 25 76 335 186 255 62 43 72 54 < AK' :\1 21 23 94 4 22 10 11 I 4 0 BF' M 22 28 143 5 51 14 15 10 ' (') Cheirogaleus ::t BC' F 23 20 162 7 33 9 18 I major < BH' F 23 40 192 10 25 24 26 2 4 C'l ON ~1 21 35 213 6 45 19 31 2 9 i,j; OS F 17 230 13 42 41 116 5 5 22 >z 0 Euolrcus DU M 18 270 19 4 1 40 123 8 5 6 26 (') elegantulus DW M 19 340 12 30 36 129 4 3 6 21 OX F 18 320 15 36 33 128 6 4 5 27 ~ ::t AY F 19 230 20 85 8 51 8 11 2 9

Go/ago BC F 18 21 11 2 8 50 3 5 4 9 13 I 6 alleni BC2 F 18 250 16 112 9 33 3 5 5 6 17 2 4 ES M 17 260 37 144 21 78 21 23 4 16 AZ M 11 48 6 24 3 5 0.4 0.5 0. 1 0.3 1.5 1.0 0.2 0.3

Galogo BA M 11 60 5 36 4 12 0.5 0.5 0.2 0.3 1.1 ~3 ~3 0.8 demidooii BA2 M 12 5 34 5 14 0.6 0.7 0.2 0.4 1.0 I~ 0.4 1.1 BB2 M 13 7 59 3 16 0.5 0.5 0.1 0.4 1.8 ~2 ~9 1.3

Lepilemur BF' F 26 45 68 174 166 28 11 81 35 mustelinus

Lepilemur DO M 24 630 52 106 137 2 13 35 16 45 49 leucopus

L orl!i 01 22 2~0 19 !!5 4~ 8 10 3 6 tardrgradus

Microcebus 1 1 5 32 6 murinus

Perodicticus FM M 3 1 1160 36 200 2 1 333 20 34 8 119 polio

Phaner os F' 20 270 14 95 43 130 5 28 6 27 fumfer

New World monkeys BU' F 23 113 8 57 19 2 11 c Saguinus BV M 24 19 150 14 67 8 36 3 15 c geoffroyi CA F 23 66 157 14 72 50 38 4 2 1 ..., CH' M 20 420 26 183 12 46 ! 3 39 3 8 _.. ~

Leontoeebus B:--1' ~~ 25 13 116 6 23 19 3 mida.~ § Aotus DA F 28 970 84 288 47 120 72 61 22 37 Q trwrrgatus ... > Saimrn BX M 30 6 1 308 16 53 45 70 14 % oerstedi BY F 28 49 342 18 48 32 103 4 12 ::::: BZ f' 30 63 356 19 46 47 8 1 6 11 0

Cebus CB f' 39 I l l 852 20 ~ COpUCinUS ~_.. Cebus BL' M 40 68 462 38 53 106 6 6 :::> g riseus BM' F 40 48 519 4 38 31 134 5 6 ::: P1 2' ~1 41 1470 200 9!5 184 490 33 34 10 44 266 447 I 17 28 1 > 'fr. Alouatta CR :\1 51 430 1052 289 1059 839 534 391 959 pal/iota BW M 50 230 719 148 630 328 302 145 47 1 BT f' 53 296 815 156 778 479 339 138 642

A louotta BK' M 6 1 180 1106 150 578 227 556 163 422 seniculus

Lagothnx P3 1' F 59 5670 264 2 115 18 1 660 89 164 46 140 403 757 113 289 lagotricha P39' M 56 10430 488 1796 293 699 96 8 1 30 77 ! 014 693 228 442

Ateles BO' F 53 172 765 101 232 212 252 54 95 paniscus

1Capt1ve. 1F'1 xed. JJm moLUre w 'Nos. AA, BA , cl<: C.M.H .. nos. POt. DOt, el< D.J.C. 0> w 0> TABLE 6. Measurements of lxxly length a nd werght, and of surface area, weight and t'olume of stomach, small rn testrne, caecum, and colon in Old \Vorld monkeys ""

Body Body Surface area, cm" Weight, gm Volume, cm3 !dent. length, weight, Specaes no.• Sex cm gm Stom. S. l. Caec. Colon Stom. S I. Caec. Colon Stom. S.l. Caec. Colon Cercopithecine monkeys Miopithecus, I P1 3' M 38 950 59 451 40 212 26 2 16 43 96 16 76 talapoin P37' F 28 880 64 594 30 258 26 12 48 142 12 106 AM F 30 59 157 26 214 43 14 18 8 1 AO F 29 44 149 25 87 27 18 12 20 Bl M 24 49 231 12 122 32 34 4 32

Cercopithecus EM F 42 2650 187 784 76 371 240 218 46 192 i O 446 45 325 13 15 5 30 55 71 18 129 0 cephus EY M 49 3800 > EZ F 41 2400 144 582 60 458 27 18 10 43 163 107 48 220 < 572 FD M 54 4500 155 1008 56 877 37 8 1 17 86 181 321 83 0 "- Cercopithecus EO F 46 3850 206 710 83 827 61 49 12 132 278 260 69 605 Q neglectus AR F 46 144 556 69 728 163 132 47 444 P28' M 58 11340 289 1382 77 982 61 100 11 119 460 448 43 518 < ~· 99 760 87 654 93 195 75 340 ~ Cercopithecus AP M 57 > nictitans AS F 47 73 763 65 563 59 179 48 280 z AX2 M 58 177 798 95 753 221 214 80 410 0 EL M 59 6500 120 927 80 8 16 61 56 13 88 124 225 57 441 3: Cercopithecus AB' M3 37 34 169 13 143 19 17 3 35 :r r aethiops AC ' F3 40 14 234 3 1 105 5 42 15 25 > 0 AN F 55 124 559 69 977 130 162 54 799 Cercocebus AX F 51 91 657 67 580 82 189 51 268 " albigena FK' M' 47 3700 88 453 20 374 24 51 6 62 78 108 8 164

Macaca FN F 51 270 1187 72 1323 416 434 46 954 sylvana FO F' 38 180 795 59 826 226 222 3 1 503

Macaca Pll' 39 3350 77 618 8 1 377 15 56 13 32 64 160 47 123 mulatto

Macaca OH ~ 42 226 587 62 772 320 185 51 558 sinica DJ' M 47 122 638 25 310 127 191 9 125

Macaca P29 M 37 2700 143 10 11 28 693 15 22 3 3 1 160 346 8 364 {ascicularlS P45 M 40 3900 306 918 29 659 32 70 9 66 502 268 8 320 P46 F 40 3050 178 1144 67 866 37 56 8 73 223 390 40 568

Papio FK M 72 16600 402 2854 64 1894 760 1596 47 1518 sphinx EP F 51 6100 250 1143 50 1228 76 97 13 163 372 409 33 1395 FR F 63 12300 322 2435 70 2240 123 296 13 332 543 968 195 1782

Papio AF' F' 29 20 173 4 67 8 19 11 papio

Colobine monkeys Colobus AQ F 56 1021 556 26 549 2055 107 13 2 18 polykomos FB F 58 6500 1056 925 15 630 154 149 5 72 2162 184 6 301 Cl c..., Presbytis OF M 63 1585 1673 105 978 3974 633 80 845 s: entellus DL M 65 10000 1439 1167 140 760 3438 330 104 505 0 ;;; :;:! Presbytis DC F 48 938 740 139 548 1814 181 77 275 6 senu DM M 59 1416 687 139 548 3357 162 96 336 5 Cl Presbytis P30 F 50 6850 1694 1929 90 966 265 60 9 99 4831 604 64 645 -< cristata P33 1 F 53 5440 11 75 1329 30 607 182 2209 385 12 285 > 65 5 59 z c; Pres bytis PIS M 50 7960 1363 1953 64 670 180 77 8 66 3237 699 41 343 obscuro Pl9 F' 45 4230 956 1311 52 558 105 53 4 42 1788 397 27 264 ..,--- P26 M 53 7200 1351 1969 88 902 154 62 6 76 2974 734 51 588 P32' F 56 6350 1282 1129 90 869 211 45 8 50 3139 327 64 546 s: > Presbytis Pl4 M 51 6860 1020 1386 60 532 114 82 6 52 2072 336 34 156 :: melalophos Pl6 M' 44 5220 694 1075 23 369 109 76 3 44 1128 247 8 132 s: PI? F 47 6410 1648 1796 60 552 145 107 6 63 3521 5 17 36 224 > P22 M 49 6510 1078 1389 42 695 90 50 4 42 2158 395 20 362 F;; P23 F 50 7340 1382 1695 68 848 124 71 8 50 3327 588 43 469 P24 F 52 6880 1274 2021 38 612 150 60 7 71 2296 633 14 292

Presbytis P38' M 56 6350 1125 1672 45 637 105 21 38 2259 505 20 329 rubicunda

N o.salis P25' M 64 15880 1978 3 120 100 1234 357 153 6 82 6523 1127 66 655 larvatus

Pygathrix P34' F 53 4540 1243 1512 36 578 137 63 5 50 2960 444 12 261 nemaeus P30' F 60 3630 1431 1601 80 854 200 47 4 45 3442 53 1 42 433

1Capti ve. •tol xed.. ' Immature. c.o 0> Nos. AA, BA. etc. • C.M.ll.: nos. PO! , 001. etc. = D.J .C. w <:<> a>....

TABLE 7. Measurements of body length and weight, ond of surface area, we~ght , and volume of stomach, small intestiM, caecum, and colon in apes, domestic mammals and temperate wild mammals Body Body Surface area, cm' Weight, gm Volume, cm' ldent. length, weight, Species no.• Sex cm gm Stom. S.l. Caec. Colon Stom. S.l. Caec. Colon Stom. S.l. Caec. Colon

Apes Hylobates P05' M 40 5000 204 453 15 383 58 8 1 4 74 274 154 3 259 lar P06' F 40 5400 104 268 6 403 53 35 2 68 100 68 2 267

Hylobates P41' F 47 7260 304 592 77 1128 56 77 17 144 499 596 34 920 pileatus c :::> Hylobates P27' F 52 11340 457 2278 75 1557 146 150 10 230 919 1007 34 1891 c syndactylus P40' M 56 7250 140 1708 8 1 954 55 183 22 184 156 697 58 883 " (') :t Pongo P42' M 61 8620 256 1263 70 978 71 124 17 157 385 461 56 107 1 < t'l pygmaeus P35' M 95 880 6564 155 5774 331 568 22 980 2457 4046 55 7800 ~ > z Pan AD' F 83 472 1700 162 18 12 965 815 91 1451 c troglodytes EN M 72 34000 690 3761 286 2925 1705 1967 407 4335 (") 3: :t Pan EQ M 84 51000 1087 4018 590 4813 3370 1897 955 7006 r gorilla > !2 ;>::

Domestic mammals Felis D09 M 45 4000 144 345 8 125 24 104 17 163 60 2 48 (cat) D12 F 40 2450 104 249 7 87 20 67 14 100 36 1 25 D13 M 43 2730 120 372 9 123 16 84 17 124 7 1 2 40 D18 F 42 2450 106 348 12 148 17 42 11 102 75 3 62 D19 F 42 2700 132 374 11 130 21 43 11 143 86 3 52 D20 M 46 4340 117 291 8 111 24 60 13 119 41 2 36

Canis 003 M 78 13500 300 1030 40 225 133 263 8 42 490 238 16 00 (dog) D04 M 59 7250 215 585 30 126 46 125 5 30 297 102 8 43 D05 F 60 10680 426 992 37 208 109 198 8 42 826 253 11 75 DOG F 58 9400 196 562 25 75 52 130 4 26 258 136 10 m D2 1 F 81 12550 344 1445 40 192 153 327 6 53 599 483 16 61 0 24 F 48 4750 162 776 20 135 48 170 7 24 194 196 5 54

Sus D27 M 54 7650 381 1057 30 170 107 285 14 35 701 294 10 58 (pig) D29 M 55 7450 193 656 30 132 7 1 178 5 23 253 193 10 45 D30 M 55 7950 216 696 30 99 68 163 5 21 297 166 10 35 Dl5 M 98 47980 160 14425 440 4702 333 1144 70 685 1597 9119 700 3710 D41 126 65320 917 9968 432 6246 464 1010 78 984 2610 4828 619 5855 D42 123 60780 792 14036 630 6824 332 1327 128 1106 2097 7420 902 6042

Equus 014 M 157 202730 728 10991 9240 27993 675 3204 1395 5450 1847 6207 28296 50551 (horse)

Capra DO t M 127 84950 31297 8967 300 5 13 1 2250 7 10 67 585 16220 2924 286 2452 (goat) D02 M 145 94220 36475 11948 437 6047 3210 950 98 878 20878 4277 282 3339 D33 M' 84 2 1900 15029 6102 275 1830 686 607 27 186 6317 1747 273 592 0 M:t 67 1 579 33 24 1 5086 1208 164 467 c D34 82 23850 13195 4901 187 1601 -: ;::: Ouis D43 104 40820 14110 15780 490 3642 1062 925 61 384 7989 6414 530 1587 0 (sheep) 044 99 47170 13760 10591 403 2496 1093 868 58 393 7568 3496 461 533 ::!1 11702 10299 150 2066 959 798 57 368 8040 3523 119 701 D45 99 38100 Q 0 0 -< Wild mammals (temperate! > Oryctolagus MB 43 2600 157 958 529 431 185 2 14 353 117 z cuniculus c Sciurus D47 M 24 600 26 307 54 136 5 9 3 13 43 29 30 0 ::: vulgaris -: Mustela D38 18 140 30 13 1 0 12 16 19 0 2 nivalis z M us tela D39 24 30 42 121 0 19 2 5 0 26 13 0 2 s: > erminea ::::... 406 929 48 229 78 106 4 25 768 329 23 9 1 > Vu/pes D37 M 64 8000 1n vu/pes D46 F 65 5500 308 993 75 336 50 122 5 21 508 372 30 204 D48 M 52 6250 320 992 56 232 68 130 7 27 538 329 18 100 D49 F 58 5750 352 854 48 279 57 104 5 28 621 302 15 151 D50 M 56 6200 259 929 54 236 60 105 5 26 392 340 19 117

Phocaena 0 35 M 130 29030 1151 11213 11213 11 2 13 462 1125 3672 6831 phocaena 0 36 F 1501 2 1309 2 1309 2 1309 636 1928 547 1 18733 D40 168 50450 1501 12455 0 53 885 1333 0 9 5471 9257 0 25

Tursiops D51 230 450000 1588 25540 0 389 200 430 10 10 370 1 2091 3 0 208 truncatus ea <:<> •Capt-ive. 1 Fixcd. 11m mnture. a> 'Nos. AA , BA , et<:., C.M.H.; no.o. POl. 001. etc. • D.J.C. 01 TABLE 8. Measurements of body length and weight, and of surface area, wetght, and volume of stomach, small intestine, caecum, and colon 1n ~ nonprimate tropical mamm als a> a> Body Body Surface a rea, cm• Weight, gm Volume . cm3 Ident. length, weight.. Spee1 es no. 1 Sex cm gm Stom. S.l. Caec Colon Stom. S.l. Caec. Colon Stom. S.l. Caec. Colon Wi ld mammals (tropical! Atilax MW F 45 2380 70 575 9 74 31 86 3 19 55 paludinosus 124 21 Potamogo/e MX 23 740 19 368 0 39 22 t•elox 0 8 67 0 11 t\1anis ~1E 28 1550 189 5 17 0 134 tricuspr s 245 85 0 55 Manis M R M' 23 1950 39 6 15 0 50 12 34 0 11 gigantea 23 73 0 10 Epixerus MC ,-, 24 580 30 201 21 52 4 6 2 16 22 5 6 ebii ~11 F 23 540 48 2 16 2 1 68 5 6 I 4 3 1 26 6 0 flelzoscwrus MH M 12 20 290 5 1 190 48 63 6 3 3 34 > rufobrachwm 25 11 8 < Funisciurus M K 0 16 161 15 30 3 5 2 6 anerylhru s 18 '- Funisciurus ML 18 268 16 48 10 3 7 S? pyrrhopus 25 3 Anomalurus < ~11" 24 10 2 16 90 93 5 9 7 5 3 {raseri 34 22 11 "' E•dolon MF F ill 14 190 0 2 > heluum z 0 Dendrohyrar MC 40 1405 114 311 350 335 8 1 48 196 74 (') dorsalis ~1 0 F 39 2323 140 456 482 572 54 25 6 1 43 11 0 73 331 ~ MP 38 2066 169 120 391 393 549 44 29 48 33 86 MU F 3 1 14 15 53 129 143 3 15 275 304 25 17 30 12 114 r MY M 44 2720 55 80 126 588 362 594 54 40 60 44 94 131 > 156 SO? ;>; Nand inia MD F 42 2400 143 481 0 150 160 142 0 53 binotala MY M 45 2250 105 420 0 98 34 65 0 23 10 1 100 0 27 NA M 43 2440 60 209 0 73 22 38 0 16 43 37 0 15 Bradypus MA 46 60 1 411 0 262 tridactylus 986 97 0 88 Poiana MS 29 5 10 36 184 27 11 17 richardsoni 3 20 28 6 G enetia MQ 50 1480 63 274 2 48 19 54 serualina 5 15 47 42 3 15 Profelis MZ F' 57 5230 134 404 2 92 58 130 a u ra/a 26 120 88 32 Pa nthera MM M' 84 15700 42 1 1580 22 342 13 1 392 4 pardus 61 8 13 593 10 163

•Captive. 'Fixed. 1lmmat.ure. 'Nos. AA. BA. etc.- C.M.H.; Nos PO I, DOl , etc. • DJ C

s""0 ~ ; g :;. !!- :.1; "9.1:; (") 8 0 § r ~ ~ ~ 0 ~i m § l: 0 -n ~ I ~1 1 n r ~ "' -n mz g-~ ~ 5 ;:: (") I ~ 5I ~ 0 3 <"> m ~ z 0 ~ -· I 1° 0 ~ c z i m 3 ~ tii " -i tii I ~ < 2 . 3 I; N- ~ "' < !:.o"' 0 ~· 3 ...,0 ~~ ~... ro Cl ~~ c 0 ~ ~ -i "'- "'~ Q Cl n . -n c £' ; , -n --; 0 0 m ... ~ .m!!l§l lill!mtriiiiiiiiM-·IIIIIIBIIi~Jiil ! ::0 l I I I I I IJ. 0-- m r g a' 3 z ..., ~ -d V! -i "' -:r ,. I 0 c " •• c- § 2.c c '- cD 0 ~ er -,)> ~ ;;a Oo .. :;:· c 0 ~ I• i>"ll (") 0 I• • :% ro ..., v !; ~ o ro ~ ~ ..., 0 ill:::,,,,,r::::::o·O·O• :::::::::::::: v ::::::::::::::::: :::::::::::::::::::::::: g a1 ro o ... l !·:.:t:~}I:IIIImt:; !; ~ e - ::::::::::::::::: ·:·:·:·: :::::::::::::::: -· o VI ::::::::::::::: :::J::::::::::::::··-·.·.·.·.·.·.·.·.·.·.·.·.·. "'3 . g_ - c; ======:ttt:::::~l~~ll!ll:!i!i!i!iiiiii~i\~,~illlll.i.lllllli.I,I.JiiliJ!I:It,J 7 VI 3 I! ~ 0 -~ · 3 0 --> as 0 (") ::: :::::::r < ::: f; 0 ::: ""x - · + ..,_ ..., &. g :!n ro > "0 ro o .. VI ?/> :g 2. cr ro • a " - · cn ~ . ~ ; 3 3 0 • " c + [ !;~ (") .,_ • ~ ~~ 0 ,. , , , , , ' z r:~ ;;s ~ ~~ ~~i!! c>~~ 1'1 ~~bi'~::~ . tolf; '"'~ § > ~~ ! ~ = ~ ~ f ~ ~ ~ <:!"~ if f) .... .,- ... ,'13 g '13 "' b-.onn -. -. t) -. n -. ::'~~ :s~ ~ 0 ;, ~ ;;~] ~~§! ~~ ;a € ! !i~l ...... ~ '< "O :J ~~£ ~j~~ j• ;~;~~;;- ;;;;· . :- a · s• - •,. • • -~·· ~{ .. !~~E oa!~~ & a. ~ a ~ a 1111 "' "' "' .., ~ o " - - ~o~oc Q i~'8·~ -· ~~ - 2 - ~ .... ~-a~~'!"' ~ ~z.z;-r r . ~:l. "CC :1.. \11 - ...... , f •a-a.; .. ~ ... 1 ... ~ ~ 2~~~-s 0 .. 3 ~ ~ ~~~:~; ~S. ~ ~~{ -e~ ...... - c ~ ., H~ .. g l t:'~ .. ~;~~ ;;;~; ~ a .. =-1 ~ ~ "~ !11 =~=- ~~ =~ "' n .., ... - .. ~ 0 111 • n fli .. < ~ ~ ~[~la~~~ ~ ~ ~~s ~ -[2~·~'~ .. C· ()· ~~L a.- 2 ~g.~ ~ ~ ~ ! ,. ::1 "' ~8~ 5 lf2 !~~~[ aa2i~ ~~! ~~a~. .... a;~ tll .. " v. ~ ;; .... . tl) ~ -~ "' ~ .. !:1 ~&·~~~;~~ -;.~ ~ ~~ z~::. ~ '8~a~:; • - -I') ::) :J Ill .. ... ? lflo .. ... ~~~ Ill ~ [~~~~ [! ~ 'o r .. ~ ::: i~ ~ :J "tl t. .., .... ~ " ~ ,.~~~~~ ~~~!. ;; ~ ;.g ~~ ~ ! 1 !. c. ., ., 0 .. - ~ .. ~ ~ ~ "0 :r .. c .. n ~i t. o;-~;; ~ ~ ~ ~ • .. Ill ~ :; .. l • • ~- [ • ' ~ ~ "0 0 ._,a> !.- ..;; · 368 DAVID J . CHIVERS AN D C. M. HLADIK G UT MOIU' IIOLOC: Y A 0 DII•:T I N MAI\.1~1 A I.S 369 .------f ol ivor es------)o ~---- f olivo re s-- .-- - -frugiv or es--- - t r ugivores- - - ~----faunivo r es------~ - f au n i vo r es----~ APES i I fj PoJn t ro.~l uuS I I I Hylobates pileatus I o I I • I Hyloi;Jdtes p l l~ --> I I I I ' I • i x nemae us p I ' Py gathr I I TCSbfc:Opl th<>cu.~ nf'9JI•CIU'i I c I I I I I I . I ,C.lC' iJ -'iilniCd I .. CE RCOP ITHECINE e l Ha ca c a sglvanus I I I I . I c.• rcopJt.hccus ll!Cl l tcuq ccptw..•- I I I I • Cercopi t hec u s n eglect us I Pa ' I I I I I r I C'.. C:d t .. <:CJCtJlofT I:'i ' • Cercop i thecu s cephus I .. I I I I I . Opllhf>cUS t,.)JitpoHI I • Hacaca fasc i c u l aris I .. I I . I c l'r,·op! t:ht-'CV"> ,to•t h1ops I I • I• Cercoce bus a l b igena I I c ..c .. l!lle<;llntulus I' ' I' I . "' 0 Heliosc iurus r u fob rac hium I .. Pe Tod!Ct.IC'c.!S f)DllO I I ' Anomalu r us fras~ r i . Au d hJ l.Jnlqer p I• I I LoTls t. <~ rdtqr,.dus I Epi xe r u s eb i i I ;o Phdner · (urc,fct 0 Funisci urus an e r ythrus • ' ' l.Jqo iJ!lt•n• I 1 0 ' ' Fu n i SCJ urus pyyrhopus . I ""Ch c 1 'Ous lfJd )fls: .s 'I I Nan d i. ni. a bi not ata TROPICAL MA MMALS I "' 10 ' I Poi ana richacd soni I 0 ., dd'Jpu .~ t t /dd ~:tt~ lus 0 Han i.s gi g.mt ea I I 0 ' : ' I I Den-ltOI'H.I ttrO cJFUI tiC:h,ttdS<>nl TE MP ERATE MAMMAL S 0 I' Sciur u s vulgar i s i I I Fun lSC1u r us P•trrtnr>CJ<. ' Vulpes vulpes q ' : ' 0 J I ... J,ur p.Jlud!fl()SIJ"i 0 I ' Tursio ps t r unca tus I I • • n IS 919.tntt_•.l I I _Q I I Phocaena p hoca e na • moq.tJe ve-l&Jt 0 ' I I I' Hvs t el a e r minea TEMPERATE MAMMALS I ""' 0 I O l Vul pes vulp.•s ' o l , t(!'Jd t •tMitlt:"J I I 0 I .. DOMES TIC MAMMALS I I : Capra I Sco t.~tu<. vulq.it/'1 I 0 I ,.., tt>Joll (UVstoma ch • caecu m • colon weight of stomach+ caecum +colon volume of sma ll intestine weight of small intestine F1g. 20.. Coefficients. of gut d~fTe ren tiation_ fr~m volume in each taxonomic group of primates, in other temperate and t.ro ~Jcal ma_mmals, a nd 10 domest_1c mammals, md 1cating ~he ext~n t and overlap of the main morphological dietary categories. T he d_J s tor ~ Jo n of values for co_lobm_e mo nkeys and domestic rummants, resulting from the standard t reatment of stomachs as 19. F'ig. Coefficients of gut differentiat ion from weight in each taxonomic group of _primates, in_ othe: temperate a_nd sphen cnl,_1s corrected as outli ned m tabl_e 4 and ploUed as a small closed ci rcle to the left of the standardized va lue; in the tropical ma mmals. a nd in domest ic mammals. indicating the extent and overlap of the mam m o rpho l og u~.,_'l l d•etary categor1es case of pn mates 1t. leads to a closer relat10ns h1p w1t h other primates, but it disrupts t he sequential patte a mo d •. by vertical broken lines. mornmals. rn ng ome s~.J c 370 OAVID J . CHJ VE HS AND C. M. JJLAD IK (;UT \IOHI'IIOJ.()(;Y /\Nil I)J J·: T I \Ji\~ 1 \ Ji\J.S 37 1

While sud'ace a reas are taken as critical for urn (Fig. 16). Such features also affect the menting chambers and body s ize can be il lus different dietary groups are clear·ly separated pinpointi ng differences in digestive and a b weight of the organ. Similarly, vi lli increase trated by cubic models of animals of length L !Pig. 22!. The differences between the slopes sorptive functions between species, weights of the surface ar·ea of the mucosa of the small and volume L" (Pig. 24). The fermenting in the equations fo r fo livores with la rge colon each region provide a n indica t ion of the intestine by s imilar proportions, a lthough chambers a rc required to fi ll this vo lume with and fa univores are also significant (p < 0.05). amount of muscle, a nd thus of physical activ there is cons iderable interspecific variation nutrients each day; this will be achieved if Ln faunivores, where fermentation is mini ity in tha t region. In each mammalian group (Hl adik, 1967); at this level of analysis no the size of the fermenti ng chamber is propor· ma l, the vol umes of these par·ts of the gut ar·e such data as arc available provide a clear correction is thought necessary, but fu rther tional to the s ize of the animal. However, this r·cla ted most ly to a ctual body weight

V >00000 c m 3

100000 X soooo

soooo )()000 ~ !) 0 00 z 0 JOOOO _J z 0 10000 u 0 A X X _J A . 0 :1: """' u :::> . 10000 u :I: X w :::> • < ""' u u '"" w .,., A >000 < tA(. u 0 1000 )000 ~ I 0 :1: u >coo A • ,_0 < A :I: v'l "''" ,_0 • 0 ,,., ~· 0 v'l w •oo • • :1: 0 • :::> '"' w oA .... d _J 100 :I: ,"',. 0 :::> • > 100 _J 0 0 ""' > 100 • ... • • 0 ""' ,,. • 0 0 ,, 0 X 0 0 • " •• " " .. .Jl 10 " 0 0 6 0 • 'I l

"' TROPICAL I • ~ 0\l l" .f.HS 0 W LO ,..AMMALS N[ W '"' ()QL0 ,...ONIC [ V!. ' • 0 IEMP(IUTE ' (.(I(;:()PITiot[ (.ht: • MQN !'\('1'\ COLC~·8 N r

A• .., X ~ ') T )(: M""'..Io!Al!. ' . S 6 1 U10 10 " '",. "" "' 000<00"" """' 1000""' ""' """' """' eQ!ll': I.~NGTH 3 1000 1000 )())) '!.0:0 10000 10CID 1000 3 . BODY LENGTH L= 13 2J 5e 12e cm 1000

Fig. 22. The relationsh ip betwee n the volu me of potential fermenting c hambers and body s ize in faunivores, Fig. 21. Volumes of poten tial fermenting chambers plotted against body size

1·epresented by the equation: Returning to the cubic model of anima ls of va ry ing length L and volume L" (Fig. 241, metabolic rates (BMRl, however, the volumes Allowa nce must also be made for activi ty, log A = 0.76 log L" - 0.96 (r 0.93, p < relation hips between surface m·ea and ab to be fi lled are proportiona l to the three-quar wh ich as me ntioned above costs relatively o.oon sorption ca n be described. If flow across the ter power of body weight- L"·"'' in our model mom in terms of energy in a larger an imal, mucosa occurs at a constant rate, because of and the volu me of nutr ients absorbed in 1 day despite a n improved output. Thus the fl ow The scatter is less tha n tha t fo r volume

»:00 0 20000 xx 0 00000 X

IM A X LIJz >000 1- IJ) .., LIJ 1- •

z 1000 ... 0 ....J ....J .... < ,., • • ::E ~ .. (): IJ) . 100 0 ••• 0 0 " ""' ·. . 0 0 0 ~0 < ,.,""' 0 LIJ ... 0 a:: I} < o • 'il • w .. Q • u ·~ u.< a:: '"' A:0.00 1cm2 ::J .. IJ)

JO ,. L = 10cm .. • •' L :1cm

Fig. 24. Cubic models of body length' I, 10, nnd 100 cm, and theoret icul weights .001, I, and 1000 kg. The areas necessary to fi ll these models in u nit time hy cons tant. tlow {shown by openings in top) are .001 , I, und 1000 cmz. These are eq uivalent t.o the abJoOorptivc intestinal area. The act.ual volumes are .001, I, nnd 1000 I ~ • ' ~ Ill ET I\ ~lA:I-1\l J\1.<; 377 A c m 2 log A' - 0.86 (:!:0.151 log L" 1.46 (r between body s ize and the potential area for 0.95, p < O.OOll; a nd absor·pti on (Fig. 261 show that this ar·ea must 10000 be divided by L'·'"' in faunivores, by L""' in 4) in 14 fore-gut fe rmenting fo livores, frugivores, and by L"·"' in folivores, in order 10000 folivore to eliminate allometric factors and validate l.l9 (+0.171 log L" 2.97 ( r the comparison between species. The factor L', frugivore log A' 10000 0.96, p < 0.0011. used in earl ier· s tudies to compare gut surface 1 w 7000 a reas 1-flad ik, '671, was a good appr·oximation z , fa univore These regressions now have a better fit (high 00 overlap except for animals of very small body the approaches adopted, however, the first did w weight , because of the convergence of the not yield conclusive ratios of gut difTerentia (..) three Iincs. This latter feature suggests that tion, probably t hrough ignoring allometric if. 100 smaller· animals s how sim ilar structural ad factors, and the second, accounting for such 0:: 10 ::J aptations for absorption, irrespective of diet. factors, d id not yield a single morphological <11 ~ 0 The maximum a nd minimum values of the index directly compar·able with diet. So far we ,.;lopes of these r·egr·cssions have bee n com have been considering diet from the morphol lO pared in terms of 95'h confidence intervals. ogical viewpoint, a nd befor·e concluding the They difTcr s ignificantly between fo livores a nd search for a single morphological index, some >0 faunivorcs, but frugivores difTer from these featu res of diet and feeding behavior need two extremes at only the 85'k I imit. This lack fin;t to be stressed. 10 of high significance is not sUJ·prising, si nce the • frugivorc sample comprises s pecies with rath Dl ~;T IN RELATION TO GUT MORPHOLOGY •' er difTerent d iets based on fruit. Both frugi T he diets of most species, especially pri vores and fo livorcs fa ll withi n the l i m iL~ de mates, are composed of varying combina t ions rived for metabolic plus energetic rcquircmcnLo; of each major category of food-animal mat (slopes between 0.75 and l.OOl. Faunivores, on ter, fru it, a nd leaves. This is well known from the other hand, with a slope of 0.66 (less than fi eld studies and pa rtly explains the scatter of 0.50 for a small set of highly specialized fau morphological plots in the preceding analysis, nivoresl, in their lar·ger for·ms fa ll below the mostly a mong frugivores. While recognizing ) ' s (> 7 8 ~10 >o )0 t O S,O l

ed to di!Tet·ent kinds of analys is, according to tr iangle the details of feeding bouts in terms of time these mnges may overlap, even among sym u w sooo (Chivers, '74; Struhsaker, '78; MacKinnon and patric species, it may not be at the same time

+ lOO While the amounts of leaves and other· veg though these t hree primates eat mostly fruit, UJz etative plant parts ingested can be deduced the overlap represents but a small pa rt of I- with sufficient accuracy from feeding t imes, their dietary ranges; for the means (x = - 5, lll 100 fruits may be underestimated as much as + 15, +26 respectively), accounting fo r diffe r UJ I- fivefo ld, and insects may be overesti mated as ences in t he supplement of plant a nd a nimal z so much as 15 times, compa red with the actual matter, provide good diagnostic dietary in LO _J amount by weight Kinnon and MacKinnon, '78). The most e!Tec species. No mammal mixes large quantities of lll tive method for representing a system con animal matter and leaves without includ ing taining three variables-a nimal matter, fruit, fruit in its diet. Since, as has been shown ] (. Cj b 7 8 9 10 20 )0 t.IJ ')() 1000 20Cil J(ll) SOl) 10000 lOQXI 3 and leaves-is a tri-rectangu lar projection (or previously, faunivory and folivory represent BODY LENGTH three-dimensional gra ph). cont t·ast ing, and incompatible, adaptations, .10 00 This approach involves plotting values for the qua ntity of fruit in such a mixed diet L 13" 27" 58" 126 c m the three major categories of food in the diet should always be cons iderable. From the dem within a three-dimensiona l system of converg onstration by Hladik et al. ('72) tha t fru it is ing axes (Fig. 27, r ight upper). Since the three a n adequate source of carbohydrate fo r the Fig. 26. 'l'he relationship between the potential area for absorption (surface area of small intestine and half the vm·iables are not independent (their sum is energetic requir·ements of most pr·imates but combined areas of stomach, caecum, and colon) and body size (from body length, cm ) in faunivores, frugivores and folivores a lways 100".-f ), the projection of any combined inadequate in protein, Kay ('73) argues that ( two types combined ), in the form of regressions derived from individual data. The correct ing faclors (L'~ ) , accounting for dietary value will fall within the t r iangle those primates securing this protein from in the allometric relations in each group, a re markedly different, because of tile variations in slope. T he st-ippled areas demarcate the 95t..l confidence li mits for the slopes: the three dietary grou ps are quite distinct at the 851'}'r Jimi t. AFL, wh et·e point A represents a diet of l OW sects are necessarily much smaller than those a nimal matter, poi nt F a d iet of lOW fruit, obtaining it from leaves. a nd poi nt L a diet wholly of leaves. In this Thus, as exempt ified by primates, there are 380 OAVID J . CIIIVERS AND C. M. III.AOIK GUT \ IO I! I'IIOLOCiY i\'\IJ DI ET 1\J \IA~1~1 i\I.S 381

PRIMATE DIETS 100% FRUGIVORE +M E AN S AND RANGES ' x - ( % Leaves } - ( % Animals } /150 jt,!·::~. y = 1.732 (%Fruits} // ( .. ··.o,. •. At~t les gftoffro y i

M BCIIC IJ ' sin t clf . ~· , // / ... ,4:.:~:. :~f. ,.. l ·~ ~~\

Cltbus cBpuc inu ~/ ' ,/ t~~~<#?~ ~\ Pa n tro g lodytes

Sagumus geoffroy•/ ...._ .;• • IJ ...,.. ·~;·, . ::• :·:• •· • •:. . ;: ~,) ' ,J.• •'•(.::_. ·:::·=·:· I ', tf r~ -----· ,\ f..~;'! /, ', d:~l ',_ ,~:;r/! ,/ ,' j

50 , ~"'"'';~,': ' ' ' / + .' L oris tardtgradus ~~ cunrculus ,' . EQn gor rlla I ' ,' ~~~~~~~~~~------_ja Dendrohy~~ - ' ' !00% Ovrs and E._quus I ' ,• I ,' FOLlVORE A,'' ... ~ '

---;~ , - , .----. ... 1 -lOO -50 0 + 50 +100 Frg. 28. Mean dietary charactcristiC!l of the 34 species rncludcd in thrs study !tables 5- 81 for which quantitat ive data on d1el are available. Locat.ions withal t.hc tnnnglc rCJ>rcscnL dict.J3 us shown in Ftb'llr e 27.

Fig. 27. Annual means and ranges of the diet of nmc pnmutc species from Panama, Gabon, and S ri Lanka (data from lllndik and llladi k, '69. '72: llladrk, '7:31 rc1>rcscnted within a tr·ranglc Isec text for explanation of i ts derivation from tri rcct.J r ngu~;lr proJect ion. an~ i t~. app.lrcations). The cornJ>Osition of the mcotn annual d ict, in terms of proportions of animal cator·s of diet, varying fr·om 100 lpure fau take the I ine of' the regression for frugivores ~natter. f~urt, und leaves, rs pmpoanted by an a rrow; most data, collectL-d over 24-tlOur periods at. all t.imes of year. are nivoresl to + 100 (pu re fol ivoresL The final as the zero, rather t han a line midway be mcluded rn the ~ha dt-d area V,, 0 copi ng with the two extremes of diet C Fig. 29L V, - V, Faunivores minimum y-value, the lowest proportion of fruit taken by a frugivore. It is likely to be Most pr-imates fall within these lim il<;, but the V,- V 0.4 5 concentration of frugivorous species, repr·e if V <... Vr. 0 Frugivores quite high, si nce the data are clearly distrib v, va uted a long a ere centic path from A to L via sented by the third regression li ne, closer to 4.0 300 the upper line, reflects their greater s imilarity F'olivores the vicinity ofF, with the greatest range of y va lues around the zero x-values. This repre to fol ivores than to fa univores. In order to where V, V., V, a nd V, represent the potential We have arrived independently at conclu.·ions sents, at least for primates, the evolutionar·y der·ive a morphological index fo r comparison volumes for· fe rmentation in the subject, and similar to those of Kay ('73), who shows that path from the ancestra l insectivorous fo rms with the dietary one, we need a scale of in fau n ivore, fr·ugivore, and fo livore of the primate species each specialize on either· ani ( Ripley, '79) through three ecolog ical grades negative a nd positive values to refl ect their same s ize, r·espectively; these latter are cal ma l matter·, or fruit or leaves, although many (Hiadik, '78bl. d irection and degree of adaptation to either culated from the r·egression equations relating specialize primarily on one catcgor·y ( > 45'k The geometrica l arrangement of t he data, fa univory or fol ivory respectively. To account to Figure 22, where body size is derived from dependence) a nd secondarily on another ( > therefore, y ield the x-values as the best indi- for the asymmetry in the relative positions of the length L, the distance between bregma the regression I ines, it is more appropriate to and isch ial callosity. Since body weight W is 382 OAVID J . CI II VEI\S AND C.M. ll i.AOIK GUT MOitPIIOJ.OGY A ND DI ET I 1 M AM~l AJ.S 383 the more widely used measure of body s ize, is based on antilogarithms; a lthough appear diets including mo1·e than 9W. of leaves, and for faunivores, the regre~s io n equa tions were recalculated ing very complex, on the s mall programmable the lower one more than 90% of anima l mat log A' = 0.66 (:!:: 0.06) log W - 0.49; L" . calculator, now in wide use, it is almost as ter. accord ing to the approximation, W lnt10n. the d ietary indices (see below). also very s imilar to the dietary indices. 1.·1 The same method is a pp! ied to the potential w 0.041 x ll.,lr 0.98l or W -. The approx•matton W In these opera tions we are locating each As s hown in Figure 29, the asymmetry 24.4 absorbing area (i ncluding half the area of species in relation to all others, according to creates a discrepancy in the s ize of units above 1. ' ~ ~ J)rt'fcrrcd. smce it y1elds a better fit. for m~t wild arhor~:ll stomach and large intestine together with the 30 the gross dietary classification derived previ and below the zero line, s ince the extremes pnmut(""' area of small intestine) in all species. The ously. Thus, it is not surprising, with the large represented by the outer lines have values of regressions of these areas (A') are those of samples, that there is good correspondence 1 a nd + L. To attain a homogeneous dis tri ' On the liP 25 calculator the program is: g ).. · 0 GTO 07 I CHS Figure 26. The asymmetry of the regression h"TO I ' ~ y ~ ABS l fx <. y GTO 36 x ie y !>"TO 0 x > y I x ') between morphological and dietary indices. bution of the units, and thus the desired index " 10' I!CI. 3 X ;> y RCL 0 X RCt 0 g 10' l RCL 2 X RCI. 0 for frugivores in relation to the other two is The problem of scatter is not easy to resolve, of gut specializat ion, the d is tances 0 a rc I ' GTO 44 I X "y g 10' I!CL 3 X "y RCL I ' l STO even more marked; thus the conditional for t \: - y {;1'0 00. After st.Qri ng the values 1, 10, and 100 in regi'\ters because of the difficulties in measuring such tr.. nsformed mathematically into the values I , 2 ..tnd :J respettively, any value of 0 mtroduccd in transformed mula is used to locate each species, accordi ng a malleable morphological system, and of in 10t.o Tl~ hy J)ressmg the RIS key. 'I'R, 11 ,. The cond itional fo rmula used !Fig. 29l 11 1 to body size, at distance D above or below this dividual variation within species. zero line: The major advance resulting from this ap proach is that, having resolved the complex "fA' A' 0 A' - A'r allometric problems, mammalian species fol o> 1 [1-(o-1ll t > r. =+ A' , - A'r lowing different adaptive strategies may be TR (ol" 100-10 A'- A' compared qua nt itatively. It is possible to de if A'< A'r. 0 = - A' r _ A' r a limit the "ecophysiological tendency" for each species, especially for primates, whose body O.;;o-:;1 [o-(o-llJ o TR(ol" o000- 10 l-1000 -1)(o-1 l where A' , A'a• A'r. and A' , represent the sizes fall in the central part of the range potential absorbing areas in the subject, and investigated. For example, among the so in faunivore, frugivore, and folivore of t he called "omnivorous" primates, which feed on O>o;,. -1 U- case, the regress ion equations were recalcu the significant differences in diet which have lated with references to body weight, rather been demonst rated recently follow those be than length: tween the various indices: o<-1 (1-( lol-lll " 10 TR" 10 - " Gut specialization index Dietary index (Fig. 27)

by area, A' by volume, V X Miopithecus lalapoin - 85 - 40 estimate, Fig. 28 CeropithtXus cephus - 27 - 2 - 10 estimate, Fig. 28 • Papio sphinx + 9 0 Cebus capucinus + 11 - 5 Macaca sinica + 16 + 22 + 15 Alorwtta palliata + 40 + 3 1 + 40 Macaca syluana + 45 + 85 Presbytis melalophos + 82 foli vore

Fig. 29. Method for comparing the potential volume of fermentation in the gastro-intestinaltracts of various primates with contrasting diets. The log of volume (of stomach, caecum, and colon) is plotted against the log of body weight (taking ~ as a good approximation for body weight), so as to eliminate allometric parameters. The resulting regressions from a large sample of faunivores and folivores (Fig. 22) are used again here, and considered as showing the st ructural limits for 29 coping w ith diets containing 90% of animal matter and 9~ of leaves, respectively. Most primates fall within these limits, l L______(~ 1rl~~~------t,1_11_~~~------~ JoeW and the d istanceD from the regression line fo r frugivores can be regarded as an indicator of the morphological tendency 3 4 s towards faunivory or folivory. The conditional formula presented allows a transformation of 0 into the index TR, 01 which, in most cases, is the same number as the dietary index, x, as defined from the tri- rectangular projection (Fig. 27). 384 DAVID J . CI·IIVERS AND C. M. I·ILADIK GUT MOHPIIOLOGY A D DI ET IN MAMMALS 385

T he simi larities between indices for· each spe main lines of research should be followed. Anatomy, Cambridge, for t heir reproduction Harrison, R.J., F.R. J ohnson, and B. A. Young ( L9 70) Th e cies are pleas ing, cons idering that mor·phol There needs to be mor·e extens ive ana lysis and of the figures. Finally, we tha nk Donald Ste oesophagus and sl.omach of dol phins. Tursiops, De/ph in ogical indices refer to single individuals, and us, S tenella. J. Zool., London, 160: 377-390. quantification of the biochemica l composition ven and R.D. Mart in in particular a mong Hi ll, W.C.O. (1958) Pharynx, oesophagus , stomach, small the dieta ry indi ces a r·e derived separately of foods, in relation to diet, a nd of the fi ne those who have given helpful advice during and large intestine: Form and position. Primatologia, from da ta of var iable quality. The success of s tructure and cellular· populations of the gas the course of this work; and Donald Steven, 3:139- 207. this a pproach depends on a) obtaining ade tro-intestina l mucosa, in relation to morphol J ohn Payne, Pier re Char-les-Domi n ique, G. Hladik , C.M. (1967) Surface relative du tractus digestif de quate gut samples that a re truly representa ogy. At the same time, t he quantity a nd com quelques primates, morphologic des villositks intestin Cansela da Fonseca , a nd Gerard Dubost fo r aJes et correlations avec le regime alimentaire. M am· tive of the population from which dietary data parability of the kinds of morphological and their constr·uctive comments on the manu malia, 31: 120- 147. are obtai ned, bl obtaining adequate d ieta ry dietary data discussed herein must be im script. Hladik, C.M. (1973) Alimentat io n et activitk d'un groupe data, in terms of weight of each food ingested, proved, if we a re to understand the real sig LITERATURE CITED de chimpanzes reintroduit. en forCt. gabonaise. Terre et Vie, 2 7·3. 43- 4 13. and c) defi ning in which species morphological nificance of "sacs" and "tubes." Bolk, L., E. Goppert, E. Kall ius, and W. Lubosch (1939) Hladik, C.M. (1 975) Ecology, diet and social patterning in ada ptations may confer greater di etary flex i Handbuch der vergleichenden Anat.omie der Wirbeltiere. Old and New World primates. In: Socio-ecology and ACKNOWLEDGMENTS bi lity, e.g., variations across the geogra phical Band Ill. Darmsystem. Urban and Schwarzenberg , Berlin Psychology of Primates . R.H. 1\ottle, ed. Mouton, The ra nge a nd feeding behavior in captivity. We thank the Smithsonian Institution, es and Vienna. Hague, pp. 3- 36 . Bell, G.H., J.N. Davidson, and H. Scarborough ( 1963) Text Hladik, C. M. ( 1977a) Chimpanzees of Gabon and chimpa n Reference has been made to the convergence pecially Dr. Martin Moyn ihan, who obtained book of Physiology and Biochemistry. Fifth edition. Liv zees of Gombe. In: Primate Ecology. Studies of Feeding of the regression lines for potential absorbing funding for C.M.H. at the Smithsonian Trop ingstone, Edinburgh. and Ranging Behaviour of Lemurs, Monkeys and Apes. area, A' (Fig. 26), which renders this model ical Research Institute from 1966 to 1968. Carleton. M.D. (1 9731 A survey of gross stomach morphol T.H. Clutton-Brock , ed. Academic Press, London, pp. inapplicable to species smal le r· than 27 cm C.M .H. was also funded in 1969- 1970 by the ogy. In: New World Cricetinae (Rodentia, Muroidea), 595- 601. body length. Jn such cases the model based on Smithsonian Biological Program in Ceylon, with comments on functional interpretations. Mise. PubI. Hladik, C.M. ( L977bl A comparative study of feeding strat Mu s . Zoo!., University of Michigan, No. 146, pp. 1- 43. egies of two sympatric species of leaf monkeys: Presbytis potentia l fermenting vol umes, V (Figs. 22, 29) administered by Drs. John Eisenberg and Suz Char les-Dominique, P., and C.M. Hladik (1971) Le lepile senex and Presbytis entellus. Ln: Feeding and Ranging is quite sati sfactory fo r small species. Figures a nne Ripley. Since then he has been employed mur du sud de Madagascar. Terre et Vie, 25:3- 66. Behaviour of Lemurs, Monkeys and Apes. T.H. Clutton for fol ivores with la rge stomachs, however, a t the Museum of Natural History, Brunoy, Charles-Dominique, P. ( 19781 Ecologie et vie sociale de Brock, ed. Academic Press, London, pp. 481-50 I. are not incl uded in Figur·e 29. To derive in by the Centre National de la Recherche Scien Nandinia binotata (Carnivores. Viverrides): Comparison Hladik, C.M. (1978a) Adapt ive st rategies of primates in avec: les prosi miens sympatriqu es du Gabon. Terre et Vie, relation t.o leaf-eating. In: Ecology of Arboreal Folivores. di ces of gut s pecializat ion (GSl l fo r such forms, tifique (F rance). Since 1970 D.J.C. has been 32:471- 528. G.G. Montgomery ed. Srnithsonian Institution Press, either the A' model should be used, or the V employed by the Un iversity of Cambridge; he Chivers, D.J. (1974) T he Siamang in Malaya. Primatol. Washington. pp. 373- 395. model r·evi eel us ing t he regression line fo r acknowledges the facil ities generously provid 4: 1-335. Hladik, C.M. (1978b) Diet and ecology of prosimians. In: Ch ivers, D.J., and J . Herbert (1978) Recent Advances in The Study of Prosimian Behaviour . G.A. Doyle and R.D. fo l ivores with la r·ge stomachs (Fig. 22). ed for his studies, and grants from the De Primatology. Vol. 1. Behaviour. Academic Press, London. Martin, eds. Academic Press, New York, pp. 307- 357. The specialized seed-eaters have not been partment of Anatomy and University Travell Clutton-Brock, T.H. (1977) Primate Ecology. Studies of Hladik, C. M., and P. Charles-Dominique ( 1974) The behav included in the e models; if primates eat seeds ing Expenses Fund for 2-month visits to Feeding and Ranging Behaviour in Lemurs, M onkeys iour and ecology of the sportive lemur (Lepilemur mus and Apes. Academic Press, London. telinus) in re lati on to its dietary peculiarities. ln: Pros i lhey usually do so in small quantit ies and Ma lays ia in 1972, 1974, and 1976, where local Comline, H.S., I.A . Sil ver, and D. H. Steven (1968) Physio when they are unripe. Certain frugivorous travel was a ided by a Royal Society Govern mian Biology. R.D. Martin, G.A. Doyle, and A.C. Walker, logical anawmy of the ruminant stomach. In: Handbook eds. Duckworth, London, pp. 23-37. squirrels of Gabon also cons ume some insects ment Grant-in-Aid. of Physiology. Sect. 6 (alimentary canal). Vol. 5. Am. Hladik, C.M., and D.J. Chivers (1978) Concluding discus (Emmons, '75) and Epixerus ebii, for example C. M.H. acknowledges gratefu lly the coop Physiol. Soc., Washington, pp. 2647- 267 1. sion: Ecological factors and specific behavioural patterns (see Table 8), has a GSI from V of 16. Gut eration of the Panamanian a uthorities , t he Crowcroft., P. (1952) Reflection in the common shrew. Na determining primate diet. In: Recent Advances in Pri ture, 170:621. mat.ology. Vol. 1, D.J. Chivers and J. Hcrbert, eds. Aca s pecia lization indices of other rain-forest Wildlife Department of Sri Lanka, the Ca Cuvier, G. (1805) Lecons d'Anatomie Comparee. Crochard, demic Press, London, pp. 433- 444. squirrels have been ca lculated from data col bonese a uthorities involved in the C.N.R.S. Paris. Hladik, A., and C.M. Hladik ( 1969) RapportS t rophiques lected recently in Malaysia (Payne, '79). The Station of Ipassa/Makokou, the Forest Depart Ellenberger, W., and H. Baum (192ll Handbuch der ver entre vegetation et primates dans la fo rCl de Barro ment of Morocco, and the Service des Eaux et gleichenden Anatomie der Haustiere. Hirsc hwald, Ber Colorado (Panama). Terre et Vie, 26:25-111. s mall Sundasciums lenuis, of length 13 cm, lin. Forets de Madagascar; and D.J.C. the Head Hladik, C.M., and A. Hlad ik (1972) Disponibilitk alimen· which eats mostly bark, sap, and seeds, a nd Em mons, L. (1975) Behaviour and Ecology of African Rain taires et domaines vitaux des primates a Ceylan. Terre some insects, has an index of t 100. The fruit Office of t he Game Department (now the De Fo rest Squirrels. Ph.D. dissertation. Cornell Un iversity, et Vie, 26:149- 215. eating species Callosciurus notatus a nd C. pa rtment of Wildlife and Nat ional Parks), the lthaca, New York . Hladik, C.M., A. Hlad ik, J. Bousset, P. Va ldebouze, G. Fooden, J . (1964) Swmach contents and gastro-intestinal Viroben, and J . Delort-Laval (197ll Le regime alimen preuosti have indices of + 97 a nd - 22 res pec State Game Wa rdens of Pahang and Perak proportions in wild shot Guianan monkeys. Am. J . Phys. tively, wi t h t he la tter eating cons iderably a nd their staff, and the Institute for Medical taire des primates de l'ile de Barro Colorado (Pana ma): Ant h rop., n .s., 22:227- 23 1. Resultals des ana lyses quantilatives. F'olia Primatol., more soft fruit: in contr·ast, the seed-eating Research in Kuala Lumpur, Malaysia. In Gautier-Hion, A. (1978) Food niches and coexistence in 16:85- 122. Ratufa bicolor has an index as low as - 93. France guts of primates were obtained from sympalric primates in Gabon. In : Recent Advances in lwamoto, T. (1974) A bioeconomic study on a provisioned Seeds r ich in protein and fat seem to need the Museum d'H istoire Naturelle in Paris, and •of Primatology. Vol. 1. Behaviour. D.J . Chivers and J . t roop of J apanese monkeys ( Macaca {uscata) a t Koshima Herbert, eds. Academic Press, London , pp. 269- 286. Islet, Miyazaki. Primates, 15:24 L- 262. processing more like animal matter than the in England fr·om Miss Ma ry Brancker, veter Genest-Villard, H. (1968) L'estomac de Lophuromys sika lwamoto, T. (1978) Food availability as a limit ing factor on vegetative parts of plants. An unus ua l pri inary s urgeon to Twycross Zoo, and from the pusi Evolution, consumption, a nd assim ilation of seeds in of British mammals. mountain gorilla group in the Thhibinda-Kahuzi region 30.·757- 774. (Zaire). In: Primate Ecology: Studies of Feeding a nd gested by mammals. We are also indebted to those who assisted Ranging Behaviour in Lemurs, Monkeys and Apes. T.H. Kay, R. F. (1973) Mastication, Molar Too th Structure and Ln the search for a fu ll physiological expla us in our unsavory la bors, especial ly our Clutton-Brock, ed. Academic Press, London , pp. 449- 4 79. Diet in Primates. Ph.D. dissertation, Yale University, na tion of the relationships between morphol wi ves, Sarah Chivers and Annette Hl adik , Grasse, P.P. (1955) 'I'raitk de zoologie: Anatomie, systkma New Haven. ogy and diet, that we have quantified , two and to the Vi sua l Aids Unit, Department of tique, biologic. Mammiteres, fasc. 2:1646- 1653. Masson, Kay, R.N.B., and E. Pfeffer (1969) Movements of water and Paris. electrolytes into and from the intestine of the sheep. In: Adresse de C.M. Hladik en 2013 :

Claude Marcel HLADIK Directeur de recherche émérite Eco-Anthropologie et Ethnobiologie Muséum National d’Histoire Naturelle 4 avenue du Petit Château 91800 Brunoy (France) [email protected]