THE JOURNAL OF EXPERIMENTAL ZOOLOGY SUPPLEMENT 3~2-9(1989)

Anatomy of the Avian Cecum

JOHN McLELLAND Department of Preclinical Veterinary Sciences, University of Edinburgh, Edinburgh, Scotland

ABSTRACT

The gross anatomy of the avian ceca is reviewed. In most birds, right and left ceca arise laterally or ventrolaterally at the junction of the small and large intestines. In a few species, the ceca open into the rectum ventrally or dorsally. In many herons and bitterns, only one cecum is present, and in the secretary bird there are two pairs of ceca. Ceca are absent in woodpeckers, hummingbirds, swifts, kingfishers, pigeons, mousebirds, cuckoos, and parrots. Ceca may be classified according to length into long, moderately or poorly developed, and vestigial types. In most birds, the ceca are simple tubular structures with minor variations in shape. However, in a few species, including the ostrich, rheas, kiwis, some tinamous, the red-throated loon, screamers, the satyr tragopan, the great bustard, and the pin-tailed sandgrouse, the ceca are sacculated or have diverticula. There is usually no correlation between the development of the ceca and systematic position. Except in grouse (Tetraonidae), in which the long ceca are related to the fibre content of the diet, the correlation between cecal development and diet is extremely limited. There is no relationship between the size of the ceca and the length and width of the rectum.

Although a number of accounts of the anatomy of the avian ceca appeared before the middle of the last century (Gesner, 1585; Perrault, 1758; de Nobleville and Salerne, 1756; Pallas, 1767; Buffon, 1770; Home, 1814; Meckel, 1821-31; Tiedemann and Gmelin, 1827; Cuvier, 1835; L'Herminier, 1837; Siebold and Stannius, 18481, most are regrettably incomplete and consequently of relatively limited value. Fortunately in more recent times there have been some important surveys of the cecal morphology of birds, undoubtedly the most comprehensive being by Gadow (1891), Mitchell (18961, Beddard (1898), Maumus ('02a,b), Magnan ('111, Groebbels ('321, Jacobshagen ('371, Naik ('621, and Naik and Dominic ('62, '63, '68, ,691, and these studies form the basis of the present review. Inevitably, however, even these accounts have their limitations. For example, of the 91 species examined by Magnan ('111, 62 were represented by only a single bird. Equally valuable to this review have been the short papers by Garrod (18761,Beddard (1886, lS90), Beddard and Mitchell (1894), and Mitchell (1895) concerning the ceca of individual species. This account deals only with gross anatomy. Obviously any definitive consideration of organ structure must take into account the available histological data, and these will be dealt with elsewhere in this issue.
0 1989 ALAN R. LISS, INC.

ORIGINS OF CECA
In most avian species, right and left ceca arise at the junction of the small and large intestines. Usually the origin is on the lateral (Fig. 1) or ventrolateral aspect of the gut. However, in a few species, e.g., the pygmy cormorant (Phalacrocorax niger),the great cormorant (Phalacrocorm carbo), the Egyptian vulture (Neophron percnopterus) (Fig. 2a), and the jackass penguin (Sphenzscus demersus), the openings are strongly ventral (Jacobshagen, '37; Naik, '62). In contrast, the single cecum in the heron family, Ardeidae, opens into the intestine dorsally (Fig. 2b) (Naik, '62). The right and left ceca in the ostrich (Struthio camelus) (Fig. li) and in sandgrouse (Pterocles) have a single blended orifice, which opens into the ventral part of the intestine (Jacobshagen, '37). Whereas right and left ceca usually lie at the same level of the gut, in a few birds, including doves and some passerines, the openings are situated at slightly different levels. Sometimes the right opening is more cranial, as in the dyal (Copsychus saularis) (Fig. 2c); alternatively, it is the left opening in the golden oriole (Oriolus oriolus) that is the more cranial (Fig. 2d). From their origin, the ceca are generally directed cranially and are attached t o the terminal part of the ileum by a fold of peritoneum, the

ANATOMY OF AVIAN CECUM

1
a
b
C

h
Fig. 1. Ceca of a) purple heron (Ardeapurpurea),b) sparrow-hawk (Accipiter nisus), c ) marabou (Leptoptilos crumeniferus), d) a rail (Rallidae), e) helmet guineafowl (Numida neleagris), f ) barn owl (Tyto a h ) , g) northern

i
screamer (Chauna chauaria), h) great bustard (Otis tarda), i) ostrich (Struthio camelus). (From Maumus, '02a, reproduced by permission of Academic Press, London and New York.)

J. McLELLAND

h
Fig. 2. Ceca of a) Egyptian vulture (Neophron percmpterus), b) black-crowned night-heron (Nycticorm nycticorm), c) dyal (Copsychus saularis), d) golden oriole (Oriolus orzolus), e) common coucal (Centropus sinensis),f) cotton pygmy goose (Nettupus coromandelianus), g) white-breasted water-hen

i
(Arnaurornis phoenicurus), h) Madagascar sand grouse (Pterocles personatus), i) pygmy cormorant (Phalucrocorax niger). (a-g and i from Naik '62, reproduced by permission of Banaras Hindu University; h from Maumus '02a, reproduced by permission of Academic Press, London and New York.)

ANATOMY OF AVIAN CECUM

ileocecal ligament. However, when the ceca are exceptionally well-developed, as, for example, in galliform and anseriform species, a large part of each cecum may be bent over to face caudally.

NUMBER OF CECA Typically, most birds possess one pair of ceca. However, in much of the older literature there is considerable debate on whether a single cecum is a characteristic feature of some species. Since right and left ceca may be very unequal in length and since one cecum is frequently very rudimentary, Maumus ('02a) concluded that many authors observed only one cecum when in fact two were CECAL LENGTH present. Intraspecific variations in the relative Many measurements of cecal length in a wide size of the right and left ceca have also led to variety of species are available in the literature, confusion in the literature (e.g., see the accounts see especially the accounts of Beddard (18981, by Beddard, 1898, and Wetmore, '20, of the ceca in Magnan ('ll),Groebbels ('32)' and Naik ('62). darters, Anhinga). With some exceptions (Corti, Mitchell ('01) also provided valuable information '231, a single unpaired cecum occurs regularly in on length, without giving precise data. Inevitamany herons and bitterns (Ardeidae), including bly, however, there are large gaps in our knowlthe Indian pond-heron (Ardeola grayii), the catedge, which often preclude evaluation of cecum tle egret (Bubulous ibis), the western reef heron length as a taxonomic characteristic. Indeed, re(Egretta gularis), the black-crowned night-heron (Nycticorax nyctzcorcwc) (Fig. 2b), and the purple lating the known data on cecal length to body length heron (Ardea purpurea) (Fig. la). More than one pair of ceca has been reported b o 'd y weight) (1 = 3 % only in the secretary bird (Sagittarius serpentarius) (Maumus '02a). In this falconiform, two pairs of ceca arise from the rectum, a small caudal (Magnan, '11) emphasizes that there are in fact pair originating 9 cm from the cloaca and a larger great variations both within and between groups. Collating the information it is possible, with some cranial pair originating 1.25 m from the cloaca. reservations, to place ceca in one of three categories depending on whether they are long, moderTOTAL ABSENCE OF CECA As was mentioned above, a major problem in ately or poorly developed, or vestigial. Groups of analyzing the literature is to ascertain whether birds with ceca in each of these categories are the observations on the lack of ceca within a par- listed below. It must be emphasized that, since ticular species or group are accurate or whether some of the information is imprecise, placement of in fact the ceca are so small and hidden by fat and certain groups was subjective. mesentery that they are overlooked. FurtherLong ceca (Fig. l h , j ) more, several authors have made widely sweeping statements about the absence of ceca within Struthioniformes; Rheiformes; Apterygiformes; orders after investigating only a few species. Tinamiformes; Anseriformes (Anatidae); FalHowever, the following data on the consistent coniformes (Sagittariidae); Galliformes (Tetralack of two ceca appear to be generally accepted onidae, Phasianidae, Numididae, Melegrididae); and have been collated from Coues (18901, Gadow Gruiformes (Heliornithidae, Rallidae , Gruidae, (1891), Newton and Gadow (1896), Beddard Turnicidae,, Otitidae, Cariamidae, Rhynocheti(1898), Mitchell ( ' O l j , Maumus ('Oaa), Pycraft dae); Cuculkformes (Cuculidae); Charadriiformes ('lo), Groebbels ('321, Jacobshagen ('371, Naik (Glareolidae, Chionididae, Thinocoridae, Charad('62), and Markus ( ' 6 4 ) .Both ceca are missing in riidae, Stercorariidae); Columbiformes (PteroStrigiformes; Caprimulgiformes; species from at least seven orders. These are the clididae); Piciformes (toucans, barbets, and most woodpeck- Trogoniformes; Coraciiformes (Coraciidae, Meroers), Apodiformes (hummingbirds and swifts), pidae, Todidaej.

Corcaciiformes (Kingfishers, motmots, hornbills, and the hoopoe, Upupa epops), Columbiformes (many pigeons), Coliiformes (mousebirds), Cuculiformes (turacos, go-away birds, and many cuckoos), and Psittaciformes (lory, lorikeets, parrots, parrotlets). According to Abraham ('Ol), the ceca do not develop in the embryo of the budgerigar (Melopszttacus undulatus). Among the groups listed above, Markus ('64) singled out the Columbidae as being unusual among avian families with regard to wide variation in the presence or absence of ceca.

J. McLELLAND

Moderatelg or poorlg developed ceca (Fig. l c , d ) Casuariiformes; Sphenisciformes; Gaviiformes; Podicipediformes; Pelecaniformes (Phalacrocoracidae, Pelecanidae); Cioniiformes (Ardeidae, Phoenicopteridae, Ciconiidae, Threskiornithidae); Anseriformes (Anhimidae, Anatidae); Falconiformes (Accipitridae); Galliformes (Opisthocomidae); Gruiformes (Gruidae, Rallidae, Aramidae, Europygidae); Charadriiformes (Charadriidae, Alcidae, Scolopacidae); Columbiformes (Columbidae); Passeriformes (Corvidae, Sturnidae, Dicruridae). Vestigial ceca (Fig. l b ) Sphenisciformes; Procellariiformes; Pelecaniformes (Fregatidae, Phaethontidae, Sulidae); Ciconiiformes (Ciconiidae, Scopidae); Anseriformes (Anatidae); Falconiformes (Sagittariidae, Accipitridae); Charadriiformes (Alcidae, Scolopacidae, Paridae, Laridae); Columbiformes (Columbidae); Cuculiformes (Cuculidae, Musophagidae); Passeriformes. Among this grouping, various of the sphenisciforms, pelecaniforms, ciconiiforms, anseriforms, falconiforms, gruiforms, charadriiforms, columbiforms, and passeriforms may be placed in more than one category. Contrary, therefore, to the view of some workers, e.g., Beddard (1898) and Naik and Dominic ('631, relative development of the ceca is often variable within major taxonomic groups. Hence, this feature is of no use in avian systematics.

b. Long ceca with a constricted proximal portion, e.g., in most galliform species (Fig. le). c. Long ceca with a swollen distal portion, e.g., in woodcocks ( S c o l o p ~ ) Todidae, , and many strigiforms (Fig. l f ) and the cranial ceca of the secretary bird (Sagittarius serpentarius). d. Long ceca that are broad proximally and taper distally, e.g., in the white-breasted waterhen (Arnaurornis phoenicurus) (Fig. 2g). e. Long ceca that are broad proximally and taper distally towards a bud-like enlargement, e.g., as in the Madagascar sand grouse (Pterocles personatus) (Fig. 2h). f. Short, cylindrical, conical or oval ceca, e.g., in the pygmy cormorant (Phalacrocorax niger) (Fig. 2i). g. Short ceca with a distal bud-like narrow portion, e.g., in the marabou (Leptoptilos crurneniferus) (Fig. lc).

Among these, the ceca belonging to group b have received by far the greatest attention. Most have three zones, including a short, narrow, proximal zone or base; a long, relatively wide, middle zone or body; and a short, distal zone or apex (Pilz, '37; Fenna and Boag, '74b; McLelland, '79). For the spruce grouse (Cunachites canadensis), Fenna and Boag ('74b) found that the base was about 7.0 cm in length and 0.4 cm in diameter, and the body was about 25.0 cm in length and 0.8-1.0 cm in diameter. Along the internal surface, some species have six to eight parallel, submucosal folds. In the spruce grouse, these extend almost the entire length of the organ (Schumacher, '25; Fenna Excluding species in which one cecum is so and Boag, '74b). As in most large ceca, the villi in small that it is virtually rudimentary, many birds the base are well developed and form an interhave ceca that are unequal in length, the right digitating meshwork, which, it has been sugcecum usually being the longer (Magnan, '11) gested, exerts a filtering action to exclude coarse (Fig. 2e) A much more important parameter than intestinal contents (Fenna and Boag, '74a). The length, from a functional viewpoint, is likely t o be ileocecorectal junction may also be modified, in the available surface area of the ceca. Unfortu- that the terminal part of the ileum protrudes for nately, measurements of this are not available. some distance into the rectal lumen as the ileal papilla, whereas surrounding the orifices of the FORM OF CECA ileum and the two ceca are three well developed Avian ceca may be either simple or sacculated. sphincters (Clarke, '78). A similar development of Simple ceca the ileal papilla and the ileal and cecal sphincters Simple ceca are tubular structures without out- has been described in the domestic duck (Anas pouchings or diverticula. From the data provided platyrhynchos) by Mahdi and McLelland ('88). by Maumus ('02a) and Naik ('621, it is possible to Sacculated ceca identify seven forms. These have outpouchings or diverticula and apa. Long, cylindrical ceca, e.g., in the cotton pear to be restricted t o a very small number of pygmy goose (Nettapus coromandelianus) (Fig. species, including some ratites (Struthio, Rhea 2f). and Apteryx) (Fig. li), the red-winged tinamou

ANATOMY OF AVIAN CECUM

(Rhynchotus rufescens) and the elegant crestedtinamou (Eudromia elegans) (Fig. 31, the redthroated loon (Gauia stellata), screamers (Anhimidae) (Fig. lg), the satyr tragopan (Tragopan satyra), the great bustard (Otis tarda) (Fig. lh), and the pin-tailed sand grouse (Pterocles alchata) (Garrod, 1876; Beddard, 1886, 1890, 1898; Beddard and Mitchell, 1894; Mitchell, 1895; Maumus, 'O2a; Groebbels, '32; Jacobshagen, '37). Except for ratites and the elegant crested-tinamou, there is little information about the ceca of these birds. In the ostrich (Struthio camelus) (Fig. li), the ceca in the mature bird are each about 95 cm in length (Bezuidenhout, '86) and their haustra-like sacs are arranged in a helical manner, the depressions between the sacculations corresponding internally t o a spiral valve-like fold with approximately 20 turns. In the proximal part of the ceca, the fold is very low, but after two spirals it reaches its greatest height and then diminishes progressively distally to terminte about 14 cm from the apex. Here sacculations are absent. In the Rhea, the helical arrangement of the sacculations is less obvious and the valvular transverse folds seem t o be arranged in two longitudinal rows, which alternate with one another. The ceca in Apteryx, by comparison, have few sacculations. Among the screamers, the cecal sacculations may be due to the shortening of a single longitudinal muscular band as in the northern screamer (Chauna chauaria) (Fig. lg) or to two bands as in the southern screamer (Chauna torquatu). This arrangement would be very similar to the elastic or muscular teniae occurring in the horse large intestine. According t o Garrod (18961, the openings of the ceca in Chauna torquata are surrounded by well developed sphincters and lead into a diverticulum of the rectum. The unusual ceca of the elegant crested-tinamou (Eudromia eleguns) (Beddard, 1890) exhibit numerous minute papilliform outgrowths (Fig. 3). Corresponding t o these outgrowths, the internal surface has a network of ridges similar to those of the ruminant reticulum. Towards the apex of each cecum, the diverticula are less developed, although the ridges increase slightly in size. Here the ridges running at right angles to the long axis become more numerous than those running longitudinally, with the result that over the last few centimetres the honeycomb appearance is almost replaced by a spiral valve-like arrangement. Sharp-edged pebbles have been observed in the lumen of this cecum (Maumus, 'O2a).

W
Fig. 3. Cecum of the elegant crested-tinamou (Eudromia elegans). (From Beddard, 1890, with permission of the publisher.)

CECAL DEVELOPMENT AND RECTAL LENGTH Newton and Gadow (1896) proposed that a correlation exists between the degree of development of the ceca and the length and width of the rectum, but they provided no supporting evidence. Despite extensive data on cecal and rectal lengths in a large number of species (Beddard, 1898; Magnan, '11; Naik, '62) it is difficult to distinguish a recognizable pattern, a view also supported by Jacobshagen ('37). By far the most anatomically distinctive rectum belongs to the ostrich (Struthzo camelus). In this bird (which also has large, sacculated ceca), the rectum measures about 16 m in length (Bezuidenhout, '86). It can be divided into a sacculated thin-walled proximal part with a wide lumen and an unsacculated thick-walled distal part with a narrow lumen. The ratio of length for the rectum vs. the small intestine is about 2 : 1. Although in the majority of species the rectum is a straight tube, it is coiled in Struthio (Bezuidenhout, '86) and also in Rhea, Chauna, and Opisthocomus (Mitchell, 1896).

J. McLELLAND

CECAL DEVELOPMENT AND DIET

A relationship between the size of the ceca and diet has been proposed by a number of workers (Mitchell, '01; Maumus, 'O2a; Magnan, '11; Pinchon, '42). Although there were important exceptions, large ceca were correlated with herbivory and small ceca with carnivory. More recently, Naik ('62), on the basis of observations on 80 species of Indian birds belonging to 33 families in 15 orders, reported that the ceca tend to be well developed in omnivores, herbivores, and mollusceaters; small in piscivores and graminivores; and highly variable in length in insectivores and carnivores. One problem in the ceca-diet relationship is that very few species are restricted to a single food. Furthermore, there are often other interspecific variables including seasonal changes in diet, differences in diet due to different ecological habitats, and variations in diet with age. A review of the diets of birds based on Landsborough Thomson ('64) shows clearly that most feeding LITERATURE CITED habits are represented within each of the three categories of ceca described (p. 6). Among birds Abraham, K. (1901) Beitrage zur Entwicklungsgeschichte des Wellen-sittich (Melopsittacus undulatus). Ergebn. with long ceca, for example, are species known Anat. Entwbesch., 17:589. preferentially to eat many different types of food, Beddard, F.E. (1886) On some points in the anatomy of including meat, vegetable matter, seed, fruit, inChauna chauaria. Proc. Zool. SOC. Lond., 1886:178-181. sects, and small invertebrates, whereas many are Beddard, F.E. (1890) On the alimentary canal of the Martineta Tinamou (Calidronas elegans). Ibis, 1890:61-66. truly omnivorous. Moreover, birds eating the same diet usually exhibit a wide range of cecal Beddard, F.E. (1898) The Structure and Classification of Birds. Longmans, Green and Co., London. development. The ceca in insect-feeders, for ex- Beddard, F.E., and P.C. Mitchell (1894) On the anatomy of ample, are extremely long in nightjars, trogons, Palameda cornuta. Proc. Zool. Sac. Lond., 1894.536-557. and bee-eaters but only vestigial or even absent Bezuidenhout, A.J. (1986) The topography of the thoracoabdominal viscera in the Ostrich (Struthio camelus). Onderin many passerines, some cuckoos, and swifts. stepoort J.Vet. Res., 53.111-117, Some carnivores have ceca that are very long and G.L.L. (1770) Histoire naturelle des Oiseaux. Delimexpanded (owls); in others they are poorly devel- Buffon, primerie Royale, Paris. oped and often vestigial (hawks). Although vesti- Clarke, P.L. (1978) The structure of the ileo-caeco-colicjuncgial ceca are characteristic of many piscivores tion of the domestic fowl (Gallus gullus L.). Br. Poult. Sci., 19:595-600. such as penguins and gannets, large ceca occur in divers and loons, and in at least one species, Corti, A. (1923) Contributo alla migliore conoscenza dei diverticuli chiechi dell' intestino posteriore degli uccelli. Ric. the red-throated loon (Gavia stellata), they are Morf., 3:211-295. sacculated. Thus correlations between cecal de- Coues, E. (1890) Handbook of Field and General Ornithology. velopment and diet are tenuous for many species. Macmillan, London. The obligate browsers (grouse) of the family Cuvier, G. (1835) Leqons d'Anatomie ComparBe. Paudouin, Paris, Vol. IV. Tetraonidae represent a group with a clear relaNobleville, A. and F. Salerne (1756) Histoire naturelle tionship between diet and cecal size. These birds deeclaircie dans une de ses parties, I'ornithologie. Paris. possess simple ceca that are massively elongated Fenna, L., and D.A. Boag (1974a) Filling and emptying of the and relatively much larger than in seed-eating galliform caecum. Can. J. Zool., 52.537440. galliforms such as partridges and pheasants. The Fenna, L., and D.A. Boag (1974b) Adaptive significance of the caeca in Japanese quail and spruce grouse (Galliformes). combined lengths of both ceca often approximates Can. J. Zool., 52:1577-1584. that of the small intestine (Leopold, '53). The Gadow, H. (1891) Vogel. In: Bronn's Klassen und Ordnungen large size of the ceca is related to the cellulose des Thierreichs Anat. Theil. C.F. Winter'sche, Leipzig, Vol. content of the diet, the ceca acting as fermenta6.

tion chambers (Gasaway, '76). Furthermore, significant increases in cecal length have been shown to occur following seasonal or artificial changes in diet t o one containing a higher fiber content (Lewis, '63; Pendergast and Boag, '70, '73; MOSS, '72; Fenna and Boag, '741, the changes, however, apparently being prompted by an increase in the food ingested per unit time rather than by a change in the quality of the diet. Although a similar potential for cellulose digestion appears t o exist in some herbivorous species with sacculated ceca (ostrich, rheas, and screamers), specific information is unfortunately lacking. It should be noted that the fermentation process need not be restricted to enlarged or sacculated forms of ceca. There is evidence in the emu (Rromaius novaehollandiae), for example, which has relatively small ceca (120 mm in length compared with 1440 mm in the red grouse, Lagopus lagopus scoticus) that fermentation occurs in the distal part of the small intestine (Herd and Dawson, ' 8 4 ) .

ANATOMY OF AVIAN CECUM

Garrod, A.H. (1876) On the anatomy of Chauna derbiana, and on the systematic position of the screamers (Palamedeidae). Proc. Zool. SOC. Lond., 1876:189-200. Gasaway, W.C. (1976) Volatile fatty acids and metabolizable energy derived from cecal fermentation in the Willow Ptarmigan. Comp. Biochem. Physiol., 53A:115-121. Gesner, C. (1585)Historiae Animalium. Cambieriano, Francofurti. Groebbels, F. (1932) Der Vogel. Bau, Funktion, Lebenserscheinung, Einpassung. Borntraeger, Berlin, Vol. 1. Herd, R.M., and T.J. Dawson (1984) Fibre digestion in the Emu, Dromaius nouaehollandiae, a large bird with a simple gut and high rates of passage. Physiol. Zool., 57:7-84. Home, E. (1814) Lectures on Comparative Anatomy. Nicol, London, Vol. 1. Jacobshagen, E. (1937) Mittel- und Enddarm. In: Handbuch der vergleichenden Anatomie der Wirbeltiere. L. Bolk, E. Goppert, E. Kallius, and W. Lubosch, eds. UrbanSchwy-zenberg, Berlin and Vienna, Vol. 3. Landsborough Thomson, A. (1964) A New Dictionary of Birds. Nelson, London. Leopold, AS. (1953) Intestinal morphology of gallinaceous birds in relation to food habits. J. Wildlife Mgmt., 17:197203. Lewin, V. (1963) Reproduction and development of young in a population of California Quail. Condor, 66249-278. LHerminier (1837) Recherches anatomiques sur quelques genres doiseaux rares ou encore peu connus sous le rapport de lorganisation profonde. Ann. Sci. Nat. Zool., 8:96-106. McLelland, J. (1979) Digestive system. In: Form and Function in Birds. A.S. King and J. McLelland, eds. Academic Press, London and New York, Vol. 1. Magnan, A. (1911) Le Tube Digestive et le R6gime Alimentaire des Oiseaux. Theses, Univ. Paris. Mahdi, A.H., and J. McLelland (1988) The arrangement of the muscle at the ileo-caeco-rectal junction of the domestic duck (Anas platyrhynchos) and the presence of anatomical sphincters. J. Anat. (in press). Markus, M.B. (1964) Intestinal caeca in the South African Columbida. Bull. B.O.C., 84:137-138. Maumus, J. (1902a) Les Caecums des Oiseaux. Theses, Fac. Sci., Paris. Maumus, J. (1902b) Les caecums des oiseaux. Ann. Sci. Nat. Zool., 15:1- 148. Meckel, J.-F. (1821-1831) System der vergleichenden Anatomie. Rengerschen Buchhandlung, Halle. Mitchell, P.C. (1895) On the anatomy of Chauna chuuaria. Proc. Zool. SOC. Lond., 1895:350-358.

Mitchell, P.C. (1896) On the intestinal tract of birds. Proc. Zool. SOC. Lond., 1896:136-159. Mitchell, P.C. (1901) On the intestinal tract of birds, with remarks on the valuation and nomenclature of zoological Lond. Zool., 8:173-275. characters. Trans. Linn. SOC. Naik, D.R. (1962) A Study of the Intestinal Caeca of some Indian Birds. M.Sc. Thesis, Banaras Hindu University. Naik, D.R., and C.J. Dominic (1962) The intestinal caeca of some Indian birds in relation to food habits. Naturwissenschaften, 49:287. Naik, D.R., and C.J. Dominic (1963) The intestinal caeca as a criterion in avian taxonomy. Proc. 50th Ind. Sci. Congr., 1962, Part 111533. Naik, D.R., and C.J. Dominic (1968) Intestinal caeca of owls. Roc. 55th Ind. Sci. Congr. 1968, Part 111522. Naik, D.R., and C.J. Dominic (1969) A study of the intestinal caeca of some Indian birds. Proc. 56th Ind. Sci. Congr., 1969, Part III:473-474. Newton, A,, and H. Gadow (1896) A Dictionary of Birds. Black, London. Pallas, P.-S. (1767) Spicilegia Zoologica. Lange, Berolini. Pendergast, B.A., and D.A. Boag (1970) Seasonal changes in diet of Spruce Grouse in central Alberta. J. Wildlife Mgmt., 34:605-611. Pendergast, B.A., and D.A. Boag (1973) Seasonal changes in the internal anatomy of the Spruce Grouse in Alberta. Auk, 90:307-317. Perrault, C. (1758) Memoires pou servir a 1Histoirenaturelle des Animaux. Arkstee and Merkus, Amsterdam and Leipzig. Pilz, H. (1937) Artmerkmale am Darmkanal des Hausgeflugels (Gans, Ente, Huhn, Taube). Morphol. Jb., 79:275304. Pinchon, R. (1942) Contribution a 16tude morphologique des caecums dans la serie des oiseaux. Thkses, Fac. Sci., Univ. Paris. Pycraft, W.P. (19101 A History of Birds. Methuen, London. Schumacher, S. (1925) Der Bau der Blinddarme und des ubrigen Darmrohres von Spielhahn (Lyrurus tetrix L.). Z. Anat. Entgesch., 76:640-644. Siebold, C.T. and H. Stannius (1848) Lehrbuch der Vergleichenden Anatomie. Viet, Berlin. Tiedemann, F. and L. Gmelin (1827) Recherches experimentales physiologiqu6s et chimiques sur la digestion consideree dans les quatre classes danimaux vertebres. Bailliere, Paris. Wetmore, A. (1920) Intestinal caeca in the Anhinga. Auk, 37:286-287.