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Revista chilena de anatomía

Print version ISSN 0716-9868

Rev. chil. anat. vol.16 n.2 Temuco  1998 

(Speotyto cunicularia, MOLINA, 1782).

(Speotyto cunicularia, MOLINA, 1 782).

* Silvia de Oliveira Rocha
** Maria Aparecida Inforzato de Lima

ROCHA, D. O. S. & DE LIMA, M. A. I. Histological aspects of the stomach of burrowing owl (Speotyto cunicularia, MOLINA, 1782). Rev. Chil. Anat., 16(2):191-197, 1998.

SUMMARY: A histological study of burrowing owl stomach, proventriculus and ventriculus was carried out under light microscopy.

On the proventriculus (proventriculus, pars glandularis) the lining columnar mucous cells epithelium presents folds and superficial simple tubular gland (gll. proventricularis superficiales and lamina muscularis mucosae), supported by corion, form the tunica mucosa gastris. The thick tela submucosae gastris is predomnantly constituted by numerous and exuberant gll. proventricularis gastris profundae, a branched tubular type gland that open to mucosae surface. A well developed tunica muscularis gastris of smooth muscle presents internal stratum circulare and external stratum longitudinal. Between these two layers the connective tissue shows the presence of blood vessels and ganglion cells of Auerbach plexus.

The tunica serosa is constituted by connective tissue containing adipose cells, blood vessels and nervous elements of serous plexus. In the ventriculus (ventriculus, pars muscularis) situated caudally to proventriculus, histologically we found the same tunics of the antecessor, excepting the lack of tela submucosae gastris.

The linning columnar epithelium with low folds connected by a thick cuticle (cuticula gastrica) and simple tubular gland (gll. ventricularis) followed by lamina mucosa gastris.

Separated by a thin connective tissue, adjacent to lamina muscularis mucosae, there is the well developed tunica muscularis gastris with thick inner layer (stratum circulare) and outer layer (stratum longitudinale) showing between them plexus of Auerbach.

The tunica serosa of ventriculus is similar to that of proventriculus.

KEY WORDS: 1. Stomach; 2. Speotyto cunicularia; 3. Anatomy.


The digestive tract of birds is descrited, in the literature as constituted by mouth limited by beak, salivary gland, tongue, pharinx, esophagus with ou without craw, stomach with proventriculus and ventriculus (gizzard), small intestine and large intestine, including caeci and coprodeum (CALHOUN, 1954; FARNER, 1960; SELANDER, 1963; TONER, 1963; HELANDER, 1981).

The size of different portions of digestive tract of birds varies according to the type of alimentary habits

(FARNER; McLELLAND, 1979; KEHOE & ANKEY, 1985; JORDANO, 1987).

Generally, the stomach of birds is descrebed as a very elastic muscle-membranous tube which extends from pharinx to proventriculus, containing, in the majority of birds a dilation next to thoracic cavity called craw (FARNER; WARNER et al., 1967; FITZGERALD, 1969; LIMA, 1977; McLELLAND.

Esophagus is internally lined by squamous stratified and cornified epithelium and presents esophagian mucous glands (KADEN, 1936; LIMA, 1977).

The stomach of birds is divided into two chambers: proventriculus (proventriculus, pars glandularis) and gizzard (ventriculus, pars muscularis) that is the muscular portion (CALHOUN; FARNER; McLELLAND).

The region of transition between proventriculus and gizzard of ventriculus is named zona intermedia gastris that is present in the majority of birds. This region is separeted from proventriculus by a constriction or isthmus (isthmus gastris) (HODGES, 1974). It is admitted that the physiology of proventriculus is to secrete the gastric juice, however, this is yet a matter of contention; meanwhile the gizzard would have the mechanical function of trituration of food (CALHOUN; FARNER; TONER; McLELLAND). Characterizing the proven-triculus there are submucosae glands that occupie the great majority of wall area (SELANDER).

TONER studying domestic birds agrees with CHODNIK (1947) who described the linning epithelial cells of proventricular glands as being cuboidal or columnar type agrees with of proventricular glands as being cuboidal or columnar type.

The ventriculus, because of its function of compression and trituration of food, has a more developed musculature mainly in the insectivorous and graminivorous birds that eat food more hard compared with the carnivorous or piscivorous birds (FARNER; STURKIE, 1965; McLELLAND).

In the distal portion of stomach, anatomically can be distinguished the pyloric part (pars pylorica) that is situated between ventriculus and duodenum. This region shows an intermediary structure between these two (McLELLAND).

In relation to the morphology of owl digestive tract, we found poor references in the literature. This fact awakened our interest to study the morphology (histology) of stomach of this bird.

Thus, we proposed to carry out the histological study of stomach (proventriculus and ventriculus) of burrowing owl, Speotyto cunicularia (Ave strigidae) very familiar in the Brazilian field and grazing ground. This bird presents alimentary habits at twilight and night, but also, can chase during the day light. It is carnivorous bird, but insect are also, part of its food at major rate than that of the little vertebrates (SCHUBART et al.).


In the present work, we utilized 4 adult male burrowing owl (Speotyto cunicularia) weighing approximately 150 g, captured in the country side of São Paulo, Brazil.

The birds were kept in individual cages, fed with new-born rats, chow for dogs and water ad libitum during 3 days at circadian time table (12 h of light and 12 h of dark).

After anesthesia by sulphuric ether innalation, the digestive tube was exposed and rinsed with saline solution on paraffin wax plate (Fig. 1) and fragments of proventriculus and ventriculus were fixed for 24 hours in Bouin's solution and for 18 hours in acetate formaline, at 4C. Following, the fragments were dehydrated with series of crescent concentrations of ethylalcohol. After dehydration and treatment with xylene, the fragments were imbedded in paraffine wax. Histological sections of 6 micrometers were stained by Hematoxylin and Eosin and Polychrome method (CASTRO & CAMARGO, 1951).

The nomenclature description of the regions were according to Nomina Anatomica Avium (McLELLAND).


In the burrowing owl, as in the majority of birds, the stomach (gaster) is constituted by two distinct chambers: proventriculus (proventriculus, pars glandularis), representing chemical or glandular stomach; and ventriculius (ventriculus, pars muscularis) or gizzard named mechamical or muscular stomach.


The tunica mucosa (tunica mucosa gastris) is folded, someting presenting anastomosis of the folds and the lining epithelium is columnar simple with clear cytoplasm. The cells of basal region of folds are low and much more stained than those of superficial region.

In the lamina propria, we found simple tubular gland (gll. proventriculus superficiales) whose glandular cell are similar to those of superficial lining epithelium. (Fig. 1-A)

Fig. 1. A. Photomicrograph proventriculus mucosae epithelium. p = epithelium folds; l = lamina propria; g = proventriculus deep glands; d = central unique duct; ® = connective tissue septum; m = muscular tunica, magnification : 90x.

Beneth lamina propria, some isolated smooth muscle are present, constituing a thin muscularis mucosae (lamina muscularis mucosae). The tunica submucosae

(tela submucosa gastris) is formed by frame of conective tissue containing numerous and volumous proventricular wall. These exuberant branched tubular type gland are, each of them, cuboid epithelial cells that are intensely eosinophilic and those situated at basal position give a serrated appearance. All of the branched tubular glands open to the main unique tubule, also, lined up by cuboid cell, which leads to proventricular lumin al surface.

Among proventricular gland capsule are present septa of thin connective tissue that extend to muscular tunic.

The tunic muscular (tunica muscularis gastris) is constituted by two layers of smooth muscle fibers. The inner layer (stratum circulare) is thick and arranged circulary, and the outer layer (stratum longitudinare), where the muscle fibers have longitudinal disposition (Fig. 1-B).

Fig. 1. B. Photomicrograph proventriculus mucosae epithelium. ep = lining columnar gastric epithelium. lu = glandular lumen,magnification: 250x.

Between these two muscular layer, can be seen blood vessels and myoenteric nervous plexus (Auerbach).

The proventriculus serosa (tunica serosa) is formed by conective tissue wich in blood vessels and nerves and ganglionic cells of serous plexus.

Ventricular or gizzard

Gizzard (ventriculus) is situated caudally to proventriculus and present a slightly flattened oval shape.

Tunica mucosa (tunica mucosa gastris) is well developed. The lining columnar epithelium presents folds of varied heights and is covered by typical cuticle (cuticula gastris) of ventricular. In the lamina propria, many tubular glands, sometimes branched open always at base of superficial lining cell folds.

Lamina propria is limited by a thick longitudinally disposed smooth muscular layer (lamina muscularis mucosae) that continues to muscular tunic. The submucosal tunic (tela submucosae gastris) was not identified.

Muscular tunic (tunica muscularis gastris) is well developed and we distinguished basically two smooth muscle layers, an externalthin longitudinal layer (stratum longitudinale) and other internal thick circular layer (stratum circulare).

Between these two muscular layers, can be seen, a thin connective tissue blood vessels and nervous myoenteric plexus of Auerbach.

The serosa (tunica serosa) is characteristically represented by mesothelial lining epithelium and conective tissue rich in blood vessels and nervous elements of serous plexus.


The birds, to maintain their high metabolical level, utilize the most of their time for search of the food.

Our interest was directed to the histological description of burrowing owl stomach (proventriculus and ventriculus).

The varied species of birds present different alimentary habits. Concerning to the digestive tract morphology of birds (CALHOUN) mensions in the literature, the existence of controversy, in relation to the number of tunics in the digestive tract wall.

MARSHALL & FOLLEY (1956) consider the existence of only three tunics, meanwhile, the great majority of authors admit as four number of tunics as we do.

In burrowing owl, proventriculus is constituted by the same four tunic, just has described antecedently (HODGES; MENIN et al., 1990).

The tunica mucosa in totally folded and the lining epithelium in the characteristic cuboidal or columnar in burrowing owl proventricular mucosa, as in other birds


In the burrowing owl, according to SELANDER, the morphological variation of oval or circular form is related with phase of cell activity.

In lamina propria, beneth lining epithelium near the base of folds, in the present work, small sample tubular glands (superficial glands) described by McLELLAND opening to the base of folds.

In 1977, LIMA observed these glands of Columbia livia situated among folds apparently seeming as a simple cubic epithelial invaginations.

Some authors (LIMA; McLELLAND; FIERI) described beyond superficial glands, an additional major glands occupying the greater part of this wall (deeper glands). However other authors as BRADLEY & GRAHME (1951); TONER do not agree with these findings and refer to deeper proventricular glands in the submucosa tunica coinciding with our observations.

Fig. 2. Photomicrograph of gizzard mucosae epithelium. mm = muscular mucosa E; ep = lining columnar epithelium of gizzard; gep = glandular columnar epithelium; tm = muscular tunica; s = serosa, magnification: 90x.

In regard to lamina propria, the results of this investigation coincide with those of FIERI, who described the lamina propria as being constituted by connective tissue where can be present cells, collagen fibers and bloods vessels.

Beneth lamina propria, isolated smooth muscle of muscularis mucosae is well developed and it may be divided into two layers, one internal thick and adjacent to the boundary between glandular and lining epithelium surface and other thin longitudinal and between gland and submucosa. Both muscular layers of this muscularis mucosae are described by muscular bands that are situated between glandular components.

PERNKOPF & LEHNER (1937) suggested that the division of this muscle can be associated, somehow, with the mechanism of clearance of the gland.

In regard to tunica submucosa, our results showed that it is constituted by connective tissue that contains deep glands which take greet part of proventricular wall, meanwhile McLELLAND refered that this tunic in proven-triculus is extremely thin.

In relation to the localization and histology of these deep glands, are matter of contention. KOVAES (1928) proposed that histologically these glands are similar to those of fundus in mammalian stomach, and BROWNE (1922) stressed that the proventriculus is analogue with mammalian true stomach.

The proventricular deep glands, in great majority of birds are unilocular type. In our findings, we observed glands of tubular branched type, which presented enveloped by connective tissue capsule.

Separating, the gland each other, there were consuctive tissue septh which trespass submucosa to reach the muscular tunic.

In relation to the form of glandular cells, they na cuboidal type and their apical portions are not in contact with neighbor cells, giving the aspect to luminal surface of tubule, mainly when sectimed longitudinally. These findings coincide with those of FIERI.

Glandular tubules open to central collecting chamber lined up by simple columnar epithelium, and this collection of chamber continues to lumen of the unique excretory duct that open to the extremity of proventricular papilla.

Concerning to the muscular tunic, we found no disagreement with the results reported by other authors.

Therefore, we are in accordance with CALHOUN; McLELLAND (1979); FIERI (1984) that refered to an internal layer of smooth muscle fibers which are circular and thick, and another external layer longitudinal and thin. Between these two layers, can be observed blood vessels and nervus elements of myoenteric plexus (Auerbach). Finally, the tunica serosa of proventriculus is represented by connective tissue rich in blood vessels and ganglionar cells that belong to nervus plexus of serosa covered by mesothelium: in relation to ventriculus of burrowing owl, we described the same four basic tunics of proventriculus.

In many of varied species, the tunica mucosa is described as it is lined up by simple columnar epithelium (CALHOUN; LIMA; McLELLAND; FIERI) generally consisting of muciparous columnar or cuboidal cells, similar to those of other vertebrates (FARNER, 1960). The surface of ventriculus (gizzard) is totally lined up by a layer of queratinoid material that is constituted by a protein-polyssacarid complex (HODGES, 1974) manual cuticle that covers the luminal surface and the mucosa that contacts this cuticle presents many folds.

The lamina propria of burrowing owl ventricle is very developed and numerous simple tubular glands are seen and sometimes, they branch at their basal portion.

In relation to the existance of muscularis mucosae in ventriculus in matter of contention. Some authors as CALHOUN and McLELLAND refer to the absence of muscularis mucosae. Our findings display a muscularis mucosae constituted by smooth muscle fibers longitudinally disposed corresponding to the result of FARNER who described a well developed muscularis mucosae.

Due to the proximity of mucosa with tunica muscular, we could not describe the tunica submucosa, because it was impossible to identify it.

In the tunica muscular of burrowing owl ventriculus, we do not find the three layers as refereed in Uroloncha domestica by IMAIZUMI & HAMA (1969) that described the tunica muscular occupying the major part of the organ wall, that is constituted by internal circular layer external, longitudinal layer and the last poorly developed layer that, sometimes, in many of species may be absent (SWENANDER, 1902).

Considering the complexity of disposition of smooth muscular fibers of the ventriculus, we believe that only a detailed study of the different regions could provide more satisfactory results concerned with morphology.

Finally, the tunica serosa of burrowing owl ventriculus is very similar to that the majority of birds which is constituted by connective tissue and covered by mesothelium that presents ganglionic cells of nervous plexus of serosa.

ROCHA, D. O. S. & DE LIMA, M. A. I. Aspectos histológicos del estómago de la lechuza (Speotyto cunicularia, MOLINA, 1782). Rev. Chil. Anat., 16(2):191-197, 1998.

RESUMEN: Fue realizado un estudio histológico con microscopio óptico, del estómago, proventrículo y ventrículo de la lechuza. En el proventrículo (proventriculus, pars glandularis), el epitelio de las células de la mucosa columnar del revestimiento presenta láminas y una glándula tubular simple superficial (gll. proventricularis superficiaes y lamina muscularis mucosae), apoyado por corion, formando la túnica mucosa gástrica. La tela fina, submucosae gastris está constituida predominantemente por numerosas y exuberantes gll. proventricularis gastris profundae, una glándula de tipo tubular bifurcada que se abre sobre la superficie de la mucosa. Una tunica muscularis gastris bien desarrollada de músculo liso presenta internamente stratum circulare y externamente stratum longitudinal. Entre esas dos capas, el tejido conectivo muestra vasos sanguíneos y células ganglionares del plexo de Auerbach. La túnica serosa está constituida por tejido conectivo que presenta células adiposas, vasos sanguíneos y elementos nerviosos de plexo seroso.

En el ventrículo (ventriculus pars muscularis) situado caudalmente al proventrículo, encontramos histológicamente las mismas túnicas que en el anterior, exceptuando la tela submucosae gastris.

El epitelio columnar de revestimiento presenta pocas láminas conectadas por una fina cutícula (cuticula gastrica) y glándula tubular simple (gll. ventricularis) seguida por lamina mucosa gastris.

Separado por un fino tejido conectivo, adyacente a la lamina muscularis mucosae, se encuentra una bien desarrollada tunica muscularis gastris con una fina capa interna (stratum circulare) y otra externa (stratum longitudinale), mostrándose entre ellas el plexo de Auerbach. La túnica serosa del ventrículo es similar a la del proventrículo.

PALABRAS CLAVE: 1. Estómago; 2. Speotyto cunicularia; 3. Anatomía.

* Regent Professor of the Department of Morphology and Physiology of Faculdade de Medicina do ABC, Santo André, S.P., Brazil.
** Adjunt Professor of Histology of the Department of Morphology of Universidade Federal de São Paulo, S.P., Brazil.

Dirección para correspondencia:
Prof. Silvia de Oliveira Rocha
Av. Dra. Altino Arantes, 870 Apto. 123
Vila Clementino - CEP 04042-004
São Paulo - SP

Recibido : 22-07-1998
Aceptado: 17-08-1998


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