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Revista chilena de anatomía

Print version ISSN 0716-9868

Rev. chil. anat. vol.18 n.2 Temuco  2000

http://dx.doi.org/10.4067/S0716-98682000000200006 

COMPARATIVE MORPHOLOGY OF THE OVARIES OF THREE SPECIES OF
DASYPODIDAE (MAMMALIA, XENARTHRA)  


MORFOLOGÍA COMPARADA DEL OVARIO DE TRES ESPECIES DE DASIPÓDIDOS
(MAMMALIA, XENARTHRA)

* Stella Maris Codón
** Emma Beatriz Casanave

 

CODÓN, S. M. & CASANAVE, E. B. Comparative morphology of the ovaries of three species of Dasypodidae (Mammalia Xenarthra). Rev. Chil. Anat., 18(2):251-257, 2000.

SUMMARY: Ovarian morphology in the armadillos Chaetophractus vellerosus (Gray, 1865), Zaedyus pichiy (Desmarest, 1804) and Dasypus hybridus (Desmarest, 1804), was studied.

Chaetophractus vellerosus and Z. pichiy present cylindrical ovaries with rounded extremities, a ventral parenchymatous zone "cortex" and a dorsal vascular one "medulla", with typical structure. In D. hybridus they are bean-shaped, the concavity corresponding to the parenchymatous zone and the convexity to the vascular zone. The presence of polyovular follicles in C. vellerosus and Z. pichiy is usual. Structures associated with the ovary (epoophoron, rete ovarii) are similar in the three species. While the features of the ovaries of C. vellerosus and Z. pichiy are comparable with those of C. villosus (Desmarest, 1804), the ones of D. hybridus are similar to those of D. novemcinctus Linné, 1758.

KEY WORDS. 1. Armadillos; 2. Dasypodidae; 3. Morphology; 4. Ovary. INTRODUCTION

Chaetophractus vellerosus (Gray, 1865), Zaedyus pichiy (Desmarest, 1804) and Dasypus hybridus (Desmarest, 1804) are armadillos belonging to the family Dasypodidae in the South-American Order Xenarthra (Edentata), which also includes anteaters and sloths.

Although the importance of armadillos from both the zoological point of view and as experimental models in biomedical studies is well-known (STORRS et al., 1974; P.A.H.O., 1978; GARCÍA SAMARTINO et al., 1987; MALDONADO & CASANAVE, 1996; CASANAVE & POLINI, 1999; POLINI et al., 1999), the insufficient knowledge about their reproductive features is noticeable. Dasypus novemcinctus Linné, 1758 (NEWMAN & PATTERSON, 1910; NEWMAN, 1912; ALTMANN, 1924; TALMAGE & BUCHANAN, 1954; ENDERS & BUCHANAN, 1959; ENDERS, 1960) and C. villosus (Desmarest,1804) (CODÓN & CASANAVE, 1996; CODÓN, 1997; CODÓN et al., in press), are the only species whose ovaries had been studied both from the anatomical and histological point of view.

The objective of this work is to describe the ovaries of C. vellerosus, Z. pichiy and D. hybridus, as a contribution to the knowledge of their morphology.

MATERIAL AND METHOD

Armadillos were live-trapped every month in the Bahía Blanca area, Buenos Aires, Argentina, within a ratio of 40-90 km southwest of the city. Seventeen mature female armadillos, C. vellerosus (n = 7, weight 780 - 1.140 g), Z. pichiy (n = 5, weight 900 - 1.160 g) and D. hybridus (n = 5, weight 1.200 - 1.600 g), were used. Specimens were euthanized with 75 mg/kg sodium thiopentate (i.p.). Ovaries were observed in situ to describe their anatomical relations. For histological study, they were fixed in Bouin' fluid, dehydrated, embedded in paraffin and sectioned at 5 µm thickness with a Leitz microtome. Sections were stained with haematoxylin-eosin and Masson's trichrome. They were examined and photographed with a Nikon AFM microscopy.

RESULTS

The three species have a pair of ovaries fixed to the sublumbar region by the anterior portion of the broad ligament of the uterus, the mesovarium. They lie to both sides of the cranial region of the uterus, ventrally to it. They are located caudally and laterally to the kidneys. The proper ligament of the ovary extends from its uterine extremity to the uterine fundus. In C. vellerosus and Z. pichiy, the ovaries are cylindrical with rounded extremities, with the long axis featuring an oblique orientation in respect to the middle line and to the transverse axis of the animal (Figs. 1, 2). In D. hybridus they are bean-shaped and parallel to the longitudinal axis, with the concavity oriented to the middle line and the convexity, where the blood vessels enter to the ovary (hilum), located laterally (Fig. 3).




Figs. 1, 2 and 3. Ventral view of the ovary and the oviduct: 1. Chaetophractus vellerosus; 2. Zaedyus pichiy; 3. Dasypus hybridus (a, ampulla; f, fimbriae; i, isthmus; o, ovary). Bars: 2 mm.

In the three species the ampulla of the oviduct coils around the tubal extremity of the ovary and the fimbriae are located over the parenchymatous zone (Figs. 1-3). In addition, the ampulla of Z. pichiy extends ventrally and reaches the middle of the ovary (Fig. 2), while in D. hybridus it continues caudally along the concave side up to the middle of the ovary too (Fig. 3). In C. vellerosus, the isthmus begins in the tubal extremity of the ovary and is related with the ventral side of it (Fig. 1). In Z. pichiy, it begins in the middle of the ovary and extends ventrally, to the mid-line (Fig. 2). In D. hybridus, it also begins in the middle of the ovary but continues caudally (Fig. 3).

The ovary of C. vellerosus and Z. pichiy has a ventral parenchymatous zone with the typical structure of ovarian cortex (Fig. 4) and a dorsal vascular zone corresponding to the ovarian medulla. In D. hybridus, the concave side corresponds to the parenchymatous zone and the convex one to the vascular zone. In the three species the parenchymatous zone, covered by a mesothelium made up of a simple layer of cuboidal cells, is composed of a stroma of loose connective tissue which externally is more fibrous, thus forming the tunica albuginea (Figs. 4, 5). The ovarian vascular zone made up of loose connective tissue has numerous blood vessels (Fig. 6).


Fig. 4. Light micrograph of the ovarian cortex of Zaedyus. pichiy with follicles (f) in different degree of develop-ment as well as atretic follicles (a). Note the numerous polyovular follicles (p) and the tunica albuginea (arrow). Masson. 100x. Inset: Detail of a polyovular tertiary follicle with three oocytes, one of them in atretic stage. Masson. 100x.

The parenchymatous zone contains the ovarian follicles in different stages of development (Figs. 4, 5). Primordial, primary, secondary, tertiary and Graafian follicles, were distinguished. The primordial ones, with the oocyte surrounded by one layer of flat follicular cells, are periferically placed in C. vellerosus and Z. pichiy. In D. hybridus, the concavity is the zone with the greatest concentration of primordial follicles (Fig. 5). In the three species the growing follicles are in the inner portion of the parenchymatous zone (Figs. 4, 5). Primary follicles have the oocyte surrounded by a single layer of cuboidal cells, secondary follicles have two or more layers of cuboidal follicular cells, tertiary follicles have fluid filled spaces between the follicular cells arranged in numerous layers and Graafian follicles have a single cavity with the oocyte peripherally placed. Atretic follicles with different degree of growth were also observed (Fig. 4).


Fig. 5. Ovarian cortex of Dasypus hybridus surrounded by the tunica albuginea (arrow), showing abundant primordial follicles (*) in the zone of the concavity and follicles (f) with different degree of development in the inner portion. Masson. 100x.

In addition to the monovular follicles described, polyovular follicles containing more than one oocyte, were observed until the stage of tertiary follicle in C. vellerosus and Z. pichiy (Fig. 4).

Corpora lutea with typical mammal histology was observed both in one specimen of C. vellerosus gathered in late September and in one of D. hybridus collected in March, occupying most of the ovarian mass in the latter. Neither embryos in none of the two specimens, nor free vesicles in the uterus of D. hybridus were observed.

The morphology and location of the structures associated with the ovary (epoophoron and rete ovarii) are similar in the three species. The epoophoron, made up of tubules with a simple ciliated, light columnar epithelium, is placed cranially to the ovary, in the connective tissue that surrounds the ampulla of the oviduct (Fig. 7). The rete ovarii, with tubules lined by a simple cuboidal or low columnar epithelium, is located between the epoophoron and the body of the ovary (Fig. 7), extending into the ovarian vascular zone (Fig. 6). Connection between epoophoron and rete ovarii was observed in Z. pichiy (Fig. 7).


Fig. 6. Tubules of the rete ovarii (r) lined by low columnar epithelium in the vascular zone (m) of the ovary in C. vellerosus. Note blood vessels (v). Masson. 100x.


Fig. 7. Epoophoron (e) and rete ovarii (r) in the connective tissue surrounding the ampulla of the oviduct, cranially to the ovary in Z. pichiy. Note the connection (arrow) between them. Masson. 40x. BUCHANAN, ENDERS).

DISCUSSION

The shape of the ovaries in C. vellerosus, Z. pichiy and D. hybridus differs from the fusiform one referred as characteristic of Dasypodidae by GRASSÉ (1955) and RAYNAUD (1969). However, the shape as well as the orientation of the ovary of C. vellerosus and Z. pichiy, are comparable with those reported for C. villosus (CODÓN, CODÓN & CASANAVE) and the ones of D. hybridus are similar to those described for D. novemcinctus (NEWMAN & PATTERSON, TALMAGE & BUCHANAN, ENDERS & BUCHANAN, ENDERS)

Regarding the relations of the ovary and the oviduct of the three species, they differ from one another as well as from those of D. novemcinctus, where the relation with the ampulla takes place along the convex face of the ovary and the one with the isthmus occurs only in its uterine extremity (ENDERS & BUCHANAN). Even so, the disposition in C. vellerosus is similar to that described for C. villosus (CODÓN & CASANAVE).

The histological arrangement in a peripheral cortex and a central medulla considered as typical of mammals (PIRLOT, 1976; ROWELL et al., 1987; TAKADA et al., 1987; TEDMAN, 1991), is observed neither in the armadillo species here studied nor in C. villosus (CODÓN & CASANAVE). Nevertheless, the structure observed in our species is comparable to the one reported for the ovaries of adult Perissodactyla (SISSON & GROSSMAN, 1959).

Morphology of follicles is similar to that described for C. villosus (CODÓN et al.). The regular presence of polyovular follicles in C. vellerosus and Z. pichiy is coincident with the observed in several adult mammals (THEURING & HANSMANN, 1986; SWARTZ & CORKERN, 1992; MC DOUGALL et al., 1997). It would be interesting in the future to investigate whether polyovular follicles are functional.

The presence of corpora lutea in females of C. vellerosus collected in late September suggest that this is the time of ovulation of this species in our region. In addition, from our field and laboratory experience, especially the occurrence of births in November and December, we assume that its gestation period is about two months, as well as the reported for C. villosus (GRASSÉ) and Z. pichiy (REDFORD & EISEMBERG, 1992).

The observation of a large corpora lutea in a female of D. hybridus gathered in March, suggests that the specimen must have been either in the postovulatory phase or pregnant, in the period of delayed implantation characteristic of Dasypus (HAMLETT, 1935). It is worth pointing out that the time in which the corpora lutea was observed is in agreement both with the period of delay of implantation in Argentina (FERNÁNDEZ, 1909; HAMLETT) and with the ovulatory period (CUBA CAPARO, 1979). It is well known for D. novemcinctus that the corpora lutea, as well as the presence of free vesicles in the uterine lumen, are the most conspicuous features of the reproductive tract in the period of delayed implantation (HAMLETT). Moreover the very large size of the corpora lutea observed in D. hybridus was reported for both stages, postovulatory phase and delayed implantation, in D. novemcinctus (TALMAGE & BUCHANAN; ENDERS & BUCHANAN), making discrimination between them impossible from this point of view. Then, as free vesicles in the uterine lumen were not seen, we consider that the specimen was in the postovulatory period.

The morphology and location of the epoophoron in the three species are comparable with those of C. villosus (CODÓN & CASANAVE) and other mammals (KRESS & MILLIAN, 1987), but their location is more restricted than in D. novemcinctus (ENDERS & BUCHANAN). Moreover, the features of the rete ovarii in the three species are similar to those described for C. villosus (CODÓN & CASANAVE) and other mammals (BYSKOV, 1974; CZERNOVILSKY, 1985; ODEND'HAL et al., 1986; TAKEVA & MIHAILOVA, 1986; KELLER et al., 1987; MAITLAND & ULLMANN, 1993; ROSS et al., 1997) but their location differs from that of D. novemcinctus in which they are only in the tubal extremity of the ovary (ENDERS & BUCHANAN). The connection between epoophoron and rete ovary observed in Z. pichiy is coincident with the observed in D. novemcinctus (ENDERS & BUCHANAN) and some other mammals (KRESS & MILLIAN).

RESUMEN: Se estudió la morfología del ovario de armadillos Chaetophractus vellerosus, Zaedyus pichiy y Dasypus hybridus. En Chaetophractus vellerosus y Z. pichiy los ovarios son cilíndricos, con extremos redondeados, con una zona parenquimatosa ventral "corteza" y una zona vascular dorsal, "médula", con estructura típica. En D. hybridus son reniformes, correspondiendo la concavidad a la zona parenquimatosa y la convexidad a la vascular. Es destacable la presencia de folículos poliovulares en C. vellerosus y Z. pichiy. Las estructuras asociadas con el ovario (epoophoron, rete ovarii) son similares en las tres especies. Las características de los ovarios de C. vellerosus y Z. pichiy son comparables con las de C. villosus y las de D. hybridus son similares a las de Dasypus novemcinctus.

PALABRAS CLAVE: 1. Armadillos; 2. Dasypodidae; 3. Morfología; 4. Ovario. * Laboratorio de Histología Animal, Depto. de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur (UNS), Bahía Blanca, Argentina.
**Laboratorio de Fisiología Animal y Consejo de Investigaciones Científicas y Técnicas (CONICET), Depto. de Biología, Bioquímica y Farmacia.Universidad Nacional del Sur (UNS), Bahía Blanca, Argentina.

The paper was supported by Secretaría General de Ciencias y Tecnología, UNS, Project 24/BO60.

Dirección para correspondencia:
Prof. Dra. Stella Maris Codón
Depto. de Biología, Bioquímica y Farmacia
Universidad Nacional del Sur
San Juan 670
8000 Bahía Blanca
ARGENTINA

Email: smcodon@criba.edu.ar

Recibido : 21-08-2000
Aceptado: 27-09-2000

REFERENCES

ALTMANN, F. Beiträge zur anatomie des weiblichen genetales de Dasypodiden. Z. ges. Anat., 72:390-406, 1924.         [ Links ]

BYSKOV, A. G. Does the rete ovarii act as a trigger for the onset of meiosis? Nature, 252:396-7, 1974.         [ Links ]

CASANAVE, E. B. & POLINI, N. N. Comparative study of some haematological parameters of two wild Chaetophractus villosus (Mammalia, Dasypodidae) populations. Comp. Haematol. Int., 9(1):13-6, 1999.         [ Links ]

CODÓN, S. M. Estudio comparado del aparato genital de las hembras de los dasipódidos bonaerenses. Tesis doctoral, Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur, Bahía Blanca, Argentina, 1997.         [ Links ]

CODÓN, S. M. & CASANAVE, E. B. Histology of the ovary of the armadillo Chaetophractus villosus (Mammalia, Dasypodidae). Rev. Bras. Biol., 56:599-604, 1996.         [ Links ]

CODÓN, S. M.; ESTECONDO, S.G.; GALÍNDEZ, E. J. & CASANAVE, E. B. Ultrastructure and morphometry of ovarian follicles in the armadillo Chaetophractus villosus (Mammalia, Dasypodidae). Rev. Bras. Biol., 61(4), in press.         [ Links ]

CUBA CAPARO, A. Atlas de histología del armadillo de 7 bandas Dasypus hybridus. Buenos Aires, Centro Panamericano de Zoonosis, 1979.         [ Links ]

CZERNOVILSKY, B. Co-expression of cytokeratin and vimentin filaments in mesothelial, granulosa and rete ovarii cells of the human ovary. Eu. J. Cell. Biol., 370:175-90, 1985.         [ Links ]

ENDERS, A. C. A histological study of the cortex of the ovary of the adult armadillo, with special reference to the question of neoformation of oocytes. Anat. Rec., 136:491-9, 1960.         [ Links ]

ENDERS, A. C. & BUCHANAN, G. D. The reproductive tract of the female nine-banded armadillo. Tex. Rep. Biol. Med., 17:323-40, 1959.         [ Links ]

FERNÁNDEZ, M. Beiträge zur embryologie der gürteltiere. I. Zur keimblätterinversion und spezifischen polyembryonie der mulita (Tatusia hybrida Desm.). Morph. Jb., 39:302-33, 1909.         [ Links ]

GARCÍA SAMARTINO, L.; AFFANNI, J. M.; CASANAVE, E. B.; FERRARI, R. & IODICE, O. On the presence of a peculiar alpha rhythm in the olfactory tubercle of waking armadillos. Electroenceph. clin. Neurophysiol., 66:185-90, 1987.         [ Links ]

GRASSÉ, P. P. Ordre des Édentés. In: Traité de zoologie. V. 17. Fasc. II, p. 1182-266, Paris, Masson, 1955.         [ Links ]

HAMLETT, G. W. D. Delayed implantation and discontinuous development in the mammals. Quart. Rev. Biol., 10: 432-47. 1935.         [ Links ]

KELLER, L. S. F.; GRIFFITH, J. W. & MAX LANG, C. Reproductive failure associated with cystic rete ovarii in guinea pigs. Vet. Pathol., 24:335-9, 1987.         [ Links ]

KRESS, A. & MILLIAN, J. The female genital tract of the shrew Croccidura russula. Adv. Anat. Embryol. Cell. Biol., 101:1-74, 1987.         [ Links ]

MAITLAND, P. & ULLMANN, S. L. Gonadal development in the opossum, Monodelphis domestica: the rete ovarii does not contribute to the steroidogenic tissues. J. Anat., 183:43-56, 1993.         [ Links ]

MALDONADO, E. & CASANAVE, E. B. Electro-cardiography in Chaetophractus villosus (Mammalia, Dasypodidae). Revta. Ciênc. Bioméd., 17:17-22, 1996.         [ Links ]

MC DOUGALL, K.; HAY, M. A.; GOODROWE, K. L.; GARTLEY, C. J. & KING, W. A. Changes in the number of follicles and of oocytes in ovaries of prepubertal, peripubertal and mature bitches. J. Reprod. Fert., 51:23-51, 1997.         [ Links ]

NEWMAN, H. H. The ovum of the nine-banded armadillo: growth of the ovocytes, maturation and fertilization. Biol. Bull., 23:100-41, 1912.         [ Links ]

NEWMAN, H. H. & PATTERSON, J. T. The development of the nine-banded armadillo from the primitive streak stage to birth; with special reference to the question of specific polyembriony. J. Morph., 21:359-426, 1910.         [ Links ]

ODEND'HAL, S.; WENZEL, J. G. W. & PLAYER, E. C. The rete ovarii of cattle and deer communicates with the uterine tube. Anat. Rec., 216:40-3, 1986.         [ Links ]

PAN AMERICAN HEALTH ORGANIZATION (P. A. H. O.). The armadillo as an experimental model on biomedical research, Scientific Publication 366, Washington, 1978.         [ Links ]

POLINI, N.N.; CAMINA, R. & CASANAVE, E.B. Morphological and Morphometrical study of the blood leucocytes from C. villosus, Mammalia, Dasypodidae. Comp. Haematol. Internat., 9(3): 162-7, 1999.         [ Links ]

PIRLOT, P. Aparatos urinario y genital. In: Morfología evolutiva de los Cordados, pp. 615-81, Barcelona, Omega, 1976.         [ Links ]

RAYNAUD, A. Appareil génital des mammifères placentaires. In: Traité de zoologie. V. 16. Fasc. VI, pp. 453-636, Paris, Masson, 1969.         [ Links ]

REDFORD, K. H. & EISENBERG, J. F. Order Xenarthra (Edentata). In: Mammals of the Neotropics. V. 2. The Southern Cone, pp. 46-68, Chicago, The University of Chicago Press, 1992.         [ Links ]

ROSS, M. H.; ROMRELL, L. J. & KAYE, G. Y. Aparato Genital Femenino. In: Histología. Texto y Atlas Color, pp. 674-737, México, Panamericana, 1997.         [ Links ]

ROWELL, J. E.; BETTERIDGE, K. J.; RANDALL, G. C. B. & FENWICK, J. C. Anatomy of the reproductive tract of the female muskoxen (Ovibos moschatus). J. Reprod. Fert., 80:431-44, 1987.         [ Links ]

SISSON, S & GROSSMAN, J. D. Organos genitales femeninos. In: Anatomía de los animales domésticos, 4a. ed., p. 586-605, Barcelona, Salvat, 1959.         [ Links ]

STORRS, E. E.; BURCHFIELD, H. P. & BINFORD, C. Leprosy in the armadillo: New model for biomedical research. Science, 183:851-2, 1974.         [ Links ]

SWARTZ, W. J. & CORKERN, M. Effects of methoxychlor treatment of pregnant mice on female off spring of the treated and subsequent pregnancies. Reprod. Toxicol., 6:431-7, 1992.         [ Links ]

TAKADA, S.; SHIMADA, T.; NAKAMURA, M.; MORI, H. & KIGAWA, T. Vascular pattern of the mammalian ovary with special referrence to the three-dimensional architecture of the spiral artery. Arch. Histol. Jap., 50:407-18, 1987.         [ Links ]

TAKEVA, T. H. & MIHAILOVA, K. N. Electron microscopic investigation of rete ovarii in the oestral cycle of the guinea pig. C.R. Acad. Bulg. Sci., 39:145-8, 1986.         [ Links ]

TALMAGE, R. V. & BUCHANAN, G. D. The armadillo Dasypus novemcinctus. A review of its natural history, ecology, anatomy and reproductive physiology. Rice Inst. Pamph., 41:1-135, 1954.         [ Links ]

TEDMAN, R. A. The female reproductive tract of the australian sea lion, Neophoca cinerea (Carnivora: Otariidae). Aust. J. Zool., 39:351-72, 1991.         [ Links ]

THEURING, F. & HANSMANN, Y. Follicular development in immature djungarian hamsters (Phodopus sungorus) and the influence of exogenous gonadotropins. Biol. Reprod., 35:407-12, 1986.         [ Links ]