Morphological characteristics of the neonate of the white-eared opossum (Didelphis albiventris Lund, 1840) (Metatheria: Didelphidae)

Bruno Machado Bertasoli, Amilton Cesar dos Santos, Thais Borges Lessa, Iria Gabriela Dias dos Santos, Aline Gonçalves Lio Copola, Celina de Almeida Furlanetto Mançanares, Gerluza Aparecida Borges da Silva and Erika Cristina Jorge

Abstract
Due its post-birth distinction from other mammals, and the absence of detailed work on the morphology of the marsupial neonates, and their respective organogenic development, the objective of this study was to provide macroscopic and microscopic detailed descriptions of the white-eared opossum (Didelphis albiventris Lund, 1840) neonates and a potential comparison to embryos/fetuses from other mammalian species described in the literature. For this study, we used 5 D. albiventris neonates of four days old. For macroscopic analysis, samples were fixed and photographed, and for microscopic analysis, specimens were processed by routine histology techniques and stained with hematoxylin and eosin. Neonates presented some embryological characteristics, such as pronounced facial immaturity, presence of optic vesicle, gap on the fourth brain, brain vesicles, and underdeveloped lungs and mesonephros. However, they also presented well-developed structures, such as apparent nasal and oral cavities and well-developed pelvic and thoracic limbs, especially the hands, where it was possible to find claws at the ends of the digits. Due to the ease of access to D. albiventris neonates, the early development state after birth and not sacrifice of the mother for neonate collected, this species can be considered an excellent model for comparative developmental studies. These results can be extrapolated and compared to morphogenesis of rats, guinea pigs, rabbits, horses, cattle and humans at different stages of development, regardless of the length of the gestation period, considering the particularities of each species.

Keywords
White-eared opossum, Didelphimorphia, Embryology, Histology, Marsupial.

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References
Abreu, D. K.; Rodrigues, E. A. F.; Monteiro, J. M.; Franciolli, A. L. R.; Costola-Souza, C.; Roballo, K. C. S.; Ambrósio, C. E.; Miglino, M. A. Estudo microscópico e macroscópico, com enfoque radiográfico e de alizarina, no desenvolvimento embrionário e fetal de gatos domésticos (Felis catus) em diferentes idades gestacionais. Pesq. Vet. Bras., v. 31, p. 31-57, 2011.

Barros, M. A.; Martins, J. F. P.; Samoto, V. Y.; Oliveira, V. C.; Gonçalves, N.; Mançanares, C. A. F.; Vidane, A.; Carvalho, A. F.; Ambrosio, C. E.; Miglino, M. A. Marsupial morphology of reproduction: South America opossum male model. Micros. Res. Tec., v. 76, p. 388-397, 2013.

Beaudoin, S.; Barbet, P.; Bargy, F. Developmental stages in the rabbit embryo: guidelines to hoose an appropriate experimental model. F. Diag. Ther., v. 18, p. 422-427, 2003.

Bertassoli, B. M.; Santos, A. C.; Oliveira, F. D.; Oliveira, D. M.; Assis-Neto, A. C.; Carvalho, A. F. Morphology of the trachea and larynx of the opossums (Didelphis sp.). Ciência An. Bras., v. 14, n. 2, p. 222-229, 2013.

Bertassoli, B. M.; Santos, A. C.; Will, S. E. A. L.; Fratini, P.; Assis-Neto, A. C. Morphological analysis of the extraembryonic membranes of domestic pig (Sus scrofa) at 20 days of gestation. J. Bas. Appl. Res. Inter., v. 10, n. 1, 2015.

Evans, H. E.; Sack, W. O. Prenatal development of domestic and laboratory mammals: growth curves, external features and selected references. Anat. Histol. Embr., v. 2, p. 11-45, 1973.

Felipe, A. E.; Masson, P. G.; Rodríguez, J. A.; Alzola, R. H. External morphological characterization of 60-days gestation Myocastor coypus (Coipu) fetuses. Int. J. Morph., v. 1, p. 71-76, 2006.

Franciolli, A. L. R.; Cordeiro, B. M.; Fonseca, E. T.; Rodrigues, M. N.; Sarmento, C. A.; Carvalho, A. F.; Miglino, M. A.; Silva, L. A. Characteristics of the equine embryo and fetuses from days 15 to 107 of pregnancy. Theriogenology, v. 76, p. 819-832, 2011.

Frappell, P. B.; MacFarlane, P. M. Development of the Respiratory System in marsupials. Resp. Physiol. Neurobiol., v. 154, p. 252-267, 2006.

Gonçalves, N. M., Maçanares, C. A. F.; Miglino, M. A.; Samoto, V. Y.; Martins, D. S.; Ambrósio, C. E.; Ferraz, R. H. S.; Carvalho, A. F. Aspectos morfológicos dos órgãos genitais femininos do gambá (Didelphis sp.). Brazilian J. Vet. Res. Ani. Sci., v. 46, p. 332-338, 2009.

Goswami, A.; Weisbecker, V.; Sanchez-Villagra, M. R. Developmental modularity and the marsupial-placental dichotomy. J. Exp. Zool., v. 312, p. 186-195, 2009.

Hildebrand, M. Análise da estrutura dos vertebrados. São Paulo: Atheneu, 1995.

Holz, P. Marsupialia (Marsupials). In: Fowler, M. E.; Miller, R. E. (Eds.). Zoo and wild animal medicine. 5. ed. Missouri: Elsevier, 2003. p. 288-303.

Illanes, J.; Orellana, C.; Fertilio, B.; Leyton, V.; Venegas, F. Análisis macroscópico y microscópico del desarrollo embrionario y fetal en el gato (Felis catus), en relación con el desarrollo de la vesícula coriónica y de la placenta. Int. J. Morph., v. 25, p. 467-481, 2007.

Kraus, D. B.; Fadem, B. H. Reproduction, development and physiology of the gray short-tailed opossum (Monodelphis domestica). Lab. Anim. Sci., v. 37, p. 478-482, 1987.

Krause, W. J. Scanning electron microscopic study of the opossum nasal cavity prior to and shortly after birth. Anat. Embryol., v. 185, p. 281-289, 1992.

Krause, W. J.; Cutts, H.; Leson, C. R. Morphological observations on the mesonephros in the postnatal opossum, Dideplhis virginiana. J. Anat., v. 129, n. 2, p. 377-397, 1979.

Malta, M. C. C.; Luppi, M. M. Marsupialia - Didelmorphia (Gambá, Cuíca). In: Cubas, Z. S.; Silva, J. C. R.; Catão-Dias, J. L. (Eds.). Tratado de animais selvagens. São Paulo: Roca, 2007. p. 340-357.

Moore, K. L.; Persaud, T. V. N. (Eds). Embriologia clínica. 7. ed. São Paulo: Elsevier, 2004.

New, D. A. T.; Mizell, M.; Cockroft, D. L. Growth of opossum embryos I vitro during organogenesis. J. Embryol. Exp. Morphol., v. 41, p. 111-123, 1977.

Nogueira, J, C. Reprodução do gambá. Ciência Hoje, v. 3, p. 57-60, 1989.

Paglia, A. P.; Fonseca, A. B. G.; Rylands, A. B.; Herrmann, G.; Aguiar, L. S. M.; Chiarello, A. G.; Leite, Y. L. R.; Costa, L. P.; Siciliano, S.; Kierulff, M. C. M.; Mendes, S. L.; Tavares, V. C.; Mittermeier, R. A.; Patton J. L. Annotated checklist of Brazilian mammals. 2. ed. Arlington, VA: Conservation International, 2012. (Occasional Papers in Conservation Biology).

Reis, N. R.; Peracchi, A. L.; Pedro, W. A.; Lima, I. P. (Eds.). Mamíferos do Brasil. Londrina: Universidade Estadual de Londrina, 2006.

Sadler, T. W. L. Embriologia médica. 9. ed. Rio de Janeiro: Guanabara Koogan, 2004.

Theiler, K. The House Mouse: Development and normal stages from fertilization to 4 weeks of age. Springer Verlag, 1972.

Tolosa, E. M. C.; Rodrigues, C. J; Behmer, O.; Freitas Neto, A. G. Manual de técnicas para histologia normal e patológica. 2. ed. São Paulo: Manole, 2003.

Vidal, R. X. Uma breve revisão sobre alguns aspectos do desenvolvimento embrionário do coração com especial referência às artérias coronárias. Arq. Bras. Card., v. 68, p. 305-309, 1997.

Wolpert, L.; Beddington, R.; Brockes, J.; Jessell, P. L.; Meyerowitz, E. Biologia do desenvolvimento. 1. ed. Porto Alegre: Artes Médicas Sul, 2000.

Zeller, U. Mammalian reproduction: origin and evolutionary transformations. Zoologischer Anzeiger., v. 238, p. 117-130, 1999.