Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Placentation in the Amazonian manatee (Trichechus inunguis)

A. M. Carter A , M. A. Miglino B F , C. E. Ambrosio B , T. C. Santos B , F. C. W. Rosas C , J. A. d’Affonseca Neto C , S. M. Lazzarini D , A. F. Carvalho E and V. M. F. da Silva C
+ Author Affiliations
- Author Affiliations

A University of Southern Denmark, J. B. Winsloewsvej 21, DK 5000 Odense, Denmark.

B University of Sao Paulo, Faculty of Veterinary Medicine and Animal Science, Av. Prof. Dr. Orlando Marques de Paiva 87, Cidade Universitária, 05580-270 Sao Paulo, SP, Brazil.

C National Institute of Amazonian Research, Av. André Araújo, 2936, 69083-000 Manaus, AM, Brazil.

D Centre of Protection and Research of Aquatic Mammals, Rodovia Manaus-Caracarai Km 122, Balbina, 69736-000 Presindente Figueiredo, AM, Brazil.

E School of Veterinary Medicine, Av. Octávio Bastos, Nova São João, 13870-040 Sao João da Boa Vista, SP, Brazil.

F Corresponding author. Email: miglino@usp.br

Reproduction, Fertility and Development 20(4) 537-545 https://doi.org/10.1071/RD08009
Submitted: 18 January 2008  Accepted: 4 March 2008   Published: 11 April 2008

Abstract

Evidence from several sources supports a close phylogenetic relationship between elephants and sirenians. To explore whether this was reflected in similar placentation, we examined eight delivered placentae from the Amazonian manatee using light microscopy and immunohistochemistry. In addition, the fetal placental circulation was described by scanning electron microscopy of vessel casts. The manatee placenta was zonary and endotheliochorial, like that of the elephant. The interhaemal barrier comprised maternal endothelium, cytotrophoblasts and fetal endothelium. We found columnar trophoblast beneath the chorionic plate and lining lacunae in this region, but there was no trace in the term placenta of haemophagous activity. The gross anatomy of the cord and fetal membranes was consistent with previous descriptions and included a four-chambered allantoic sac, as also found in the elephant and other afrotherians. Connective tissue septae descended from the chorionic plate and carried blood vessels to the labyrinth, where they gave rise to a dense capillary network. This appeared to drain into shorter vessels near the chorionic plate. The maternal vasculature could not be examined in the same detail, but maternal capillaries ran rather straight and roughly parallel to the fetal ones. Overall, there is a close resemblance in placentation between the manatee and the elephant.

Additional keywords: Afrotheria, haemophagous organ, phylogeny, Sirenia.


Acknowledgements

These studies were supported by The Carlsberg Foundation, Denmark (A.M.C.), Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP; M.A.M.) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; M.A.M. and V.M.F.S.). The authors are very grateful to Dr Allen C. Enders for his valuable input on the interpretation of the fine structure of the placenta. The authors thank the team of INPA and CPPMA for their dedicated work with the captive manatees.


References

Allen, W. R. (2006). Ovulation, pregnancy, placentation and husbandry in the African elephant (Loxodonta africana). Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 821–834.
Crossref | GoogleScholarGoogle Scholar | PubMed | Gheerbrant E., Domning D. P., and Tassy P. (2005). Paenungulata (Sirenia, Proboscidea, Hyracoidea and relatives). In ‘The Rise of Placental Mammals: Origins and Relationships of the Major Extant Clades’. (Eds K. D. Rose and J. D. Archibald.) pp. 84–105. (Johns Hopkins University Press: Baltimore.)

Hodde, K. C. , Miodonski, A. , Bakker, C. , and Veltman, W. (1977). Scanning electron microscopy of microcorrosion casts with special attention on arteriovenous differences and application to the rat’s cochlea. Scan. Electron Microsc. 2, 477–484.
Husar S. L. (1978). ‘Trichechus manatus. Mammalian Species No. 93.’ (The American Society of Mammalogists: Lawrence, KS.)

International Union for Conservation of Nature and Natural Resources (2007). 2007 IUCN Red List of Threatened Species. Available at http://www.iucnredlist.org [Verified 9 January 2008].

Kellogg, M. E. , Burkett, S. , Dennis, T. R. , Stone, G. , Gray, B. A. , McGuire, P. M. , Zori, R. T. , and Stanyon, R. (2007). Chromosome painting in the manatee supports Afrotheria and Paenungulata. BMC Evol. Biol. 7, 6.
Crossref | GoogleScholarGoogle Scholar | PubMed | Mossman H. W. (1987). ‘Vertebrate Fetal Membranes: Comparative Ontogeny and Morphology; Evolution; Phylogenetic Significance; Basic Functions; Research Opportunities.’ (Macmillan: Houndsmills, Basingstoke, Hampshire and London.)

Oduor-Okelo, D. , Musewe, V. O. , and Gombe, S. (1983). Electron microscopic study of the chorioallantoic placenta of the rock hyrax (Heterohyrax brucei). J. Reprod. Fertil. 68, 311–316.
PubMed | Shoshani J. (2005). Order Sirenia. In ‘Mammal Species of the World: A Taxonomic and Geographic Reference’. (Eds D. E. Wilson and D.M. Reeder.) pp. 92–93. (Johns Hopkins University Press: Baltimore.)

Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85, 1–350.
Springer M. S., Murphy W. J., Eizirik E., and O’Brien S. J. (2005). Molecular evidence for major placental clades. In ‘The Rise of Placental Mammals: Origins and Relationships of the Major Extant Clades’. (Eds K. D. Rose and J. D. Archibald.) pp. 37–49. (Johns Hopkins University Press: Baltimore.)

Stanhope, M. J. , Waddell, V. G. , Madsen, O. , de Jong, W. , Hedges, S. B. , Cleven, G. C. , Kao, D. , and Springer, M. S. (1998). Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proc. Natl Acad. Sci. USA 95, 9967–9972.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Turner, W. (1889). On the placentation of Halicore dugong. Trans. R. Soc. Edinb. 35, 641–662.


Wislocki, G. B. (1935). The placentation of the manatee (Trichechus latorostris). Mem. Mus. Comp. Zool. Harvard Coll. 54, 158–178.


Wooding, F. B. P. , Stewart, F. , Mathias, S. , and Allen, W. R. (2005). Placentation in the African elephant, Loxodonta africana: III. Ultrastructural and functional features of the placenta. Placenta 26, 449–470.
Crossref | GoogleScholarGoogle Scholar | PubMed |