2) General Gestational Data

The total length of gestation is 15-16 months (including the period of delayed implantation) with singletons the rule. This delay of implantation is about 4-5 months long. There is one record of a set of twins, but the article was not available to me (Nikulin, 1954), and Hayssen et al. (1993) make reference to rare other twin gestations in Russian observations. Hybrids with other species are unknown. General data on pinniped reproduction, including walrus, may be found in the chapter by Costa & Crocker (1998).

3) Implantation

There are no publications of implantation, and Mossman (1987) described only one zonary placenta that he had observed superficially; he found it to be zonary.

4) General Characterization of the Placenta

The placenta of this term pregnancy was kindly made available by Dr. Judy St. Leger of Sea World, San Diego. It comes from a multigravida that had gained 800 lbs. during gestation and that was initially very protective of the newborn calf, but eventually the newborn had to be hand-raised. The placenta had remained in sea water for over a day but was cooled and thus in an excellent macroscopic condition. There was minimal autolysis, thus histology was also satisfactory but inadequate for electronmicroscopy. Ordinarily, the placenta is eaten by gulls, according to Hayssen et al. (1993).

This is a typical zonary placenta weighing 5,900 g and measuring 85 cm in greatest length. The "ring" of placental tissue was 25 cm wide. It was complete and the circle was 100 cm in circumference. The villous tissue was 2-2.3 cm thick and darkly congested. At the sides there was the characteristic, irregular, brownish old hematoma, the so-called hemophagous organ. The maternal surface had much fresh clot attached and was irregular on its yellowish surface. There were no subdivisions of the placental tissues. The fetal surface was smooth although a focus of white, nodular squamous metaplasia of amnion was found (5x2 cm). The umbilical cord was mostly absent and less than 10 cm remained.

Another placenta was kindly made available by Dr. Carlos Rodriguez of the New York Aquarium. It weighed 4,980 g, had a similar zonary shape and the same ‘hemophagous’ peripheral region.

A third placenta, coming from a stillborn calf, was made available by Diana Procter (Vallejo, CA). It weighed 6,700 g, its cord was 36 cm long, 4.5 cm in circumference and 2.6 cm in diameter.

5) Details of fetal/maternal barrier

The walrus placenta, like that of other pinnipeds, is labyrinthine and much resembles in its structure that of other carnivores, like the cat. The marginal "hematoma" is also brown, rather than green as in the dog. I did not find regions of active bleeding nor was there the central "hematoma" described by others for seal placentas. There are, however, different regions that can be identified grossly, but better microscopically, when inspecting the cross-sectioned organ. The largest portion is the labyrinth which, in my material, was very much congested. On top of the labyrinth of course is the chorioallantoic mesenchyme (the chorionic plate with fetal vessels). The base of the delivered placenta had some of the so-called "spongy layer" attached but it lacked most of the maternal endometrial glands that otherwise make up much of this zone. The base had debris, small bits of endometrial glands surrounded by syncytium, fibrin and fresh blood. Although decidua exists, little comes away with the delivered organ. At the base of the labyrinth there are irregular collections of syncytiotrophoblast, the much darker cells in the photographs shown below. The deep red color of the labyrinth of the walrus placenta shown here is from the presence of enormously dilated maternal blood channels. They are lined by endothelium and covered on the outside by trophoblast. This is thus an endotheliochorial organ.

The trophoblast at the base is mostly syncytial in nature and the quite inapparent cytotrophoblast in the labyrinth appears to give rise to the syncytium. The syncytium is superficially invasive into the endometrium, destroys some of the stroma and opens some glands, but it does not grow into the maternal vascular lumens or into their walls.

The other placentas available all had the same microscopic appearance. The colored material at the edges was crystalline (square crystals) and iron stain negative.

6) Umbilical cord

The normal length of the umbilical cord is unknown until the other two specimens were available. This specimen lacked most of its cord and one vein had already split off from its cross section near the placental surface. Normally it probably contains two arteries, two veins and a large allantoic duct. Numerous small blood vessels are also present that become more numerous near the placental surface where they spread over the allantoic sac. There were no nodules on the remains of this cord's amnionic surface. The umbilical cord of the New York specimen was between 45 and 50 cm long and that from Vallejo measured 36 cm in length, 4.5 cm in circumference and was 2.6 cm wide.

7) Uteroplacental circulation

This has not been described and could not be observed in this placenta other than the visualization of endometrial arteries entering the labyrinth. They are large channels and send blood to the undersurface of the chorion whence the blood is returned through the labyrinthine channels.

8) Extraplacental membranes

The amnion is lined by a single layer of cuboidal epithelium and has one larger area of squamous inclusions. It contains no blood vessels. The large allantois has a diffuse capillary vasculature and is lined by cuboidal to columnar epithelium. Yolk sac remnants were not found in this term placenta.

9) Trophoblast external to barrier

The trophoblastic invasion of the decidua is very superficial and, in the absence of a uterus with implanted placenta, no statement can be made about deeper trophoblast invasion. This is absent, however, in other pinnipeds and, since the larger endometrial vessels are not invaded (see pictures above), it is unlikely that deeper penetration of trophoblast occurs in walrus.

10) Endometrium

Walruses have a bicornuate uterus. The glands of the endometrium were partially destroyed in this term placenta but their bases remained. They did not contain any obvious secretion. True decidual transformation cannot be seen in the endometrial stroma.

11) Various features

As many other carnivora, at the margin of this zonary placenta one finds the "hemophagous zone", a border composed of degenerating villi, fibrin and remnants of probable hematomas. In contrast to the dog, it is not green but brown/yellow and laminated, much like that seen in the cat, as was also remarked by Amoroso (1961) for related pinnipeds. Yellow pigment occurs here and a few other areas of the placenta which has frequently a crystalline form. The crystals are highly birefractory in polarized light (unlike hemosiderin) and have a box-like shape. They do not stain for iron with Prussian blue stains. Beneath the chorion the more columnar trophoblast contains many crystals.

12) Endocrinology

I am not aware that any publications on the endocrine performance of pregnant walruses exist. A general survey of the reproductive physiology, including some general aspects of endocrine performance of pinnipeds, is found in Costa & Crocker (1998).

13) Genetics

Pinnipedia have either 32 or 34 chromosomes; the Walruses have 32 chromosomes with one metacentric pair having typical secondary constrictions (Fay et al., 1967; Arnason, 1974a; Hsu & Benirschke, 1977; Arnason, 1977; Arnason, 1981). The monophyletic origin of pinnipeds was affirmed by Arnason's study (1974b). The NF of pinnipeds is 64. A characteristic secondary constriction of a pair metacentrics and the very small Y chromosome are typical.

14) Immunology

I know of no publications on the immunology of walruses.

15) Pathological features

Various surveys for antibodies have been conducted in walruses and other pinnipeds. Calle et al. (2002) found no antibodies against Brucella sp. in the Pacific walrus, 3 of 40 had antibodies against Leptospira interrogans, but phocine distemper was not detected. A variety of other antibodies existed (against calicivirus, vesicular exanthema, and various subtypes of influenza A). Nielsen et al. (2000) detected antibodies against morbillivirus in 50 of Atlantic walruses and, in 2001, identified antibodies to Brucella but they were unable to identify the organism. Although Zarnke et al. (1997) identified antibodies to phocid herpesviruses, they were of the opinion that herpes infection was not a cause of mortality. Antibodies against caliciviruses were detected in Pacific walruses by Barlough et al. (1986) who had also earlier identified the virus.

Trichinella infection is common in walrus and it is a source of infection to the Inuits (Proulx et al., 2002). Brucellosis of sea mammals was studied by Foster et al. (2002) who separated the responsible organism of terrestrial animals from those in sea mammals (Brucella cetaceae & B. pinnipedia). A listing of parasites found in walruses was provided by Dailey & Brownell (1972).

Myocardial infarction and widespread atherosclerosis was the cause of death in a 25 year-old walrus reported by Gruber et al. (2002).

Cornell et al. (1975) described an unusual complication of neonatal life, the persistence of a tight fibrous band expanding from the dome of the bladder to the umbilicus that prevented complete emptying of the bladder. The about one month-old, 69 kg walrus had been hand-reared and developed pyelonephritis and hydronephrosis from this complication and died. It also had ascites and intestinal torsion.

16) Physiologic data

No physiological studies on placenta or uterine perfusion have been undertaken on walrus implantations. There is, however, an excellent consideration of the development of the (probably similar) endotheliochorial placentation in mink (Pfarrer et al., 1999). It described the development of the maternal sinusoids from endometrial capillaries through the invasive action of the syncytiotrophoblast in three developmental stages. Histologic studies and corrosion casts were employed and these authors provided an excellent overview of the features of placental perfusion in endotheliochorial placentas.

17) Other resources

To the best of my knowledge, the only cell lines available are those of Dr. U. Anderson at the University of Lund, Sweden.

18) Other remarks - What additional Information is needed?

No implantational study has been undertaken and the length of the umbilical cord needs to be ascertained. Endocrine studies are completely lacking.

Acknowledgement

The animal photograph in this chapter was kindly supplied by Dr. Sam Ridgway. I very much appreciate the help of Dr. Judy St. Leger of Sea World, San Diego for allowing me to study this placenta. Dr. Carlos Rodriguez, New York Wildlife Conservation Society kindly made the second placenta available. I also wish to acknowledge the constant help of the histopathologists at UCSD Medical Center in preparing the slides.

References

Amoroso, E.C.: Placentation. Chapter 15, pp.127-311, In, Marshall's Physiology of Reproduction, V.II, A.S. Parkes, ed. Second Edition. Little, Brown & Co. Boston, 1961.

Andersen, L.W., Born, E.W., Gjertz, I., Wiig, O., Holm, L.E. and Bendixen, C.: Population structure and gene flow of the Atlantic walrus (Odobenus rosmarus rosmarus) in the eastern Arctic based on mitochondrial DNA and microsatellite variation. Mol. Evol. 7:1323-1336, 1998.

Arnason, U.: Comparative chromosome studies in Pinnipedia. Hereditas 76:179-225, 1974a.

Arnason, U.: Phylogeny and speciation in Pinnipedia and Cetacea - a cytogenetic study. Thesis, Lund, 1974b.

Arnason, U.: The relationship between the four principal pinniped karyotypes. Hereditas 87:227-242, 1977.

Arnason, U.: Localization of nucleolar organizing regions in pinniped karyotypes. Hereditas 94:29-34, 1981.

Barlough, J.E., Berry, E.S., Skilling, D.E., Smith, A.W. and Fay, F.H.: Antibodies to marine caliciviruses in the Pacific walrus (Odobenus rosmarus divergens Illiger) J. Wildl. Dis. 22:165-168, 1986.

Calle, P.P., Seagars, D.J., McClave, C., Senne, D., House, C. and House, J.A.: Viral and bacterial serology of free-ranging Pacific walrus. J. Wildl. Dis. 38:93-100, 2002.

Cornell, L.H., Golden, B.J. and Osborn, K.G.: Pseudopersistent urachus in a baby walrus. J. Amer. Vet. Med. Ass. 167:548-549, 1975.

Costa, D.P. and Crocker, D.E.: Seals. Pp. 313-321, in Encyclopedia of Reproduction, Vol. 4, E. Knobil and J.D. Neill, eds. Academic Press, San Diego, 1998.

Dailey, M.D. and Brownell, R.L., Jr.: A checklist of marine mammal parasites. Chapter 9, pp. 528-589, in Mammals of the Sea. Biology and Medicine. S.H. Ridgway, ed. Charles C. Thomas, Springfield, Illinois, 1972.

Duffield Kulu, D.: Evolution and cytogenetics. Chapter 8, pp. 503-527, in Mammals of the Sea. Biology and Medicine. S.H. Ridgway, ed. Charles C. Thomas, Springfield, Illinois, 1972.

Fay, F.H., Rausch, V.R. and Feltz, E.T.: Cytogenetic comparison of some pinnipeds (Mammalia: Eutheria). Canad. J. Zool. 45:773-778, 1967.

Foster, G., MacMillan, A.P., Godfroid, J., Howie, F., Ross, H.M., Cloeckaert, A., Reid, R.J., Brew, S. and Patterson, I.A.: A review of Brucella sp. infection of sea mammals with particular emphasis on isolates from Scotland. Vet. Microbiol. 90:563-580, 2002.

Gotch, A.F.: Mammals - Their Latin Names Explained. Blandford Press, Poole, Dorset, 1979.

Gruber, A.D., Peters, M., Knieriem, A. and Wohlsein, P.: Atherosclerosis with multifocal myocardial infarction in a Pacific walrus (Odobenus rosmarus divergens Illiger). J. Zoo Wildl. Med. 33:139-144, 2002.

Hayssen, V., van Tienhoven, A. and van Tienhoven, A.: Asdell's Patterns of Mammalian Reproduction: a Compendium of Species-specific Data. Comstock/Cornell University Press, Ithaca, 1993.

Hsu, T.C. and Benirschke, K.: An Atlas of Mammalian Chromosomes. Vol. 10, Folio 495, 1977.

Ledje, C. and Arnason, U.: Phylogenetic relationships within caniform carnivores based on analyses of the mitochondrial 12S rRNA gene. J. Mol. Evol. 43:641-649, 1006.

Mossman, H.W.: Vertebrate Fetal Membranes. MacMillan, Houndmills, 1987.

Nielsen, O., Stewart, R.E., Measures, L., Duignan, P. and House, C.: A morbillivirus antibody survey of Atlantic walrus, narwhal and beluga in Canada. J. Wildl. Dis. 36:508-517, 2000.

Nielsen, O., Stewart, R.E., Nielsen, K., Measures, L. and Duignan, P.: Serologic survey of Brucella spp. antibodies in some marine mammals of North America. J. Wildl. Dis. 37:89-100, 2001.

Nikulin, P.G.: On twinning in Chukchi walruses. Pacific Research Institute of Fisheries and Oceanography (TNIRO). Izvestia 39:353, 1954.

Nishiwaki, M.: General Biology. Pp. 162-164, in: Mammals of the Sea. Biology and Medicine. S.H. Ridgway, ed. Charles C. Thomas, Springfield, Illinois, 1972.

Nowak, R.M.: Walker's Mammals of the World. 6th ed. The Johns Hopkins Press, Baltimore, 1999.

O'Brien, S.J., Menotti-Raymond, M., Murphy, W.J., Nash, W.G., Wienberg, J., Stanyon, R., Copeland, N.G., Jenkins, N.A., Womack, J.E. and Graves, J.A.: The promise of comparative genomics in mammals. Science 286:458-481, 1999.

Pfarrer, C., Winther, H., Leiser, R. and Dantzer, V.: The development of the endotheliochorial mink placenta: light microscopy and scanning electron microscopical morphometry of maternal vascular casts. Anat. Embryol. 199:63-74, 1999.

Proulx, J.F., MacLean, J.D., Gyorkos, T.W., Leclair, D., Richter, A.K., Serbir, B., Forbes, L. and Gajadhar, A.A.: Novel prevention program for trichinellosis in inuit communities. Clin. Infect. Dis. 34:1508-1514, 2002.

Zarnke, R.L., Harder, T.C., Vos, H.W., VerHof, J.M. and Oosterhaus, A.D.: Serologic survey for phocid herpesvirus-1 and -2 in marine mammals from Alaska and Russia. J. Wildl. Dis. 33:459-465, 1997.