Order: Xenarthra (Edentata)
1) General zoological data of species
The nine bands that characterize this species are made of scutes, modified skin with bone marrow within. They are connected by loose connective tissue. The abdomen is made of a tough skin, with numerous hairs. Armadillos are South American species, and this form extends from Texas to Uruguay/Paraguay. By being insectivorous, it is limited largely by freezing temperatures in the North. Breeding of nine-banded armadillos in captivity has so far not been uniformly achieved. They are, however, prolific in the wild and are easily maintained in captivity. Thus, no captive "colonies" exist; some animals are being held in zoos of course. They are prized food items in many countries and popular armadillo races are commonly held in Texas.
In nature, the nine-banded armadillo extends from Argentina to Texas and it is but one of about 20 species of armadillos. The nine-banded armadillo represents the only armadillo species that immigrated from South America to North America, approximately 2-3 million years ago. In the United States, it is at home in Texas, Louisiana and, more recently, it has been introduced into Florida. The home range in the United States was delineated by Buchanan (1958) and, more recently, by Humphrey (1974). For Florida it was provided by Layne & Glover (1977).
South of Uruguay, a similar species, the somewhat smaller (3,000 g) seven-banded armadillo or mulita (Dasypus hybridus), regularly produces between 8-12+ monozygotic multiple offspring. Both have a uterus simplex, in contrast to most other armadillo species. They have also the same number and appearance of chromosomes and could conceivably be subspecies. There are also many specimens with intermediate numbers of bands (7-9) known. Species delineation of the mulita (Dasypus hybridus) from the similarly seven-banded species Dasypus septemcinctus is discussed at length by Hamlett (1939) without, I feel, having come to a satisfactory answer. It is also of interest that the shells of nine-banded armadillos are larger in the equatorial regions, and half-bands are often seen. Thus, these may all be merely races or incipient species. Broader considerations of Dasypodidae were provided by Frechkop and Yepes (1949) and, of all armadillos, in the old description of Gray (1973). Wetzel and Mondolfi (1979) provided a more measured account of these species.
|Adult nine-banded armadillo from Texas, USA.|
2) General gestational data
Nine-banded armadillos in Texas breed in July, and delayed implantation, with the blastocyst resting in the uterus, lasts for about 3-4 months. Implantation then takes place in November, with birth occurring in March/April. Ramsey (1982) gives the length of gestation as being 120-150 days, but that depends on what times exactly are counted. The adult nine-banded armadillo weighs between 4,000 and 5,000 g, newborns are 100 g.
This remarkable animal is the only known species that always produces monozygotic (identical) multiple offspring. Occasional quintuplets have been witnessed to occur. Quite frequently smaller numbers, such as singletons, twins and triplets have been described as well. Whether these are the result of fetal death is not known. Buchanan (1957) who examined 60 pregnant uteri found two animals with three embryos and no trace of a fourth. One uterus contained six embryos plus an additional amnionic sac. He referred to other records of odd numbers of embryos and later (1967), he described an uterus with a fundal implantation plus a blastocyst in the uterus. From this he inferred that only the fundal, cruciform depression of the uterus is fit to allow implantation of the placenta.
The reason for the unique "polyembryony" in Dasypodidae is not understood. The original assumption, that this was due to delayed implantation (3-4 months), was contradicted by Stockard (1921). While temporary hypoxia had been assumed to be the cause, Stockard suggested that it was an "innate ability" of the armadillo embryo that leads to "budding" of the embryonic disk. Even more prolonged delay in implantation (13-24 months) observed by Storrs et al. (1988) produced no change in the number of offspring. Other variations and the possible reasons for polyembryony are discussed by Galbreath (1985). Enders (2002) has recently addressed the possible mechanism leading to polyembryony in this species and provided a nice historical overview as well. While he laid the anatomical groundwork for explaining that polyembryony can feasibly occur in this species, the reason for embryonic "cloning" in armadillos is yet to be forthcoming.
|Morula of nine-banded armadillo with thick zona pellucida flushed from the Fallopian tube.|
|Uterus in November (USA) with blastocyst lying free within endometrial cavity.|
plate of implanted immature placenta. There is no decidua basalis;
instead, the villi attach to a spongy, vascular trabecular network.
implantation is fundal with segregation of the placental disk by "budding"
into four separate lobes that occurs after implantation. Therefrom develops
a hemochorial placenta that attaches with a peripheral trabecular structure
to the myometrium. Mossman (1987) speaks of this region as "many large
endothelium-lined maternal blood spaces at the base of the placenta, and
the distal portions of fetal villi often extend freely into these spaces.
This arrangement is believed unique to the Dasypodidae but resembles the
hematomes of carnivores". There is no decidua in my experience, although
Mossman (1987) refers to the presence of decidua. The central, fundal location
of the implantation site may be the result of converging endometrial grooves
which Galbreath (1985) then related to the future development of polyembryony.
It is here, where the blastocyst comes to lie and awaits its time for implantation.
In his very detailed description of early implantation of the armadillo and initial placental development, Enders (2002) does not consider that the "restriction" of the fundal fold is a cause of polyembryony. Rather, he suggested that the polyembryony may relate to several other factors. First, there is relative premature development of the placental membranes, as opposed to an expansion of the embryo. Then, with implantation, the abembryonic trophoblast rapidly degenerates and thus it leaves the also rapidly expanding exocoelom to be exposed to the uterine fluid, with potential absorption of glandular secretions. Also, there is an early inversion of yolk sac with subsequent polar atrophy. Enders showed that, initially, two embryos segregate from the embryonic shield, to be followed by a subsequent division, so that, ultimately, four embryos become reasonably uniformly deposited in the embryonic cavity.
The trophoblast is made up of an invasive portion that destroys endometrial glands, and an absorption group that, as Enders infers, must be interpreted as participating in fluid exchange because of its microvillous surface and dilated basal folds. One puzzling aspect of early placenta formation in the armadillo has been difficult to understand because it is so different from that of the best-studied human placenta. That is the origin of the mesothelial cells that form the future villous cores, as these are present long before there is the formation of a body wall and stalk (Enders, 2002). Perhaps cytogenetic or genetic studies can address this in the future.
The development of a large exocoelom is particularly striking, as is the peculiar arrangement of the amnion. There is only one amnionic cavity and, when the first two embryos form, the two amnions are connected by a tube (seen on gross pictures below) that constricts, focally, the amnionic space. Ultimately these tubal connections between the amnionic sacs of the respective embryos are obliterated.
The placenta is villous, although Mossman (1987) considers it to be trabecular. The trabecular designation clearly derives from the solid peripheral solid strands of tissue shown above. This tissue is essentially the same as that in the giant anteater. I have more fully studied and described this region in the chapter on giant anteater. Both species are thus related in a vague way through this similarity in an unusual placentation. The "trabeculae", so it would appear to be in anteaters, represent peripheral extensions of villi, into which these may expand. They are made of connective tissue centers and plump trophoblast (probably not endothelium) covering them. A single corpus luteum only is always found in one or the other ovary during pregnancy in the nine-banded armadillo.
The placenta is grossly zonary but, individually the separate discs are "discoid" in character. There is a single chorion that carries the fetal blood vessels; but there are four individual amnionic sacs that enclose the fetuses and which are connected (with fluid-filled spaces) in the center of the disks during early stages of placentation.
|Early implantation with four disks. The four amnions are centrally connected.|
|Embryos still within the amnions.|
|Newborns with mother.|
|Implantation of immature placenta on myometrium with villous structure and large, dark masses of cytotrophoblast.|
of immature placenta with villi at left and
spongy, vascular trabecular sinuses at right; amnion above.
General characteristics of placenta
The end effect then is a slightly cotyledonary placenta with zonary shape, hemochorial in nature with a syncytial barrier to the intervillous space. There is no invasion of myometrium by wandering trophoblastic cells. In my opinion, in most places of the implanted armadillo placenta, the endometrium is lacking and the villi abut the myometrial sinusoids (with occasional myometrial trabeculae producing incomplete septa [Enders & Welsh, 1993] have a nice picture of these).
|Cross-section of implanted mature placenta with the sinusoidal, trabecular region below.|
|Third trimester pregnancy that had been injected in utero with India ink (one fetus - second from left) and craniectomy (CNS and pituitary) of left fetus was done weeks earlier. The "zonary" nature of the placenta with near-marginal cord insertions is apparent. The India ink remained confined to the second fetus from left and its placenta. There are very few turns in the normally flat umbilical cords of armadillos. Most cords insert near the margin of the placenta, which is arranged in a linear, girdle-like fashion.|
Details of barrier structure
Initially there is cytotrophoblast from which the overlying syncytium originates. The typical cytotrophoblast degenerates or becomes so much less apparent so that, ultimately, only a thin layer of syncytium covers the villi. Few true "anchoring villi" are produced.
|Higher magnification of immature villi of implanted nine-banded armadillo placenta with cytotrophoblastic columns and numerous mitoses.|
|Note the very thin syncytium over the villi and presence of mitoses and cell columns.|
Normally there are four umbilical vessels, two arteries and two veins and no ducts. The length of the cords has not been measured or published. They are not spiraled. In a large number of umbilical cords studied, some numerical and errors in size of this vasculature were found (Benirschke et al., 1964). They are shown next.
|Cross-sections of umbilical cords with varying numbers of vessels.|
|Distribution of vessels on the placental surface of quadruplets, including the abnormal structured cords. Injection studies have shown that, despite monochorionic placentation, there are no vascular connections among the placental lobes of the quadruplets. They were depicted earlier.|
7) Uteroplacental circulation
The general vasculature of the uterus has not been described in detail. In letters, however, Enders (2002) pointed out to me that, first of all, trophoblast never touches the myometrial stroma but is always separated from the muscle by an endothelial layer of these vascular sinuses. Moreover, he stated that "one of the unusual features that has not been emphasized is that blood returning from the endometrial sinuses passes through a spongework of vessels around the more internal myometrial layers before reaching larger vessels". A normal, term pregnant uterus is here shown with some adjacent vessels.
|Fully distended, term pregnant uterus and ovaries of nine-banded armadillo.|
The trophoblast of the free membranes degenerates soon after implantation. There is no decidua capsularis on the chorion laeve.
Trophoblast external to barrier
|Occasional pregnancies result only in twins, even singletons are seen occasionally for as yet unknown reasons.|
|Nine-banded armadillo with leprosy lesions of abdomen.|
16) Physiological data
Dasypodid species have low body temperatures. Cuba-Caparó determined it to be between 29.5 and 32oC). They are susceptible to cold, perhaps especially so because of the exposed marrow in their scutes.
Armadillos are also highly resistant to hypoxia (Scholander et al., 1943), a faculty that aids in burrowing and crossing streams whilst walking at the river beds. It makes it also difficult to anesthetize the animals with ether. Other, more distantly related species (Chaetophractus villosus) have seemingly similar abilities (Affanni et al., 1987).
Basic chemistry profiles were given by Strozier et al. (1971), and Ebaugh & Benson (1964) determined that red cell survival was only 70-75 days.
17) Other resources
Cell strains are available from the "Frozen Zoo" of the Zoological Society of San Diego. Amborski et al. (1974) described a method for creating cell lines. Arruda & Opromolla (1981) presented directions of how to care for armadillos in captivity, while Meritt (1973) gave dietary directions.
Other aspects of interest and other needs for study
|"Mulitas", seven-banded armadillos from Argentina.|
Adamoli, V.C., Cetica, P.D., Merani, M.S. and Solari, A.J.: Comparative morphologic placental types in Dasypodidae (Chaetophractus villosus, Cabassous chacoensis, Tolypeutes matacus and Dasypus hybridus). Biocell 25:17-22, 2001.
Affanni, J.M., Samartino, L.G., Casanave, E.B. and Dezi, R.: Absence of apnea in armadillos covered by soil. Resp. Physiol. 67:239-245, 1987.
Amborski, R.L., LoPiccolo, G. and Amborski, G.F.: Development of an established cell line derived from Dasypus novemcinctus, a laboratory animal susceptible to infection by Mycobacterium leprae. Experientia 30:546-548, 1974.
Anderson, J.M. and Benirschke, K.: Fetal circulations in the placenta of Dasypus novemcinctus, Linn. and their significance in tissue transplantation. Transplantation 1:306, 1963 .
Arruda, O.S. de and Opromolla, D.V.A. Manutença de tatus em cativero (Mammalia, Edentata). Maintenance of armadillos in Captivity (Mammalia, Edentata). Revista Biotérios 1:57-62, 1981.
Barreto, M., Barreto, P. and D'Allessandro, A.: Colombian armadillos: Stomach content and infection with Trypanosoma cruzi. J. Mammal. 66:188-193, 1985.
Beath, M.M. Benirschke, K.. and Brownhill, L.E.: The chromosomes of the nine-banded armadillo, Dasypus novemvinctus). Chromosoma 13:27, 1962.
Benirschke, K., Sullivan, M.M. and Marin-Padilla, M.: Size and number of umbilical vessels. A study of multiple pregnancy in man and armadillo. Obstet. Gynecol. 24:819-834, 1964.
Billingham, R.E. and Neaves, W.: Exchanges of skin-grafting among monozygotic quadruplets in armadillos. J. Exper. Zool. 213:257-260, 1980.
Brinck-Johnsen, T., Benirschke, K. and Brinck-Johnsen, K.: Hormonal steroids in armadillo, Dasypus novemcinctus. 1. Oestriol in pregnancy and its in vitro biosynthesis by the placenta. Acta Endocrinol. 56:675-690, 1967.
G.D., Enders, A.C. and Talmage, R.V.: Implantation in armadillos ovariectomized
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Cell lines from: http://www.sandiegozoo.org/conservation/cres_home.html. Please direct your inquiries to Dr. Oliver Ryder (firstname.lastname@example.org).
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Datta, M.: Study of meiotic chromosomes of the nine-banded armadillo, Dasypus novemcinctus. The Nucleus 12:69, 1969.
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A.C.: The structure of the armadillo blastocyst. J. Anat. 96:39, 1962.
A.C.: Electron microscopic observations on the villous hemochorial placenta
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armadillo. Texas Rep. Biol. Med. 17:323, 1959.
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Galbreath, G.J.: The evolution of monozygotic polyembryony in Dasypus. In, The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas. G.G. Montgomery, ed. Smithsonian Institution Press, Washington, 1985. pp.243-246.
Gray, J.E.: Handlist of Edentates, Thick-skinned and ruminant mammals in the British Museum. Section 2 - Loricata. British Mus., London, pp.11-25, 1873.
Hamlett, G.W.D.: The reproductive cycle in the armadillo. Z. wiss. Zool. A. 141:143, 1932.
Hamlett, G.W.D.: Identity of Dasypus septemcinctus Linnaeus with notes on some related species. J. Mammal. 20:328-336, 1939.
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Lasley, B.L., Czekala, N.M., Nakakura, K.C., Amara, S.G. and Benirschke, K.: Armadillos for studies on delayed implantation, quadruplets, uterus simplex, and fetal adrenal physiology. In, Animal Models for Research on Contraception and Fertility. N.J. Alexander, ed. Harper and Row, Hagerstown, MD 1979. pp. 447-451.
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