Lesser Hedgehog Tenrec (Small Madagascar Hedgehog)
Echinops telfairi
Dalen Agnew & Kurt Benirschke

Order: Insectivora
Family: Tenrecidae

1) General Zoological Data

Wilson & Reeder (1993) listed a number of synonyms, such as E. miwarti, E. nigrescens, and E. pallens) as having been used for this species. This animal from Madagascar is currently under much discussion regarding its evolutionary history; that aspect is discussed extensively by Carter et al. (2004) who supply numerous references. According to the review by Hayssen et al. (1993), these animals are nocturnal and weigh between 110 and 250 g. In their review of the Masoala exhibit in the Zürich Zoo for instance, Bauert et al. (2007) described their original release of 11 tenrecs (Setifer setosus.) From this original stock, 29 young have been produced. There are relatively few other tenrec colonies in zoological gardens, but Künzle (1998) has described a colony that is kept in Munich and he has also provided a relevant web site with extensive information on this species (http://tenrec.lima-city.de/kuenzle.htm). Gathering from that information, this author has clearly the most information about the behavior, breeding, feeding and care of these small mammals. Other colonies are kept in zoos of Frankfurt, Bronx, Washington, Jersey, Topeka and Philadelphia which provided the information in the International Zoo Yearbook 22. There is variable information on the longevity of these animals; Künzle’s oldest animal died at age 11 years but Weigl (2005) cited 19 years for an animal kept in Topeka and Chicago.

Gotch (1979) derived the Latin name for this species’ from the Greek: ekhinos = hedgehog; ops = from opsis = aspect, appearance; and C. Telfair, a zoologist from Mauritius (1777-1833).

	The dam with offspring.

2) General Gestational Data

The gestation from which we received this placenta lasted 71 days. Künzle (1998) gave the average gestational time as 50 to 60 days with 3-4 young (4-9 g) produced once a year; his experience is considerably larger than our single species gestation and thus it is likely to be more reliable. The maternal weight is around 150-180 g.

3) Implantation

The definitive placenta of this species has been described in great detail by Carter et al. (2004). They used gestations with embryos of 25-66 mm lengths, in addition to 13 placentas from term gestations. These placentologists employed H&E histology, cytokeratin staining, as well as detailed electronmicroscopy for their report. Mossman (1987) does not refer to having seen a placenta of this species. Instead, he referred to Strauss (1944) as having studied other tenrecs and finding a characteristic “Blutbeutel” (hemophagous zone) in the placenta. This is also referred to as occurring in the central zone of the placentas (Carter et al., 2004) who indicated that implantation occurs in an antimesometrial position of the bicornuate uterus.

This is a discoid, hemochorial placenta with a sharply defined area of labyrinth and a basal spongious zone. Additionally, there is a peripheral region of ‘paraplacenta’. Then there is a central folded area of ‘hemophagous’ tissue, the “Blutbeutel” described by Strauss (1944). Carter et al. (2004) described that areas of the spongious zone reach focally the myometrium, an observation that is depicted below from our placenta.

4) General Characterization of the Placenta

The specimen comes from the Potter Park Zoo in Lansing, N.Y. and stems from a Cesarean section. The help of Tara Myers Harrison was essential in obtaining the specimen and this is much appreciated. The neonate weighed 11 g and this discoid placenta weighed 1.3 g. The gestational age was approximately 71 days and it was considered to be a term gestation. The placenta measured 1.9 x 1.5 cm and was nearly ovoid.

	Maternal surface after fixation with cord below, and the membranes extending left.
	Fetal surface that allows visualization of the cord insertion.
	Maternal surface of the delivered placenta.

5) Details of the fetal/maternal barrier

This is a hemomonochorial chorioallantoic placenta with ‘paraplacenta’ and a small central hemophagous region. The labyrinth is extremely vascular and the cytokeratin staining by Carter et al. (2004) demonstrated its trophoblast components convincingly. Since they have provided extraordinarily beautiful illustrations, the reader is referred to their contribution for more detailed pictorial evidence and discussion. The trophoblast in these regions was shown to have a microvillous surface. Jones et al. (2007) studied the glycosylation of the trophoblast in this and four other species. They showed that the tenrec has ‘unusually abundant terminal N-acetyl galactosamine’. The spongious zone is sharply delimited from the labyrinth and consists mostly of large cytotrophoblastic cells with sinuses of maternal blood. Occasional multinucleate cells and numerous mitoses were found in this region as well. We were unable to demonstrate any mitotic activity in the labyrinth.

	Complete section of placental disk; the ‘labyrinth’ is pink and the ‘spongious’ region is most peripheral and dark blue.
	Another section through the disk with ‘paraplacenta’ at top right.
	Section through the ‘labyrinthine’ portion of the disk with large fetal vessels entering from the chorionic plate.
	Low power view of the very vascular labyrinth.
	Higher magnification of the labyrinth with larger trophoblastic cells.
	Mitoses in the spongious zone at arrows.

6) Umbilical cord

The umbilical cord inserted slightly eccentrically and had virtually no twists. Its surface was smooth. There are three vessels, one vein and two arteries. In addition, there is marked squamous metaplasia with keratin production in small patches. In this placenta the umbilical cord measured 1.8 cm in length. Unfortunately, the length of the cord is not comprised in the large review by Spatz (1968) on cord lengths of insectivores and primates.

	Cross section of the umbilical cord. Vein at right; arrow denotes squamous metaplasia.

7) Uteroplacental circulation

In their extensive paper on the tenrec placenta, Carter et al. (2004) also included a detailed consideration of the maternal blood flow. They found trophoblastic infiltration of the endometrial arteries, but not of the veins. This arteriolar vascular wall is replaced by trophoblast and, as the vessels enter the labyrinth, they expand in size and ultimately reach the fetal surface, the blood being returned in a more irregular fashion to the maternal endometrial veins.

	Maternal vessel (MV) in the spongious zone as it enters the labyrinth.
	Endometrial arteriole replaced with invading trophoblast.
	Larger fetal vessels from the chorionic plate enter the labyrinth.

8) Extraplacental membranes

There is no decidua capsularis. The amnion has a single layer of flat squamous cells. No remnants of vitelline tissue were recognized in this term placenta although Mossman (1987) recorded it for the Tenrecidae in general. We could not delineate the allantoic sac because of the disruption of the membranes. Its epithelium is cuboidal to columnar.

	Section through the membranes.

9) Trophoblast external to barrier

There is a significant infiltration of the superficial endometrium and, most importantly, of its arterioles. These vessels are progressing intraluminally as well as intramurally. We have not seen trophoblast in the myometrium underlying the implantation.

	The labyrinthine portion directly beneath the chorionic surface that contains a large fetal vessel.
	This is the spongious zone with a small amount of myometrium at the base.
	Higher magnification of the trophoblast adhering to the myometrium.

10) Endometrium

There is little endometrium remaining at the base of this placenta and it does not have the appearance of any significant decidualization. Moreover, in several places, myometrium adheres to the spongious zone without intervening endometrium. This is also reported by Carter et al. (2004), and while this would connote a placenta accrete in terms of human placentation, this appears to be a normal feature for this animal. There is extensive intermingling of trophoblast with the endometrium; some endometrial glands are still recognizable though.

	Trophoblast in endometrium.

11) Various features

There is a small central so-called hemophagous zone, originally described by Strauss (1944) as “Blutbeutel”. Carter et al. (2004) showed this to be composed of folded allantoic endoderm on one surface and trophoblast on the other, and connective tissue with allantoic vessels interspersed. The trophoblast contains occasion hematoidin crystals but erythrocytophagocytosis was rarely observed. Much degeneration is evident in this term placenta.

In addition, the tenrec has a thin ‘paraplacenta’, a peripheral region of the labyrinth into which allantoic endoderm and mesenchyma extend with some cytotrophoblast.

	Area of the hemophagous zone with adjacent markedly congested labyrinth.
	Hematoidin crystals in the “Blutbeutel”.
	‘Paraplacenta’ at the circumferential edge of the placenta.

12) Endocrinology

No specific information is available, and Mossman & Duke (1973) did not describe the ovaries in this species but studied the related Madagascan species Setifer setosus. It is unknown whether that information is relevant to Echinops. More recently, Enders et al. (2005) described details of the ovaries of this species and a related Nimba Otter Shrew. Remarkably, the deeply furrowed ovaries (similar to European hedgehogs), that are enclosed in a distinct bursa, showed no antral spaces in the developing eggs. Only a thin fluid-filled space was identified; moreover, there was no distinct tunica albuginea. No other endocrine studies are known to us.

13) Genetics

Two different chromosome patterns have been reported by Borgaonkar (1969). In general, the animals have 40 chromosomes (see O’Brien et al., 2006), but some males were reported also as having diminutive Y1 and Y2 chromosomes (2n=41). Fredga (1970) has further discussed the unusual chromosomes of males with this additional chromosome. Hybrids with other species have not been described. The genome of this species is one of 16 mammals whose sequence is scheduled for complete study; initial data have been published in 2005/6. Stanhope et al. (1998) and others have provided molecular evidence suggesting that these animals should be grouped under Afrotheria, an aspect that is further elaborated upon by Carter et al. (2004).

	Karyotype of male with 2n=40 (from O’Brien et al., 2006).

14) Immunology

We are not aware of any immunological studies done in this animal.      

15) Pathological features

Künzle (1998) described a high perinatal and juvenile mortality rate. Mouth abscesses and a mite epidemic are mentioned in his report as causes of mortality.

 
16) Physiologic data

The major interest of the group reporting data by Künzle (1998) is the neurophysiology because this species presents significant challenges in neural development. During the winter, the animals spend their time in ‘torpor’ within the cavities they have prepared. Females are said to produce an odor in the mating season while the males produce a milky substance from periorbital glands (Fahey, 2001). The uterus is bicornuate.

17) Other resources

We are not aware of the existence of cell lines etc.

18) Other remarks – What additional Information is needed?

Detailed endocrine studies and ovarian histology are desirable to be obtained in the future. Also, we know little about the interval from fertilization to implantation.

Acknowledgement

The animal photograph in this chapter comes from Tara Myers Harrison and is much appreciated.

References

Bauert, M.R., Furrer, S.C., Zingg, R. and Steinmetz, H.W.: Three years of experience running the Masoala rainforest ecosystem at Zurich Zoo, Switzerland. Int. Zoo Yb. 41:203-216, 2007.

Borgaonkar, D.S.: Insectivora cytogenetics. pp. 218-246, in Benirschke, K., ed. Comparative Mammalian Cytogenetics. Springer-Verlag, NY 1969.

Carter, A.M., Blankenship, T.N., Künzle, H. and Enders, A.C.: Structure of the definitive placenta of the tenrec, Echinops telfairi. Placenta 25:218-232, 2004.

Enders, A.C., Carter, A.M., Künzle, H. and Vogel, P.: Structure of the ovaries of the Nimba otter shrew, Micropotamogale lamottei, and the Madagascar hedgehog tenrec, Echinops telfairi. Cells, Tissues, Organs. 179:179-191, 2005.

Fahey, B.: “Echinops telfairi” (on-line), Animal Diversity Web.http://animaldiversity.ummz.umich.edu/site/accounts/information/Echinops_telfairi.html.

Fredga, K.: Unusual sex chromosome inheritance in mammals. Phil. Trans. Roy. Soc. London 259B:15-36, 1970.

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Jones, C.J., Carter, A.M., Aplin, J.D. and Enders, A.C.: Glycosylation at the fetomaternal interface in hemomonochorial placentae from five widely separated species of mammal: is there evidence for convergent evolution? Cells Tissues Organs 185:269-284, 2007.

Künzle, H.: Care and breeding of the Madagascan hedgehog tenrec, Echinops telfairi, under laboratory conditions. Der Tierschutzbeauftragte 1/98, 5-12, 2/98 113-115 and reviewed in: http://tenrec.lima-city.de/kuenzle.htm.

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Mossman, H.W. and Duke, K.L.: Comparative Morphology of the Mammalian Ovary. University of Wisconsin Press, Madison, Wisconsin, 1973.

O’Brien, S.J., Menninger, J.C. and Nash, W.G., eds.: Atlas of Mammalian Chromosomes. Wiley-Liss; A. John Wiley & Sons, Inc. Hoboken, N.J., 2006.

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