JOURNAL OF MORPHOLOGY 205233-242 (1990)

Postnatal Development of the Skin of the Marsupial Native Cat Dasyurus hallucatus T. PRALOMKARN, J. NELSON, AND R.T.GEMMELL Department of Anatomy, University of Queensland, St. Lucia, 4067, Queemland, Australia (T.P., R.T.G.);Zoology Department, Monash Uniuersity, Clayton, 3168, Victoria, Australia (J.N.)

ABSTRACT Skin development of the Northern native cat was examined from birth to weaning at 150 days post partum. An outer layer of cells, termed the periderm or epitrichium, is present on the epidermis of the newborn. This layer of cells is not discernible at 7 days post partum. Skin development of the native cat differs from that of the eutherian mammal. The periderm of the eutherian is no longer discernible when the developing hairs first penetrate the epidermis. In the marsupial, this loss of the periderm occurs well before the appearance of follicles. Melanocytes and Langerhans cells are seen a t day 23 post partum, follicles at day 30, sebaceous glands at day 59, and sweat glands at day 67. Thus, when the mother first leaves her young in the nest at about days 60 to 70 of lactation, the skin is at a stage of development that will assist the young with thermoregulation.The skin continues to develop throughout lactation and attains an adult appearance by day 150 post partum. The lamb, rat, and marsupial are all at dif- the marsupial (Krause and Leeson, '73, '75; Gemferent stages of development at birth. The new- mell and Little, '82; Walker and Gemmell, '83; born marsupial is a t a very rudimentary stage of Gemmell, '86; Gemmell and Nelson, '88c). The development compared with the eutherian new- general pattern of ossification in marsupials is born. The maturation of various organ systems similar to that of eutherians except that the long in both eutherians and marsupials follows a sim- bones of the forelimbs and the thoracic verteilar pattern, the main differencesbeing prompted brae have a precocious development compared by the requirement of marsupial young to trans- with those of eutherian mammals. This differfer from the aqueous environment of the uterus ence may be due to the requirement of the marto the aerobic pouch at an early stage of develop- supial forearms for the passage of the young ment. The development of the pituitary and from the cloaca to the pouch. Accelerated rib adrenal gland appears to be advanced in the development also occurs and is possibly related marsupial (Catling and Vinson, '76; Gemmell et to respiratory movements which are initiated at al., '82; Leatherland and Renfree, '83; Walker a very much earlier stage than in eutherian mamand Gemmell, '83; Hall and Hughes, '85; Gem- mals (Gemmell et al., '88b). mell and Nelson, '88a), as these glands are probThere are few studies of skin development in ably required for the initiation of birth. Glands marsupials (Henrikson, '69; Lyne, '70; Lyne et such as the thyroid, which are not essential for al., '70; Krause et al., '78). The development of birth, develop when the young is in the pouch thermoregulation and developmentof endocrine (Setchell, '74; Krause and Cutts, '83; Johnston glands that influence maturation of skin in marand Gemmell, '87). Similarly, touch, olfactory, supials have been reported previously (Gemmell and proprioceptive senses required for migra- and Johnston, '85; Gemmell et al., '87; Johnston tion to the pouch are advanced, whereas those and Gemmell'87). This study will correlate these not essential to birth, including taste, sight, and events with the development of skin in the nahearing, are in an immature form (Hughes and tive cat. The fate of the periderm, a superficial Hall, '84; Jones and Munger, '85; Gemmell et al., layer of cells of the developing epidermis, will be '88a; Gemmell and Nelson, '88b). examined to determine whether this structure In general, organ development is similar in has a role in preventing dessication in the develboth marsupials and eutherians, although some oping marsupial. Comparisonswill also be made differences have been reported. The lung is at an between skin development in the marsupial and earlier stage of development when first used by in the eutherian. D

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By day 7 postpartum, the layers of cells forming the epidermis have increased to approximately 18and the periderm is not discernible. In the developing native cat at 10 days post partum, the epidermis is composed of four layers: a stratum basale; a stratum spinosum composed of approximately eight layers of flattened cells containing fibers; a stratum granulosum with 2 layers of cells containing keratohyalin granules; and a stratum corneum formed by approximately eight layers of fiber-filled cells (Figs. 58). The layers of the epidermis are not easily discernible, and some cells stain more densely MATERIALS AND METHODS than cells from those layers developing previNineteen Northern native cats of either sex, ously or subsequently (Fig. 6). Nevertheless, the aged I, 7,8,9, 10,13,17,20,21,22,23,29,30,45, epidermis starts to show the various layers 50, 59, 67, 81, and 150 days post partum, were present in the mature native cat. used in this study. Pregnant or female native By day 23, the basal cells of the epidermis cats with pouch young were trapped in the wild. have enlarged in volume. Follicle primordia, the The age of the pouch young were known from first signs of hair formation, are then observed their birth date or estimated from growth curves. (Fig. 9). The variation in staining density of the The growth curves, consisting of head and body layers of the spinosum is not so evident (Figs. 10, sizes and body weights, were produced from 11).Dermal melanocytes are first observed at measurements on animals of known age. The day 23 post partum (Fig. 9). Single cells have newborn native cats (day 1)were fixed by immer- been observed in the basal region of the native sion, and the remaining native cats were fixed by cat epidermis at day 10; however, the characterintracardial perfusion with a paraformaldehyde istic granules of the Langerhans cells are not and glutaraldehyde fixative (Gemmell et al., '82). seen until day 23 post partum (Figs. 10, 11). Skin tissue samples were subsequently post Follicles are present by day 30 and the dermis stained in buffered osmium tetroxide, dehy- has obtained a layer of lipid cells. drated, and embedded in Araldite. Sections 1 By day 59 sebaceous glands are observed,and pm thick were stained with Azur A and exam- by day 67 post partum sweat glands are seen. ined with the light microscope.Thin sections (50 The epidermis of the native cat at day 67 posnm) were stained sequentially with uranyl ace- sesses fewer layers (approximately 12) than at tate and lead citrate and examined by means of a day 23 (approximately 18) (Figs. 12, 13) and Zeiss 10 transmission electron microscope. more layers than that at day 150 (approximately 6) (Fig. 15). The epidermis at day 23 has the RESULTS various layers present in adult epidermis, and The dorsal skin of the newborn Northern na- Langerhans cells are observed (Figs.10,ll).Even tive cat is composed of a thin layer of epidermis though the epidermis of the juvenile native cat in close contact with the capillary bed located on on day 150 post partum was 10 pm thick and at an equally thin layer of dermis (Figs. 1,2). The day 67 post partum was 28 pm thick (Figs. 12epidermis is composed of approximately six lay- 15),the dermal thickness increased from 130pm ers of cells. The cytoplasm of the cells of the at day 10 post partum to approximately 280 pm stratum basale are filled with ribosomes. In the at day 150 postpartum. At day 150 hair follicles, stratum granulosum, ribosomes are less preva- sebaceousglands, and sweat glands are observed lent and the cells possess numerous fibrils (Figs. (Fig. 14) and Merkel cells are also present in the 3,4). Dense staining deposits, presumably kera- basal region of the epidermis (Fig. 16). tohyalin, are present in the stratum granulosum DISCUSSION (Fig. 4). The cellular layer distal to the granular layer is filled with fibrils, as are the periderm Skin development in the Australian native cat cells (Fig. 4). The outermost layer of cells of the is similar to that in the American opossum,Didelepidermis is commonly known as the periderrn phis uirginiana (Krause et al., '78). Interestingly, or epitrichium (Figs. 3, 4). The cellular volume these marsupials also have a similar lactation of the periderm cell is increased and the fibrillar period, the native cat having a lactation period of contents have decreased in staining density com- about 125 to 147 days (Nelson and Smith, '71; pared to the penultimate cellular layer of the Begg, '81) and the opossum 100 to 110 days epidermis (Figs. 3,4). (Reynolds,'52).Further, Langerhans cells as well Skin developmentwas examined in the Northern native cat Dasyurus hallucatus, a carnivorous marsupial that is found in the forest and woodlands of northern Australia. The males weigh over 800 gm and the females about 470 gm. The female has a litter of as many as eight after a gestation period of approximately 21 days, each young weighing about 18 mg (Gemmell et al., '88a). The young are carried in a pouch until days 60 to 70 of lactation and the total lactation period is 125to 147 days (Nelson and Smith, '71; Begg, '81).

MARSUPIAL SKIN DEVELOPMENT

Fig. 1. Dasyurus hallucatw. Photograph of the dorsal skin of a newborn specimen. Note that the outer layer of the epidermis consists of the nucleated cells of the periderm (arrow). x 900. Fig. 2. Dasyurus hallucatus. Photograph of skin in a newborn, showing the close proximity between the epidermis (E)andacapillary(C). XW.

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Fig. 3. Dasyurus hallucatus. Electron micrograph of the epidermisof a newborn, illustratingbasal cells (B),a granular layer (G),and periderm (P).~ 4 , 5 0 0 . Fig. 4. Dasyurus hallacatw. Cells of the granular layer (G) of a newborn contain keratohyalin (K). The electrondense cells of the layer between the periderm (P) and the granular layer are filled with fibrils. x 12,500.

Fig. 5. Dasyurus hallacatus. Photograph showing the epidermis at day 10postpartum. The various layersof epidermal cells are flattened and there is no outer periderm. x 540. Fig. 6. Dasyurus hallacatus. Photograph showing the epidermis at day 13 post partum. Note the variation in staining density of the various cellular layers. x 540. Fig. 7. Dusyurus hatlucatus. Electron micrograph of the epidermis at day 10 shows approximately 18 layers of flat-

tened cells, which are distributed in a basal region (B), spiny layer (S), granular layer (G),and a cornified layer (C). x 2,700. Fig. 8. Dasyurus hallucatus. Cells of the spiny layer (S) are thinner than those of the granular layer (G), indicating that the granular cells appear to increasein volume before the transformation into the fully fiber-filledcells of the comified layer (C). ~6,500.

MARSUPIAL SKIN DEVELOPMENT

Fig. 9. Dasyurus hallucatus. Photograph of the skin at day 23 post partum, showing the presence of signs of hair formation. Melanocytes (arrows) are present in the dermis. EP, epithelialplacodes. ~ 9 0 0 .

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Fig. 10. Dasyurus hallacatus. Electron micrograph of the epidermisat day 10 post partum, showing a non-keratinocyte (arrow) in the basal zone. ~6,500. Fig. 11. Dasyum hallacatus. A Langerhans cell (arrow) in the basal zone at day 23 postpartum, showing characteristic Langerhans granules. x 15,600.

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Fig. 12. Dasyum hallucatus. Photograph of the skin at day 67 post partum. Hair follicles (F) with cells of sebaceous glands (arrow) are seen. x 550.

Fig. 13. Dasyurus hallacatw. Electron micrograph of the epidermis at day 67 post partum, showing elongated basal cells (B), spiny cells (S),granular cells (G),and cornified cells (C). Langerhans cells (L) are present in the basal region. x 6,400.

MARSUPIAL SKIN DEVELOPMENT

Fig. 14. Dmyurus hallacatus. Photograph of the skin a t day 150 postpartum. Hair follicles (F),sweat glands (mow), and lipid of adipose cells are present in the relatively thick dermis. x320.

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Fig. 15. Dmyurus hallucatus. Electronmicrographof the

skin at day 150 post partum, showing basal, spiny, granular, and cornified layers of the epidermis. x 6,000.

Fig. 16. Dmyurus hallucatus. Basal region of the epidermis at day 150 post partum, showing a Merkel cell (M) and attendant nerve cell process (N). x 8,000.

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as follicles were observed at day 23 in the native cat and at day 18 in the opossum. These similarities suggest that maturation of the various elements of skin appear to be similar in marsupials that have a similar lactation period. The periderm (also called the epitrichium) is defined as “the superficial transient layer of epithelial cells of the embryonic epidermis.” In eutherians, the periderm is observed prior to the formation of hair follicles and disappears when the hair shafts emerge through the epidermis. The periderm in the sheep is observed at day 33 of gestation and is shed a t the time of emergence of the first hairs at approximately day 115 of gestation (Lyne and Hollis, ’72). In the rat and the mouse the periderm is shed just before birth, as the folliclesbegin to develop (Gibbs,’41; Hanson, ’47);and in the human fetus this outer layer of the developing epidermis is lost at week 24 of gestation, when the first hairs erupt (Holbrook and Smith, ’81).Thus in the eutherian the periderm is only present in utero and disappears with the eruption of hair. For marsupials, the terms periderm, epitrichium, and sometimes epidermis appear synonymous. McCrady (’38) described the newborn Didelphis uirginiana as possessing an epitrichium which covers the eyes, ears, and sides of the mouth. The eyelids were stated to “have become fused together and covered over by epitrichium.” Hill and Hill (’55),defining the structural features of the newborn Dasyurus uiuerrinus, described “the presence over the very thin epidermis of an impermeable keratinised membrane, the epitrichium, for the protection of the young from dessication.” Lyne et al. (’70) described the newborn Trichosurus uulpecula skin as very thin, with a well defined periderm or epitrichium. It was not stated when this well-defined layer of cells disappeared. The periderm was not present in the opossum at 7 days postpartum (Krause et al., ’78). Hughes and Hall (’&I), in a later study of the newborn opossum, described an epitrichium which completely covered the external ear and eye. The cellular covering of the eye, ear, and sides of mouth of the newborn marsupial is composed of a developing epidermis with an outer layer of fibrillar cells, commonly known as the periderm or epitrichium (Gemmell et al., ’88a). This study demonstrated that the periderm or epitrichium is present on the newborn native cat and disappears soon after birth. This disappearance occurs well before the appearance of hair follicles and shafts. Thus the correlation between hair shafts and the disappearance of the

periderm observed in eutherians is not present in marsupials. On closer examination of the periderm, it is apparent that the cells are filled with fibrils and degenerated cellular organelles and have a similar structure to that of cornified cells. It is possible that the greater thickness observed in the external layer of cornified cells (periderm or epitrichium) is due to the presence of intracellular fluids. When the newborn marsupial moves from the aqueous environment of the uterus to the aerobic environment of the pouch, this fluid is lost from the periderm and thus the outer layer of cells assumes the normal features of a cornified layer. If this hypothesis is correct, it is unlikely that the periderm is a major structure preventing dessication of the young; rather it is the outer layer of a developing epidermis. Although keratinocytes make up the majority of cells in the epidermis, several other types of cells are also present. Merkel cells, thought to be part of sensitivemechanoreceptors,are observed around the mouth of the newborn marsupial (Jones and Munger, ’86; Gemmell et al., ’88a). These cells which are found in abundance around the oral region of newborn marsupials were not observed in the dorsal skin of the developing native cat until day 150. Lyne et al. (’70) also did not describe Merkel cells in the developing epidermis of the possum; however, they did observe these cells at day 57 in the epidermis of the sheep (Lyne and Hollis, ’68). Another type of epidermal cell, the Langerhans cell, thought to be an antigen-presenting cell (Shelley and Juhlin, ’76; Sting1 et al., ’78; Towes et al., ’80),was first seen at day 23 postpartum in the native cat. All marsupial young, including those of the native cat, are born without hair and are incapable of maintaining a steady rectal temperature. The thyroid gland, an endocrine gland which influences skin structure and thermoregulation, is not present in the newborn marsupial. Thyroid function, production of hair, and thermogenic capacity in the marsupial do not occur until approximately two-thirds of the way through pouch occupancy.These activities occur in the rat and mouse just before birth and in the fetal sheep during late gestation (Johnston and Gemmell, ’87).The appearance of hair and sebaceous and sweat glands at day 67 post partum in the native cat would support the view that thermogenic capacity is developed in the latter part of pouch life. Although the native cat has an immature form of integument when born compared with immature eutherians such as the rat, the various layers

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Gemmell, R.T., B. Peters, and J. Nelson (1988a) Ultrastructural identificationof Merkel cells around the mouth of the newborn marsupial. Anat. Embryol. 177r403-408. Gemmell, R.T., G. Johnston, and M.M. Bryden (1988b)Osteogenesis in two marsupial species, the bandicoot Isoodon macrourus and the possum Trichosurus uulpecula.J. Anat. 159~15L-164. Gibbs, H.F. (1941) A study of the post-natal developmentof the skin and hair of the mouse. Anat. Rec.80r61-82. Hall, L.S., and R.L. Hughes (1985) The embryological development and cytdEerentiation of the anterior pituitary in the mmupiallsoodon macrourus.Anat. Embryol.172~353363. Hanson, J. (1947)The histogenesis of t h e epidermis in the rat and mouse. J. Anat. 81:174-196. Henrikson, R.C. (1969) Observations on the fine structure of the epidermis of an Australian marsupial (Trichorurus uulpecula).J. Anat. 104t409. Hill, J.P., and W.C.O. Hill (1955) The growth stages of pouch young of the native cat (Dasyurus uiuerrinus)together with observations on the anatomy of the newborn young. Trans. Zool. Soc. Lond 28r349-453. Holbrook, K.A., and L.T. Smith (1981) Ultrastructural aspects of human skin during embryonic, fetal, premature, neonatal and adult periods of life. Birth Defects 1 7 . 3 8 . ACKNOWLEDGMENTS Hughes, R.L., and L.S. Hall (1984) Embryonic development The authors thank the Australian Research in the common brushtail possum (Tnchosurus uulpecula). Grants Scheme and the National Health and In A.P. Smith and I.D. Hume (4s.): Possums and Gliders. Sydney:Australian Mammal Society, pp. 197-212. Medical Research Council for financial assisJohnston, G.M., and R.T. Gemmell(1987)Thyroid developtance. ment in the marsupial bandicoot, Isoodon macrourus.Anat. Rec. 217:178-187. Jones, T.E., and B.L. Munger (1985) Early differentiation of LITERATURE CITED the afferent system in glabrous snout skin of the opossum Begg, R.J. (1981) The small mammals of Little Nourlangie (Monodelphis domesticus). Somatosensory Res. 3r169Rock, N.T. 111.Ecology of Dasyurus hallucatus, the North184. em quoll (Marsupialia:Dasyuridae). Aust. Wild. Res. 8t73Krause, W.J., and J.H. Cutta (1983) Postnatal development 85. of the thyroid gland in the opossum (Didelphis uirginiam). Catling, P.C., and G.P. Vwon (1976) Adrenocortical horActa Anat. 116:322-338. mones in the neonate and pouch young of the tammar Krause, Wd., and C.R. Leeson (1973)The postnatal developwallaby, Macropus eugenii.J. Endocrinol. 69447-448. ment of the respiratory system of the opossum. I. Light and Gemmell, R.T. (1986) Lung development in the marsupial scanningmicroscopy. Am. J. Anat. 137r.337-356. bandicoot,Isoodon mcrourus. J. Anat. 148~193-204. Krause, W.J., and C.R. Leeson (1975) Postnatal development Gemmell, R.T., and G. Johnston (1985) The development of of the respiratory system of the opoasum. 11. Electron thermoregulationand the emergence from the pouch of the microscopy of the epithelium and the pleura. Acta Anat. marsupial bandicoot, Isoodon macrourus. Physiol. ZooL 9228-44. 58:29%302. Krause, W.J., J.H. Cutts, and C.R. Leeson (1978) Postnatal Gemmell, R.T., and G.J. Little (1982) The structure of the development of the epidermis in a marsupial Didelphis lung of the newborn marsupial bandicoot,Isoodon macrouuirginiam. J. Anat. 125t85-99. rus. Cell Tissue Res. 223t445453. Leatherland, J.F., and M.B. Renfree (1983) Structure of the Gemmell, R.T., and J. Nelson (1988a) The ultrastructure of pars distalis in pouch-young tammarwallabies (Macropus the pituitary and the adrenal gland of three newborn mareugenii).Cell Tissue Res. 230t587403. supials (Dasyurus hallucatus, Trichosurus uulpecula and Lyne, A.G. (1970) The melanocyte population in the skin Isoodon rnacrourus).Anat. Embryol. 177:39M2. during developmentof the marsupial Trichosum uulpecGemmell, R.T., and J. Nelson (1988b) The ultrastructure of ula. Aust. J. Biol. Sci. 23.697-708. the olfactorv svstem of three newborn marsuDial Lyne, A.G., and D.E. Hollis (1968) Merkel cells in sheep - srxcies. epidermis during fetal development. J. Ultrastruct. Res. Anat. Rec. i21.65M2. 3444472. Gemmell, R.T., and J. Nelson (198&) The ultrastructure of the lung of two newborn marsupial species, (Dasyurus Lyne, A.G., and D.E. Hollis (1972)The structure and development of the epidermis in sheep fetuses. J. Ultrastruct. Res. hallucatus and Trichosurus uulpecula). Cell Tissue Res. 38~444-458. 252;682485. Gemmell, R.T., P. Singh-Asa, G. Jenkin, and G.D. Thorburn Lyne, A.G., R.C. Henrikson,and D.E. Hollis (1970) Development of the epidermisof the marsupial Trichosurusuulpec(1982) Ultrastructuralevidence for steroid hormone prducula. Aust. J. Biol. Sci. 23:1067-1075. tion in the adrenal of the marsupial,Isoodon macroum at McCrady, E., Jr. (1938) The Embryology of the Opossum. birth. Anat. Rec. 203:505412. 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of the epidermis are discernible soon after birth. Hair and sebaceous and sweat glands are observed in the skin just prior to the mother leaving the young in the nest a t days 60 to 70 of lactation. When the young ace independent (by day 150),the skin is of a similar structure to that of the newly independent eutherian mammal. The transfer of the young from the uterus occurs when the epithelial covering of the body is very immature. On entering the pouch, the periderm is compacted and the epidermal layers proliferate in preparation for the formation of the follicles. The appearance of follicles and associated glands allow the young to be left in the pouch approximately half way through lactation and the skin thickness and number of follicles increases to allow the newborn young to survive at weaning.

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in native cats of the family Dasyuridae. Int. Zool. Year Book 11:38-41. Reynolds, H.C. (1952) Studies on reproduction in the opossum Didelphis uirginiana. Univ. Calif. Publ. Zool. 5 2 1 4 8 . Setchell, P.J. (1974) The development of thermoregulation and thyroid function in the marsupial Macropus eugenii (Desmarest).Comp. Biochem. Physiol. 47k111&1121. Shelley, W.B., and L. Juhlin (1976) Langerhans cells form a reticdoepithelial trap for external contact antigens. Nature 261t4647.

Stingl, G., S.I. Katz, L. Clement, I. Green, and Shevach, E.M. (1978) Immunologic functions of Ia-bearing epidermal Langerhans cells. J. Invest. Dermatol. 121:200&2013. Towes, G.B., P.R. Bergstresser, and J.W. Streilein (1980) Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follow skin painting with DNFB. J. Immunol. 124t44H53. Walker, M.T., andR.T. Gemmell(l983) Organogenesisof the pituitary, adrenal and lung a t birth in the wallaby Mucropus rufogriseus. Am. J. Anat. 168:331-344.

Postnatal development of the skin of the marsupial native cat Dasyurus hallucatus.

Skin development of the Northern native cat was examined from birth to weaning at 150 days post partum. An outer layer of cells, termed the periderm o...
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