This research was conducted on the interdigital gland of the roebuck (Capreolus capreolus L.). In the presented study the detailed morphology, type of secretion and anatomical location of this gland are described. The gland is composed of a pouch and an excretory duct. The glandular tissue contains sebaceous acini of the holocrine secretion and tubular-coil glands of the apocrine secretion, and no hair follicles or sweat glands were found. Differential staining established the gland’s detailed structure and, using the Sudan Black B method, we have shown the distribution of lipids inside glandular acini.Istraživanje je provedeno na uzorcima interdigitalnih žlijezda srnjaka (Capreolus capreolus L.). Smještaj, morfološke osobitosti i sekrecija navedene žlijezde su detaljno opisani. žlijezda ima oblik vrećice s izvodnim kanalom. U njenom tkivu razlikuju se lojni acinusi holokrine sekrecije i tubularne klupčaste stanice apokrine sekrecije. Dlačni folikuli i znojne žlijezde nisu utvrđeni. Diferencijalnim bojenjem utvrđena je struktura žlijezde, a pomoću Sudan Black B metode prikazan je raspored lipida u žlijezdanim acinima

Alen Slavica

Ante Hraste

Dean Konjević

Zdravko Janicki

Zdravko Marinović

Ðurđica Stubičan

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27VETERINARSKI ARHIV 73 (1), 27-37, 2003* Contact address:Prof. Dr. Zdravo Janicki, Chair for Game Biology, Pathology and Breeding, Faculty of Veterinary Medicine, Universityof Zagreb, Heinzelova 55, 10000 Zagreb, Croatia, Phone: +385 1 2390 260; Fax: +385 1 2441 390;E-mail: janicki@vef.hrISSN 0372-5480Printed in CroatiaMorphohistological characteristics of the interdigital gland inthe roebuck (Capreolus capreolus L.)Zdravko Janicki1*, Ante Hraste2, Alen Slavica1, Dean Konjeviæ1,Zdravko Marinoviæ3, and Ðurðica Stubièan41Chair for Game Biology, Pathology and Breeding, Faculty of Veterinary Medicine,University of Zagreb, Zagreb, Croatia2Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia3‘Veterinar d.o.o.’ Veterinary Outpatient Department, Slavonski Brod, Croatia4Library of the Faculty of Veterinary Medicine, University of Zagreb, Zagreb, CroatiaJANICKI, Z., A. HRASTE, A. SLAVICA, D. KONJEVIÆ, Z. MARINOVIÆ, Ð.STUBIÈAN: Morphohistological characteristics of the interdigital gland in theroebuck (Capreolus capreolus L.). Vet. arhiv 73, 27-37, 2003.ABSTRACTThis research was conducted on the interdigital gland of the roebuck (Capreolus capreolusL.). In the presented study the detailed morphology, type of secretion and anatomical locationof this gland are described. The gland is composed of a pouch and an excretory duct. Theglandular tissue contains sebaceous acini of the holocrine secretion and tubular-coil glands ofthe apocrine secretion, and no hair follicles or sweat glands were found. Differential stainingestablished the gland’s detailed structure and, using the Sudan Black B method, we have shownthe distribution of lipids inside glandular acini.Key words: roebuck, interdigital gland, histology, histochemistry28 Vet. arhiv 73 (1), 27-37, 2003Z. Janicki et al.: Interdigital gland in the roebuckIntroductionMany species belonging to the Artiodactyla order have well-developedinterdigital glands, but they differ morphologically from specie to species.SIVACHELVAN et al. (1992), has reported that it comes as a developed organ.RAESFELD (1978) designates the space between the digits the ‘’hoof skinorgan’’, while BAVDEK (1981) calls the same gland in sheep calls ‘’interdigitalsinus’’. In sheep, roe deer and Japanese serow the glandular secretedmaterial is inside a pouch with a hair-covered excreting duct, from whichsecretion trickles (SIVACHELVAN et al., 1992), but in other species this glandis merely a form of skin fold (POCOCK, 1910). This gland produces theapocrine and holocrine types of secretion. The Japanese serow has well-developed interdigital glands on all four extremities (ATOJI et al., 1988) whilethe roe deer (Capreolus capreolus L.) has the glands only on the hindfeet. Prompted by the dearth of written works on the roebuck’s interdigitalgland we decided to attempt to correct this omission. Therefore, the primarygoal of this study is to demonstrate the primary morphohistochemicalcharacteristics of the roebuck’s interdigital gland, or in other words to showits anatomical placement, its appearance and constitution, as well asdescribing its content and the way in which is produced. Finally, we providea description of the role the gland plays in the roebuck’s life, and also ashort comparison between this gland and the glands of other species.Materials and methodsIn order to conduct this research we collected 10 pairs of the roebuckhind feet. All animals were adults and they were shot on the area ofJastrebarsko during a selective hunt during the period May - August 1996.The mating season of the roe deer occurs in July and lasts approximatelyone month. The roebuck shows a seasonal cycle of testicular and accessorysex gland activity. If young roebuck are in good physical condition they arecapable of breeding before the age of one year. The gland preparationswere stained using haematoxylin and eosin (HE) and differential stainingby the Van Giesen method (ŠVOB, 1974). For proving of the lipids we usedthe Sudan Black B method (ROMEIS, 1968). Acid glycosanimoglycanes wereproven using the method of staining with alcian blue at pH 2.5 (PEARSE,29Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 20031968). Glycogen distribution was determined using the PAS staining method(PEARSE, 1968).ResultsThe roebuck interdigital gland is located in the space between the digits(regio interdigitalis) on its hind feet. The glands are situated inside the looseconnective tissue and covered with skin, so that only the opening duct isvisible in the interdigital space (Fig. 1).Fig. 1. Opening of an excretory duct on the interdigital skin surfaceThe glandular tissue forms the pouch, the size of an average hazelnut,and can be divided at the bottom, in the middle part and at the excretingduct. Inside the interdigital gland we could observe the pouch secretion,which at room temperature is thick, with the desquamate epithelium and athin, delicate, de-pigmented hair within it. The pouch bottom of the interdigitalgland is placed at the level of half of the first phalanx and extends to thethird phalanx (Fig. 2). The excretory duct is placed almost horizontal to theproximal part of the free interdigital space and ends with an opening to thedorsal surface of the interdigital fold. The lumen of the interdigital pouch iscovered with a thin layer of the epidermis. On the sections stained with30Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 2003Fig. 2. Gland location in the interdigital space: A) Interdigital gland B) Second phalanx;C) Articular surface of the metacarpal boneFig. 3. Interdigital gland in the roebuck, H&E, ×20, scale bar = 100 µm. A) Immaturesebaceous cells; B) Glandular parenchyma; C) Excretory duct31Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 2003Fig. 4. Interdigital gland in the roebuck, H&E, ×20, scale bar = 100 µm. A) Coil glands;B) Sebaceous glands; C) Connective tissueFig. 5. Interdigital gland in the roebuck, Van Giesen, ×20, scale bar = 100 µm. A) Coilglands; B) Sebaceous glands32Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 2003haematoxylin and eosin we could see the glandular parenchyma, theimmature sebaceous gland and the excretory duct with the secretion product(Fig. 3). Close to the gland we found the muscle fibers and between themthe connective tissue fibres. At the borderline between the subcutis andthe dermis (corium) there were accumulations of narrow, coil-tubular glandsof the apocrine secretion, and due to their darker pigmentation they can beseen macroscopically on the cross-sections of the prepared gland. Theseglands are surrounded with connective tissue and muscle fibres (Fig. 4).Close to the borderline between the subcutis and the dermis there areapocrine glandular tubules. Among them we found layers of collagen andmuscle fibres of differing density. On the borderline between the subcutisand the dermis there is a larger amount of the elastic and only a smalleramount of the collagen fibres. It would appear that the amount of the elasticfibres gradually increases towards the subcutis and the epidermis, and thatthe fibres lie parallel to the epidermis. On the other hand, at the bottom ofthe glandular pouch, collagen and elastic fibres are more densely developedaround the coil-tubular glands than around the sebaceous glandular acini.Fig. 6. Interdigital gland in the roebuck, Sudan Black B ×20, scale bar = 100 µm.A)  Sebaceous gland lumen; B) Excretory duct33Vet. arhiv 73 (1), 27-37, 2003Z. Janicki et al.: Interdigital gland in the roebuckOn the material stained using the differential staining method of VanGiesen we were able to observe sebaceous glandular cells and secretioninside the pouch lumen, ranging from greenish to yellowish, while the coilglands of the apocrine secretion were intensely yellowish-green (Fig. 5).Staining with Sudan Black B showed a high concentration of sudanophilicsubstance in all layers of the sebaceous and the coil glands (Fig. 6). Thecombined sebaceous alveoli form a kind of excretory duct through whichthe secretion is discharge into the pouch lumen, unlike in the body’s sebaceousglands. Above the basal membrane of the roebuck’s interdigital gland thereis a stratum germinativum with cells capable of intensive metabolic activity.The glandular cells located peripherally next to the basal membrane aresmaller and flatter, as opposed to the more centrally located cells. Duringcell growth they become more rounded in shape, with clearly visible cellmembrane and nucleus. Cells that are closer to the centre of the alveoli aremuch bigger, their cytoplasm is weakly stained, the nucleus is invisible, andthe cell wall is obviously thinner and cracked, which all that points to theirgradual fatty infiltration. This is characterized by the accumulation of lipids,whose concentration is highest in the area of the gland excretory duct.Staining with the PAS method reveals that a small amount of neutralglycosaminoglycan is present in a lower concentration level in the cells,while acid glycosaminoglycans stained with alcian blue are present on thehigher amount in the secretory product.DiscussionIn this study we have demonstrated that the roebuck interdigital glandcan be found only on its hind feet. This is contrary to findings of   RAESFELD(1978) in the moufflon (Ovis musimon L.) and the antelope, and to those ofATOJI et al. (1988) in the Japanese serow (Capricornis crispus), due to thefact that all those species have interdigital gland on all four feet. The shapeand size of the interdigital gland in the roebuck are analogous to the descriptionof the same glands in the Japanese serow and sheep (KLIMOV, 1947; ATOJIet al., 1987; SIVACHELVAN et al., 1992). The size of the gland and of the glandularacini is closely connected with the reproductive cycle, as observed byBULLOUGH and LAURENCE (1960), MULLER et al. (1983) and ODEND’HAL et al.(1992). Our findings regarding the structure and location of the interdigital34Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 2003glands in the roebuck differ somewhat from the description of this gland inthe sheep (BAVDEK, 1981). In sheep the gland is located inside the connectivetissue, surrounded by a capsule and also has sweat gland cells (POCOCK,1910). In our findings we were unable see that the connective tissue formsa capsule that covers the surface of the gland, nor could we find sweatglands cells. The glandular pouch consists of sebaceous and coil glandswhich are disseminated in the connective tissue, while the skin covers thesurface of the gland. Therefore, the opening of excretory duct can be seenmacroscopically only from the dorsal side in the interdigital space, whilefrom the plantar side the skin limits the gland. The movement of lifting,gathering, sagging and interspacing of hoofs mechanically discharges thegland. This is why the interdigital space at the level of the second phalangeacts as a pump for the gland. The finding of the muscle fibres around thecoil glands, according to BAVDEK (1981), KLIMOV (1947) and RAESFELD (1978),confirms that secretion is aided by muscle contractions (ROTHMAN, 1954).According to SOKOLOV et al. (1990) the roebuck marks his territory with theincreased secretion of the interdigital gland, while RAESFELD (1978) thinksthat it occurs in dangerous situations, e.g. when the roebuck runs from apossible predator. In order to prevent total and immediate discharge ofsecretion of the interdigital gland a danger situation the gland lumenpossesses an intertwined hair (upon which the secretion of the glandgradually seeps). This finding only partially corresponds with the descriptionby SIVACHELVAN et al. (1992) of the foetal and post-natal development of theinterdigital gland in the sheep, as we found no hair follicles in the lumen. Itseems, therefore, that, as observed by MONTAGNA (1956, 1963), in adultsthe hair follicles are reduced and gradually completely disappear when theanimal matures. The wall of the roebuck’s interdigital pouch is thicker andbetter developed than in other hoofed animals (ATOJI and SUZUKI, 1987). Inour findings the amount of phospholipids and neutral fats differs in theinterdigital gland. The very high amount of sudanophilic substance is visiblein the cells and gland excretory duct. It appears to be somehow lessnoticeable in the lumen of the glandular acini, while we were unable toobserve it in the basal membrane. It is well known that the formation of thesebum inside the glandular cells is the result of the transformation ofcarbohydrates into lipids. It is therefore easy to understand the unequal35concentration of lipid substances in cells inside the glandular pouch. This isalso in accordance with the MÜLLER-SCHWARZE (1978) report on fatty aciddistribution inside the sebaceous gland.This finding confirms the fact that the interdigital gland has a role inlubricating the movable parts of the hoof, while JENKINSON and NAY (1975),MONTAGNA (1963), SOKOLOV and GROMOV (1993), also attribute to it scentfunction, which is important for intercommunication. In our examination ofthe coil gland we have found a lipid content which, according to RAESFELD(1978), is a volatile substance, a fragrant component of interdigital secretion.The primary function of the interdigital gland in animals with long feet (elk- red deer - Cervus elaphus L.) is to lubricate the space between thedigits. Therefore, it is not so important for scent communication because itplays a minor role in leaving a scent trail (HOFFMAN and THOME, 1986). Theopposite is the case with species with short feet (Japanese serow and roedeer) whose interdigital gland has developed as a specialized skin glandwith a cyclic excretory activity, which as a primary function scent marksthe trail (ATOJI et al., 1988). According to MONTAGNA (1963) and JENKINSONand NAY (1975) those glands have a fungicidal and a bactericidal activity thathelps disinfect the skin, keeps it elastic and protects it from UV radiation.Therefore, we believe that in the roebuck it has the same function, which iswhy it can be regarded as a specialized organ. The size of the sebaceousglands depends on the part of the body in which they are located, on therange and the thickness of the hair cover, and on hormonal regulation(MONTAGNA, 1962; PRASAD and SINHA, 1979; BULLOUGH and LAURENCE,1960).ReferencesATOJI, Y., Y. SUZUKI (1987): Lecitin histochemistry of the intraorbital gland in Japaneseserow. Acta anatomica nipponica 62, 481-488.ATOJI, Y., M. SUGIMURA, Y. SUZUKI (1988): Lecitin histochemistry of the interdigitalgland in the Japanese serow (Capricornis crispus) in winter. J. Anatomy 161, 159-170.BAVDEK, S. (1981): Interdigitalni sinus ovaca. In: Koža in njeni derivati. VTOZD.Biotehniške fakultete v Ljubljani.BULLOUGH, W. S., E. B. LAURENCE (1960): Experimental sebaceous gland secretionsin the adult male mouse. J. Invest. Dermatol. 35, 37-42.Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 200336HOFFMAN, R. R., H. THOME (1986): Zur functionellen Morphologie undMikroarchitektur des Zirkumkaudalorgans von Cervus elaphus und Cervus nippon.Berl. Münch. Tierärztl. Wschr. 99, 418-424.JENKINSON, D. M., T. NAY (1975): The sweat glands and hair follicles of differentspecies of bovidae. Aust. J. Biol. Sci. 28, 55-68.KLIMOV, A. F. (1947): Anatomija domaæih životinja. I dio, Kožne žlijezde. Nakladnizavod Hrvatske. Zagreb. p. 392.MONTAGNA, W. (1956): The Structure and Function of Skin. 1st ed. Academic Press.New York.MONTAGNA, W. (1962): The structure and function of the skin. 2nd ed. Academic Press.New York.MONTAGNA, W. (1963): Comparative aspects of sebaceous glands. In: Advances inBiology of Skin and Sebaceous Glands. Vol. 4, (Montagna, W., R. A. Oxford, Eds.).Pergamon press. Oxford. pp. 32-45.MULLER, G. H., R. W. KIRK, D. W. SCOTT (1983): Small Animal Dermatology. 3rd ed.W. B. Saunders Company. Philadelphia. p. 889.MÜLLER-SCHWARZE, D. (1978): Responses of reindeer to interdigital secretions ofconspecifics. J. Chem. Ecol. 4, 325-335.ODEND’HAL, S., K. V. MILLER, D. M. HOFFMAN (1992): Preputial glands in thewhite-tailed deer (Odocoileus virginianus). J. Mamm. 73, 299-302.PEARSE, A. G. E. (1968): Histochemistry Theoretical and Applied. J. A. Churchill Ltd.,London.POCOCK, R. I. (1910): On the specialized cutaneous glands of ruminants. Proceedings ofthe Zoological Society of London, pp. 840-986.PRASAD, R., R. D. SINHA (1979): Histological and certain histochemicals studies onsebaceous glands and their modifications in the eyelids of the Indian buffalo (Bubalusbubalia). Indian. Vet. J. 56, 672-674.RAESFELD, V. F. (1978): Das Rehwild. Verlag Paul Parey, Hamburg und Berlin, pp. 10-15.ROMEIS, B. (1968): Mikroskopische Technik. Oldenbourg Verlag. München, Wien.ROTHMAN, S. (1954): Physiology and Biochemistry of the Skin. University of ChicagoPress. Chicago.SIVACHELVAN, M. N., A. YAHAYA, A. G. CHIBUZO (1992): Developmental changesin the interdigital pouch of Yankasa sheep. Small Ruminant Res. 9, 303-312.SOKOLOV, V. E., S. GROMOV, S. V. SIMAK (1990): Role of excretions from specificscutaneous glands in the chemical communication of Tartarian roes. Dokladi AkademiiNauk SSSR 315, 1507-1510.SOKOLOV, V. E., S. GROMOV (1993): Chemical communication in roe deer (Capreoluscapreolus). Zoologicheski Zhurnal 72, 123-136.Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 200337JANICKI, Z., A. HRASTE, A. SLAVICA, D. KONJEVIÆ, Z. MARINOVIÆ, Ð.STUBIÈAN: Morfohistološke znaèajke interdigitalnih žlijezda srnjaka(Capreolus capreolus L.). Vet. arhiv 73, 27-37, 2003.SAŽETAKIstraživanje je provedeno na uzorcima interdigitalnih žlijezda srnjaka (Capreolus capreolusL.). Smještaj, morfološke osobitosti i sekrecija navedene žlijezde su detaljno opisani. žlijezdaima oblik vreæice s izvodnim kanalom. U njenom tkivu razlikuju se lojni acinusi holokrinesekrecije i tubularne klupèaste stanice apokrine sekrecije. Dlaèni folikuli i znojne žlijezde nisuutvrðeni. Diferencijalnim bojenjem utvrðena je struktura žlijezde, a pomoæu Sudan Black Bmetode prikazan je raspored lipida u žlijezdanim acinima.Kljuène rijeèi: srnjak, interdigitalne žlijezde, histologija, histokemijaReceived: 7 November 2002Accepted: 14 February 2003Z. Janicki et al.: Interdigital gland in the roebuckVet. arhiv 73 (1), 27-37, 2003ŠVOB, M. (1974): Histološke i histokemijske metode. Izdavaèko poduzeæe ‘’Svjetlost’’.Sarajevo.

Morfohistološke značajke interdigitalnih žlijezda srnjaka (Capreolus capreolus L.).

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