3rd International Conference on Ecological, Environmental and Biological Sciences (ICEEBS'2013) April 29-30, 2013 Singapore

Scent Glands of Gundi (Ctenodactylus gundi)

Omar A. Mshiri and Nadia S. Berim

modified sebaceous glands. Abstract—Morphological, anatomical and histological Preputial glands of rodents are usually described as a pair of investigations of cutaneous glands of skin specimens obtained from flask shaped or leaf like, bilaterally symmetrical structures, adult Ctenodactylus gundi revealed only two types of scent glands; embedded in the superficial fascia of the preputial skin (1) Greatly enlarged modified sebaceous glands annexed to coarse, covering the penis or clitoris of males and females respectively tough hairs covering the prepuce skin of both sexes, Hence the name preputial and clitoral glands of male and female respectively. The [1; 11]. Preputial glands of Jaculus jaculus were described as a size, number and distribution of these glands appear to reflect their number of glandular bodies circumferentially arranged around secondary role in the social behavior of Gundi. (2) Trilobated the base of the penis or clitoris of males and females perianal scent glands located circumferentially around the external respectively [12]. skin of the anal orifice. Two of the lobes lay ventro-lateral to the The perianal glands found in mammals are generally rectal canal and the remaining lobe lies ventral to the canal. The size bilobated or trilobated in their gross anatomy. Black-tailed of the glandular lobes varies seasonally, depending on age and sexual maturity of the animal. prairie dogs have trilobted perianal glands [7]. Other mammals Morphologically; these glands appear as sexually dimorphic with trilobated perianal glands include several species of organs, being larger in males than females. Anatomically, these ground squirrels [4]; [8]; [9]; [14]. glands are embedded in the superficial fascia of the anal dermal skin Literature indicated that the number and arrangement of the invading the epidermis by a number of small tortuous secretory ducts secretory lobes in the glands of the aforementioned animals is conveying the secretion on to the surface if the anal skin. identical, even-though the placement of the glands varies with Histologically, the glands clearly represent a circumferential aggregation of compound branched holocrine alveolar glands the species. Ground squirrels for example have two lateral surrounded by a number of tubular apocrine glands opening to the lobes and one ventral lobe [13]; [9]. Guinea pigs on the other outside through separate openings. hand have trilobated perianal scent glands the central one is Although, there are some reports in the literature on the structure, located dorsal to the anal canal [10]; [15]; [16]. histology and histochemistry of the perianal and preputial glands of Although, Ctenodactylus species have been reported to use several mammals, we were unable to locate any published material their hind quarters in a number of social behaviors such as concerning Gundi’s scent glands. This study will describe the anatomical and histological details of preputial and perianal glands of sand bathing, territorial marking, intraspecific identification, the adult male and female Ctenodactylus gundi as seen during the and mating rituals [2], literature are however very poor peak of sexual activity. concerning the structure and function of the perianal glands of this species. One study was limited to geographical Keywords— Perianal; Trilobated;,Apocrine; Holocrine; distribution and classification of the species; the other Ventrolateral. concentrated on the social activities such den marking, group numbers and territorialities. I. INTRODUCTION HE North African gundi Ctenodactylus gundi, occurs II. MATERIALS AND METHODS T from Morocco to North-Western Libya: gundis live in Healthy adult sexually mature male and female Gundi groups that sometimes contain multiple adult males and (Ctenodactylus gundi) were trapped from different ecological females [5; 13]. Gundi is one of the mammalian species that niches in Libya. These animals were sacrificed, dissected, have a highly developed sense of olfaction employed very photographed, and investigated carefully for existence of efficiently in social communication, using chemical signals possible scent glands. Two types of scent glands were found, originating in urine, feces, genital secretion, saliva, and photographed, and surgically removed. The glands were cutaneous scent glands [1; 11]. Although olfactory preserved in 10% formalin, labeled, processed and sectioned communication is believed to play a significant role in the using routine histological techniques. sexual and social behavior of all rodent species, little Reference histological series of 6μ thick sections were cut information exists on scent marking behavior of Ctenodactylus from paraffin wax embedded preputial and perianal glands of species. Even though, many authors have investigated and both males and females respectively. Sections were cut cross- described rodent preputial glands in great details, little have sectionally to show the architectural arrangement of the being mentioned about coarse hair attachment to large secretory lobes around the circumference of the penis and anal orifice. Sections were stained with Harrie’s haemtoxylin and Omar A. Mshiri and Nadia S. Berim are with University of Tripoli, Eosin [6], using standard procedures. All sections processed in Faculty of Science, Zoology Department Tripoli - Libya.

246 3rd International Conference on Ecological, Environmental and Biological Sciences (ICEEBS'2013) April 29-30, 2013 Singapore such a manner were examined microscopically, and carefully by a thick layer of skeletal muscles. Evidence of apocrine and evaluated for detailed histological description of glands in holocrine break down is very evident in the tubular and hand. alveolar components of each gland. While the mature secretory alveoli of the sebaceous compartment appear hollow at their III. RESULTS centers; broken apices of the secretory epithelium are clearly Gundis (Ctenodactylus gundi) have a slightly different represented by the small blebs facing the lumen of the tubular perianal glandular arrangement than any of the aforementioned glands (Figs. 7 a & b). animals in introduction; although, the number of glandular Comparative evaluation of Gundi’s scent glands from the lobes is similar to that reported for black tailed prairie dogs, histological point of view indicated great structural differences the arrangement of the glands around the anal orifice is between preputial and perianal glands of Ctenodactylus gundi; different. The secretory lobes are arranged circumferentially Indeed, it is apparent that perianal glands are much more around the anus in a triangular fashion. The base of the conspicuous and developed than preputial glands, the latter are triangle consists of two lobes facing the base of the tail (Fig. smaller in size representing modified sebaceous glands 1). In addition, the glandular structures are not located within annexed with hair follicles that differ from the general fur in the anal canal, but they are distributed around the interior anal length and texture (Fig. 8). dermal skin, each of which opens at the exterior circumference of the anal orifice by a separate opening (Fig. 2). IV. DISCUSSION The glands are sexually dimorphic, being larger and more Although perianal glands of many mammals have been conspicuous in sexually active males than females. The described in the literature as bilobated, trilobated or number of glandular masses never exceeded three well defined multilobated [14]; [9]; [8]; [3], it is very evident from findings structures in all captured specimens. The glands can easily be of this study that such a description is applicable to Gundi seen by the naked eye depending on age and sexual maturity of (Ctenodactylus gundi) only to a certain extent. Although, the the animal (Fig. 1). glands are trilobated, their arrangement around the Each of the glandular masses represents a highly modified circumference of the anal orifice is different from other rodent compound branched sebaceous gland, surrounded by many species. While the base of the triangular area consists of two tubular apocrine glands forming one large, compound, tubule- lobes in other species, the three lobes of Ctenodactylus alveolar gland, embedded in the deep fascia of dermis of the perianal glands are distributed evenly around the anal opening. anal area; it is surrounded by a thick capsule of connective The placement of the perianal glands of Ctenodactylus is tissue and striated muscle fibers (Fig. 3). Incomplete also different from any other mammal found in the literature. trabeculea arise from the capsule invading the sebaceous gland While most perianal glands exist in the form of nipples dividing it into a number of secretory lobes, subdivided into a attached to saccular structures located within the anal canal, number of lobules, each of which is in turn composed of those of the Gundi are located in the circumferential borders of secretory alveoli (Fig. 3). the anal sphincter. Therefore, we suggest that the anal glands Each alveolus is surrounded by spindle shaped of prairie dogs and the animals alike should be referred to as myoepithelial cells and consists of a clump of simple anal sacs instead of perianal glands, since they are found in the polygonal epithelial cells arranged on a basement membrane form of protrusible nipples that can be extruded to the outside (Fig. 4). Hollowing out of the secretory alveoli occurs in the just like those of the stripped skunk. central area of the alveolus, and proceeds toward the Histologically, the perianal glands of ctenodactylus appear periphery, creating an alveolar duct which leads to a lateral to be modified tubulo-alveolar glands embedded in the deep duct. Lateral ducts from different lobules; empty their fascia of the dermis of the anal area, which also different from secretory contents into one large central lobular duct, lined by the description of [7] reported for the so- called perianal a layer of stratified squamous epithelium three to four cells in glands of the black tailed prairie dogs. Evidence of Holocrine thickness (Fig. 5). and apocrine elements was found in the secretory epithelium of The central ducts of all secretory lobes empty into one perianal glands of ctenodactylus. The duct system of these central main duct lined by a layer of stratified squamous glands is different from that described for prairie dogs, but epithelium five to seven cells in thickness. The epithelial lining very similar to that of Preputial glands of the musk rat of the main duct shows evidence of keratinization only at its Ondantra zibethicus described by [3]. The perianal glands of junction with the epidermis near the anal orifice, however; the Ctenodactylus gundi are represented by three lobes of lateral ducts lining lack any keratinization (Figs. 6 a & b). circumferentially arranged, sexually dimorphic, glandular Each gland opens through a separate opening, which appears structures subcutaneously embedded in the deep fascia of the as a pinhead whitish area at the surface of the anal orifice. skin surrounding the anal sphincter. The connective tissue capsule surrounds the holocine Each glandular mass is surrounded by a connective tissue elements of the gland is followed by two or three rows of capsule sending incomplete trabeculea dividing the gland into tubular apocrine glands, lined with simple columnar a number of lobes opening into a main duct. Each lobe is epithelium and the compound glandular mass is encapsulated composed of a number of lobules consisting of secretory

247 3rd International Conference on Ecological, Environmental and Biological Sciences (ICEEBS'2013) April 29-30, 2013 Singapore polygonal epithelial cells arranged on a basal lamina and surrounded by spindle shaped myoepithelial cells; this description agrees with many authors in the field of ethology [1, 3, 9, 10]. Presence of well defined skeletal muscle fiber in the capsular connective tissue clearly indicates that the secretory materials are emitted from these glands voluntarily when ever is needed unlike regular sebaceous glands from which the sebum is secreted involuntarily by accumulative replacement of older secretion. Presence of the striated muscle fibers dispersed within the connective tissue matrix surrounding each of the glandular masses apparently exist to function as constricting elements, that cause the extrusion of the secretory materials. Oily secretions are emitted from the glands through the secretory Fig. 2 Photomicrograph of a cross-section of one gland ducts during mating rituals and other different social showing the gland opening in relation to the anal orifice. AO, behaviors. Enlargement of the secretory openings, around the anal orifice; GO, gland opening; L,lobe; T, trabeculum; SM, circumference of the external surface of the anal sphincter skeletal muscle; CC, connective tissue capsule indicate that these glands play a significant role in scent marking, since the animals are often seen dragging their anal quarters around their territorial grounds just like domestic cats, dogs, prairie dogs and many other canidae as it has been reported by [2; 7]. It is also believed that the scent emitted from these glands may play a role in defense, mating rituals and maintaining of the social status among the species. These glands may be used as a signaling device conveying inter and intra-specific clues between the species and other species of predators since the gundis are reported to sniff each other’s genital and anal areas during mating, fighting, aggressiveness, submissiveness and dominant behaviors [13]. The less developed, modified sebaceous glands in dermal skin of the prepuce of both males and females suggest a Fig. 3. Photomicrograph of the anal area showing histological structure of the anal orifice and surrounding glands. HG, holocrine secondary role of preputial and clitoral glands in mating glands; AG, apocrine glands; AO, anal orifice; MD, main duct; LD, rituals, territoriality, aggressiveness and social behaviors of lateral duct; C, capsule; T, trabeculum. X=10 Ctenodactylus gundi.

Fig. 4. Photomicrograph of a cross-section in a number of secretory Fig.1. Anal area of male Ctenodactylus gundi showing the alveoli showing myoepithelial cells surrounding each alveolus. trilobated perianal gland arrangement around the anal orifice Arrows; Myoepithelial cells, SA; secretory alveolus. X 100 (arrows).

248 3rd International Conference on Ecological, Environmental and Biological Sciences (ICEEBS'2013) April 29-30, 2013 Singapore

B Fig. 7. Cross-section of the secretory alveoli (a) and tubules (b) of

Fig. 5. Photomicrograph of the perianal gland duct system. C; the perianal glands showing holocrine break down and detachment capsule; T,trabeculum; MD, main duct; LD, lateral duct; AD, of apical pleps of apocrine glands. HBC, holocrine breakdown; Mc, alveolar duct. X 10. Myoepithelial cells; P, Pleps; AG, Apocrine gland; CC, connective tissue capsule. X 100.

A

B Fig. 6. Photomicrograph of the epithelial lining of the secretory ducts. A, main duct; B, Lateral duct. X 40. Fig. 8. Photomicrograph of hair follicles annexed to sebaceous gland alveoli. HF, hair follicle; SG, sebaceous gland; SM, skeletal muscle.X100.

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