Histomorphology of Preorbital Gland in Territorial and Non-Territorial Male Blackbuck Antelope Cervicapra, a Critically Endangered Species

Home , Japanese serow, Preorbital gland, Scent gland

Biologia 66/2: 370—378, 2011 Section Zoology DOI: 10.2478/s11756-011-0015-4

Histomorphology of preorbital gland in territorial and non-territorial male blackbuck Antelope cervicapra, a critically endangered species

Thangavel Rajagopal1, 2 & Govindaraju Archunan1*

1Centre for Pheromone Technology, Department of Animal Science, School of Life Sciences, Bharathidasan University, Tiruchirappalli-620 024. Tamil Nadu, India; e-mail: [email protected] 2Department of Biotechnology, Ayya Nadar Janaki Ammal College (Autonomous), Sivakasi-626 124, Tamil Nadu, India.

Abstract: The preorbital gland is a specialized dermal gland of antelopes which plays an important role in territorial marking behavior and pheromonal communication. To our knowledge, there is little information available on the role of preorbital gland marks in Indian antelopes (blackbucks). Males are seen averting the gland during behavioural display and territorial marking but the functional aspect of this gland has not been examined. Hence, the aim of this study was to describe the histomorphology of the preorbital gland in territorial and non-territorial male blackbucks to determine its morphology and secretory function. The results showed that the preorbital gland is composed of modiﬁed sebaceous and apocrine glands. The apocrine gland is lined by simple cuboidal epithelial cells; the serous parts of the secretory products are often seen in the apical portions of the cells. The myoepithelial cells contain actin ﬁlaments lying on the basal membranes of the apocrine gland. There are some considerable histological changes in the presence of the sebaceous and apocrine glands in territorial males in comparison to non-territorial males. The following histological changes associated with occurrence of the sebaceous and apocrine glands have been observed in territorial and non-territorial male blackbucks: (1) increase of size of sebaceous and apocrine glands and (2) increase in density of sebaceous and apocrine glands in territorial males compared to non-territorial males. It is suggested that the higher development (i.e., size) and density of sebaceous and apocrine glands in territorial males could depend on hormone production (i.e., testosterone). Based on the histological observation and the role of sebaceous and apocrine glands in the preorbital gland supported by literature, it is possible to conclude that both territorial and non-territorial blackbuck males may produce pheromonal substances through preorbital gland (secretion) for olfactory communication. Key words: preorbital gland; sebaceous gland; blackbuck; pheromone; endangered species

Introduction be located on different parts of the body, including face, fore and hind leg, neck, chest, shoulder and gen- Olfactory communication is one of the poorly explored ital preputium area. Most scent glands are normally areas of study in ungulates, particularly antelopes and composed of sebaceous and apocrine glands that pro- cervids (Roberts 1998; Arcese 1999; Lawson et al. 2001). duce different odoriferous molecules (Scully et al. 2000). As research on social animals (hierarchical system) pro- For example, in mouse deer Tragulus javanicus Osbeck, gresses, an increasing number of investigations indicate 1765 and T. napu Cuvier, 1822, the intermandibular that many species produce and secrete a wide variety gland contains both types of secretory glands that can of chemical substances, frequently identified as scents. secrete large amounts of lipids, such as methyl ester and Although their precise function is still poorly under- long-chain hydrocarbon acid (Kalina & Adams 1984; stood, these substances have been frequently associ- Agungpriyono et al. 2006); in Japanese serow, the apoc- ated with different forms of olfactory communication rine portion of the infraorbital gland contains large in ungulates: mate recognition (Novotny et al. 1990; amounts of glycoconjugates that are released from the Miller et al. 1998; Rich & Hurst 1999), territory mark- apocrine secretory cells (Atoji & Suzuki 1990). ing (Gosling 1982; Bowyer et al. 1994) and sexual se- All cervids and antelopes possess preorbital organs, lection (Roden et al. 2005; Hemelrijk et al. 2008). which consist of a glandular region in a pouch adjacent Considerable variation and complexity in the to the nasal (medial) corner of the eye (Schaffer 1940; structure of scent glands have been described in differ- Muller-Using & Schloeth 1967). There is no clear ev- ent species of ungulates (Schummer et al. 1981; Bal- idence for role for this preorbital gland across species akrishnan & Alexander 1985). These structures may (Gray et al. 1989). The most frequently reported role

* Corresponding author

c 2011 Institute of Zoology, Slovak Academy of SciencesUnauthenticated Download Date | 9/24/15 10:21 PM Histomorphology of preorbital gland in Antelope cervicapra 371 of preorbital secretions is territorial marking (Gosling the enrichment zone – a central area with trees, grass, food 1987; Gray et al. 1989). In addition to its possible role and water troughs and wooden sheds. Water was offered ad in marking (Clutton-Brock et al. 1982), other functions libitum, whereas food was served twice a day (10.30 am and may exist in red deer (Cervus elaphus L., 1758). Dom- 4.00 pm). inant stags open their preorbital organs when they are It is strictly prohibited to apply invasive methods such as sample collection of tissue and blood for academic investi- fighting (Bartos 1983). Hatlapa (1977) showed that pre- gation on the blackbuck. Only the carcass of the blackbuck is orbital secretion in red deer has a primary function in available for examination. The natural death of male black- establishing mother-offspring bonds. Further, opening buck gave the opportunity for histological examination. Oc- of the preorbital gland in red deer calves has been re- casionally, the death was due to inter-male fighting. ported to be a signal to the mother that her calf is hungry (Wolfel 1983; Bartos et al. 2005). It is reported Social status of male blackbuck that the preorbital glands are usually open during roar- The nomenclature of the male social status is (Mungall ing in red deer stags (Butzler 1974). The expansion of 1977; Hogg & Forbes 1997): (1) harem masters (i.e., territorial) which hold harems, (2) challengers (i.e., predomi- the preorbital gland opening may be an expression of nant males) without their own harems, but they challenge aggressive intent in brow-antlered deer (Blakeslee et al. the harem master and try to hold females, (3) the bach- 1979). The preorbital gland secretions have a mucous elor groups which stay away from the female groups. In- emulsion containing white insoluble material and also dian blackbucks change their social status from ‘bachelor’ volatile and non-volatile organic compounds (Burger et to ‘challenger’ and became ‘harem masters’, but some of al. 1997). the bachelors may never reach the highest social rank during The social activity of the Indian blackbuck An- their lifetime (Mungall 1977). Territorial and non-terriotrial telope cervicapra L., 1758 is similar to that of many males were recognized by morphological features (Fig. 1). African antelopes with regard to territorial males, Sample collection groups of bachelor males and female herds. Adult male Preorbital glands were collected from 18 blackbucks which blackbucks only establish territories that are more con- included each six territorial males 4–7 years old (a), non- sistently occupied year-around (Mungall 1977; Ran- territorial adult males 4–5 years old (b) and non-territorial jitsingh 1989). The males perform scent marking be- sub-adult males 2–3 years old (c) during June 2002– December 2007. The specimens (preorbital gland) were col- haviour with their well-developed preorbital glands, lected with the help of a zoo veterinary surgeon following while in females this behaviour is vestigial or func- standard guidelines of Central Zoo Authority, New Delhi, tionless. Previous behavioural studies of Indian black- and glands were fixed in Bouin’s fluid. buck species indicate the response-guided function of Histological studies the urine and preorbital gland in marking behaviour The histology of the preorbital gland was studied adopting and territorial defence (Bhattacharya & Chattopadhya the routine paraffin method (Humason 1979). After paraffin 1984; Rajagopal & Archunan 2008; Rajagopal et al. embedding, the specimens were sectioned at a thickness 6–8 2010). However, no information is available on the his- µm and stained with Mayer’s acid alum hematoxylin and tology and the functional aspect of this gland in Indian eosin. antelope. Hence, the aim of this study was to carry Measurement of density and diameter of sebaceous and out a detailed histomorphological investigation of the apocrine glands preorbital glands in territorial and non-territorial male Histological parameters such as density of sebaceous and 2 blackbucks. apocrine glands (number of SG or AG/mm ) were measured. In addition, the density and diameter of the sebaceous and apocrine glands were measured by using a cali- Material and methods brated ocular micrometer at × 450 magnification according Study area to the modified method described by Haffner (1998). The study was conducted in the conservation and breeding Data analysis center of Arignar Anna Zoological Park (AAZP) (13◦16 S, The data of the density and diameter of the sebaceous and 79◦54 E. altitude MSL+ 10 m to 100 m) (i.e., Mean Sea apocrine gland were analysed using one factor analysis of Level), Vandalur, Chennai, Tamilnadu, South India. Chen- variance (One-way ANOVA with post hoc test) with SPSS nai has the distinction of having the first zoo in India, which statistical software 11th version (Anova Solutions Inc., Santa was started in 1855. In 1976, the zoo moved to the Vandalur Clara, USA) to compare the density and diameter of the Reserve Forest, an area of about 510 hectares near Chen- sebaceous and apocrine glands in the territorial and non- nai. The habitat of AAZP is considered a tropical evergreen territorial males. scrub, a degraded forest mostly consisting of thorny bushes. Average annual rainfall is about 250 mm. Annual average Results temperatures is 26 ◦C. Morphological observation Study animals The preorbital gland was located below the eye (Fig. 2) Blackbucks were housed in an outdoor enclosure of about 3.5 acres within a dry moat. The blackbuck enclosure consists and measured 2.8–3.5 cm in length, 1.5–1.7 cm in width of three zones: (i) the edge zone – the visitor area in which and 1.0–1.2 cm in depth, and it weighed 8.5–6.5 g in the distance between visitors and the blackbuck is about 7 territorial males (a); 2.0–2.5 cm in length, 0.8–1.5 cm in m, (ii) the rear zone – the access area for zoo employees for width 0.8–1 cm depth, 3.5–5 g weight in non-territorial the purpose of cleaning and feeding (twice daily) and, (iii) males of adult (b) and 2.0–2.5 cm in length, 0.5–1 cm

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Fig. 1. Morphological identiﬁcation of territorial and non-territorial male Indian blackbucks. Face is full black coloured in territorial male (A) compared to non-territorial adult male (B) and sub-adult male (C). The preorbital gland pouch adjacent to the nasal (medial) corner of the eye of territorial male (D), non-territorial adult male (E) and sub-adult male (F) (Photo Credit: T. Rajagopal).

Fig. 3. Bean shape of the preorbital gland in Indian blackbuck.

the skin epidermis and were surrounded by connective tissue containing muscle fibers and blood vessels. The preorbital gland in territorial and non-territorial Fig. 2. Opening of an excretory duct on the Indian blackbuck pre- males shows two glandular components: one display- orbital gland skin surface (arrow). (Photo Credit: T. Rajagopal). ing sebaceous secretory units and the other apocrine secretory units. The sebaceous component consisted of irregularly shaped bulbs, the sudoriferous compo- width, 0.5–0.8 cm depth, 2–3.5 g weight in sub-adult nents showed many glomerular apocrine glands. These males(c).Itisbeanshapedwithanopeningdirectly glands were surrounded by connective tissue and mus- towards the anterior (Fig. 3). The skin surface in the cle fibers. It is interesting to note that the amount of gland was pink in colour, had an oily appearance and sebaceous glandular lobules was very scarce in non- was covered with densely distributed hair. territorial adult (b) and sub-adult males (c). In contrast, the lobules were more abundant and had a larger Histomorphological observation size in territorial males (Fig. 4). Sebaceous glands had In general, the secretory glands were situated under many glandular lobules which were of this modified

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Fig. 4. Histological structure of the preorbital gland in territorial Indian blackbuck males (A), non-territorial adult (B) and sub-adult males (C). E – epidermis, D – dermis, HF – hair follicle, AG – apocrine gland, SG – sebaceous gland, CT – connective tissue. ×50.

Fig. 5. Paraﬃn section stained with hematoxylin and eosin. A – lobules consisting of ordinary sebaceous gland, ×250; B – modiﬁed sebaceous gland, ×250; C – the branched large sebaceous glandular lobules directly open into the skin surface (arrow), ×50; D – the sebaceous glandular lobules open into the hair follicle, ×250.

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Fig. 6. Stratified squamous epithelium of an excretory duct of the sebaceous gland (A), simple alveolar holocrine glandular lobules (B), in sebaceous gland, the fat of the cells is extracted, the cytoplasm becomes honeycombed in appearance (C, D). CC – cuboidal cells, LD – lipid droplets, SA – serous acini, MA – mucus acini. ×250. type, but a minority of holocrine lobules was still seen. ter of the alveoli and became progressively large, and The excretory duct of the larger glands bears an epithe- the cytoplasm was distended with fat droplets. The cells lium resembling the epidermis and was covered by stra- show all gradations of secretory activity from the de- tum corneum. The excretory ducts of the small glands position of single fat globules to the disintegration of are covered by stratified squamous epithelium. the cells. The nuclei shrank in the process and finally The blackbuck had both ordinary and modified disappeared altogether. Cells lost in secretion were re- type of sebaceous glands in the preorbital gland tis- placed by the peripheral cells. When the fat of the cells sue of territorial and non-territorial males (Figs 5A, B). was extracted by means of fluid, the cytoplasm became The ordinary type was only located in the superficial honeycombed in appearance (Figs 6C, D). lobules and their volume was very small compared to The apocrine gland was composed of simple coiled that of the modified sebaceous glands. Secretory acini tubules and it was more abundant in territorial males of the modified sebaceous glands were tear-shaped and (a) than non-territorial adult (b) and sub-adult males very large, as compared to acini in the ordinary type (c). Each tubule exhibited an inner layer of simple and their ducts opened into hair follicles. The modi- cuboidal secretory cells and an outer layer of myoep- fied sebaceous glands consisted of four types of cells: ithelial cells (Fig. 7). The apocrine processes of the se- peripheral cells, differentiating cells, mature cells and cretory cells were large and visible with hematoxylin necrotic cells. The sebaceous glands emptied directly and eosin reaction. Apocrine droplets were found to be on the skin surface and some secretory lobules opened stored in lumina. into the hair follicles (Figs 5C, D). The combined sebaceous alveoli form a kind of excretory duct through Density and diameter of sebaceous (SG) and apocrine which the secretion is discharged into the pouch lu- glands (AG) men (Fig. 6A). The sebaceous gland cells became more The density and diameter of sebaceous and apocrine rounded in shape, with a clearly visible cell membrane glands were found to vary in the preorbital gland of and nucleus (Fig. 6B). The cells were closer to the cen- territorial and non-territorial males. One-way ANOVA

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Fig. 7. The apocrine gland is a simple tubular gland and the secretions are found in the lumen (LU) in territorial Indian blackbuck male (A), shrunk aprocrine gland in adult male (B), this gland is surrounded by collagenous or interlobular connective tissue (ICT) of the hypodermis. The myoepithelial cells (MC) surrounding the apocrine tubules (C). ×250. with post hoc comparison (Duncan Multiple Range that the sebaceous gland in the preorbital gland of the Test) test clearly showed that the density of sebaceous male blackbuck was of a modified type. This type of se- and apocrine glands was significantly (SG: F = 72.73, df baceous gland is similar to the infraorbital gland of the = 2,15; AG: F = 64.84, df = 2,15, P < 0.001) higher in female Japanese serow (Atoji et al. 1989). In addition, it the territorial males (SG: 112.16 units/mm2; AG: 97.66 is reported that the infraorbital gland of Japanese serow units/mm2) followed by non-territorial males of adult shows sexual dimorphism: the male has the ordinary se- (SG: 53.83 units/mm2; AG: 41.50 units/mm2) and sub- baceous gland, whereas in female it is the modified type adult (SG: 36.00 units/mm2; AG: 21.50 units/mm2). (Atoji et al. 1989). By contrast, the infraorbital gland Furthermore, the diameter of sebaceous and apocrine of Formosan serow has both types of sebaceous gland glands varied significantly (One-way ANOVA: SG: F = (Atoji et al. 1996). 14.64, df = 2,15; AG: F = 29.19, df = 2,15, P < 0.001) In many ungulates such as sheep, horse, antelope, in territorial males (SG: 141.91 µm; AG: 134.55µm) cow and few marsupials, apocrine glands are widely dis- than that of non-territorial males of adult (SG: 86.34 tributed and act as scent glands to produce pheromones µm; AG: 62.51µm) and sub-adult (SG: 28.76 µm; AG: (Robertshaw 1987). In the present study, the apoc- 22.24 µm) rine glands frequently appeared between the epider- mal and dermal layers. The myoepithelial cells were Discussion observed in apocrine tubules that showed evidence of apocrine secretion of the secretory cells. Contraction The present study revealed the presence of well devel- of the myoepithelial cells facilitates the movement of oped sebaceous and apocrine glands in the preorbital secretory product into their ducts (Banks 1993). It has gland of territorial and non-territorial male blackbucks. been reported that mammalian apocrine tubular glands The sebaceous gland appeared to be larger than the found in the common integument, scrotal skin and anal apocrine gland. For instance, in species such as mado- sacs produce secretions containing complex glycocon- qua, Madoqua kirkii Günther, 1880 (Richter 1971), jugates with broad functional significance as related to steenbok, Raphicerus campestris Thunberg, 1811 (Co- intraspecific communication, and the signaling of sex- hen & Gerneke 1976), and red duiker, Cephalophus na- ual activity (Meyer et al. 2001; Yasui et al. 2004). It has talensis Smith, 1834 (Mainoya 1978) there is a well de- been shown that the apocrine portion of the infraorbital veloped glandular area, in which the sebaceous gland gland of the Japanese serow secreted large amounts of is significantly larger than the apocrine gland. Light glycoconjugates that were released from secretory cells microscopic observations of the present study showed (Atoji & Suzuki 1990). The findings contrast with a

Unauthenticated Download Date | 9/24/15 10:21 PM 376 T. Rajagopal &G.Archunan previous study by Kurosumi et al. (1984) who reported that there was no apocrine secretion in the dorsal skin of the dog. The apocrine secretion from apocrine sweat glands has been detected in the antebrachial organ of the ring- tailed lemur (Kneeland 1966), the ceruminous gland and axillary gland of humans (Kurosumi & Kawabata 1976; Kurosumi & Kurosumi 1982), the anal scent gland of the woodchuck (Smith & Hearn 1979), the skin of the pig (Gargiulo et al. 1990) and infraorbital gland of Japanese serow (Atoji et al. 1993). The present result suggests that the apocrine gland in the preorbital gland of the blackbuck contributes to the secretion of volatile substances that may be useful in chemical communication in the blackbuck herd. In territorial males, the sebaceous glands are large in size and the ducts have a quite narrow lumen and ramify in a branching, tree-like manner throughout the gland as compared to that of non-territorial males of adult and sub-adult (Fig. 8). Furthermore, the diameter of the apocrine lumen has a larger size in territorial males compared to non-territorial adult and sub- adult males. Similar observation was reported in the skin gland of the male goat (Van Lancker et al. 2005), in the interscapular area (neck region) of nectar feeding bats (Nassar et al. 2008) and in the facial gland of the bat (Caspers et al. 2009) by using histochemical methodology. Schaal (1982) reported that the higher development of the sebaceous gland in the territorial male could depend on the higher social responsibil- ity (dominance hierarchy) / production of testosterone. Jenkinson (1967) found that after sexual maturation of male rats, enlargement of the sebaceous glands was visible and was accompanied by odor production which is concomitant with higher levels of testosterone. In- crease in size and activity of sebaceous glands caused by testosterone has also been demonstrated in the rat (Strauss et al. 1962). There is evidence that androgens produce various eﬀects on the sebaceous glands in mammals. For instance, the male sex hormones have been shown to stim- ulate either sebum production or growth of sebaceous glands in the mouse (Lapiere 1953), Mongolian gerbil (Mitchel 1965), and golden hamster (Hamilton & Mon- tagna 1950). Implantation of testosterone in castrated male rats increased the volume of the glandular cells and their rate of proliferation (Ebling 1975). Morpho- metric evaluation of the volume of sebaceous glands has revealed a striking reduction in the volume of the gland in gonadectomized rats. The administration of testosterone propionate increases the volume more than Fig. 8. The development of sebaceous gland in territorial and twice that of non-castrated control rats (Sauter & Lou non-territorial Indian blackbuck male. More than ﬁve branched 1975). Lopez & Martin (2005) reported that fatty acids sebaceous glands developed in the territorial males (A), double- could be directly involved in odour production in bats. branched sebaceous gland in non-territorial adult males (B), and single-branched sebaceous gland in sub-adult males (C). SGED Miller et al. (1998) revealed that higher levels of andro- – sebaceous gland excretory duct. ×200. gens as well as larger quantities of interdigital glandular fatty acids and ester volatile compounds were noticed in dominant male white-tailed deer during the breed- of the preorbital gland and volume increase in density ing season as compared to the non-breeding season. and diameter of sebaceous and apocrine glands could The present observation suggests that the lipogenesis depend on the testosterone production. It is further

Unauthenticated Download Date | 9/24/15 10:21 PM Histomorphology of preorbital gland in Antelope cervicapra 377 suggested that these glands may produce volatiles (i.e., Bartoš L. 1983. Some observations on the relationship between pheromones) which seem to allow pheromonal commu- preorbital gland opening and social interactions in red deer. 9: / nication in blackbuck. Aggress. Behav. 59–67. DOI: 10.1002 1098/2337(1983)9:1 <59:AID-AB24800901o8>3.0.CO;2-F Precisely, this is the maiden report documenting Bhattacharya T. & Chattopadhya B. 1984. A study on the struc- the histomorphology of the preorbital gland of terri- ture of the social organization of Blackbuck, Antilope cervi- torial and non-territorial male blackbucks. The results capra Linne, in Ballavpur wildlife sanctuary, West Bengal, 22: show that territorial and non-territorial male black- India. Lynx 5–10. Blakeslee C.K., Rice C.G. & Ralls K. 1979. Behaviour and repro- bucks possess sebaceous and apocrine glands in their ductions of captive brown-antlered deer Cervus eldi thamin preorbital gland tissue. However, the oily appearance (Thomas, 1918). Säugetierk. Mitt. 27: 114–127. observed macroscopically on the surface of the preor- Bowyer R.T., Van Ballenberghe V. & Rock K.R. 1994. Scent marking by Alaskan moose: characteristics and spatial dis- bital gland is likely to be the characteristic feature tribution of rubbed trees. Can. J. Zool. 72: 2186–2192. of the secretion from sebaceous and apocrine glands. Burger B.V., Yang T.P., Le Roux M., Brandt W.F., Cox A.J. These observations are in agreement with the previ- & Hart P.F. 1997. Mammalian exocrine secretions. XI. Con- ous report of the delivery of pheromones from seba- stituents of the preorbital secretion of klipspringer, Oreotra- gus oreotragus.J.Chem.Ecol.23: 2383–2400. ceous and apocrine secretion (Kalina & Adams 1984; Butzler W. 1974. Kampf und Paarungsverhalten, sozial Rang- Agungpriyono et al. 2006). Based on the histomorpho- ordung and Aktivitatsperiodik beim Rothirsch. Beiheft Z. logical observation and the role of sebaceous and apoc- Tierpsychol. No. 16, Paul Parey Verlag, Hamburg, Berlin. rine glands in the preorbital gland as documented in Caspers B., Wibbelt G. & Voigt C.C. 2009. Histological exami- nations of facial glands in Saccopteryx bilineata (Chiroptera, literature, it is possible to conclude that the territo- Emballonuridae), and their potential use in territorial mark- rial and non-territorial male blackbucks may produce ing. Zoomorphology 128: 37–43. DOI: 10.1007/s00435-008- pheromonal substances through preorbital gland (se- 0072-6 cretion) for olfactory communication. Clutton-Brock T.H., Guinness F.E. & Albon S.D. 1982. Red Deer, Behaviour and Ecology of Two Sexes. University of Chicago Press, Chicago, IL, 378 pp. Cohen M. & Gerneke D.H. 1976. 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