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*
1
Centre for Pheromone Technology, Department of Animal Science, School of Life Sciences, Bharathidasan University,
Tiruchirappalli-620 024. Tamil Nadu, India; e-mail: [email protected]
2
Department 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
Olfactory communication is one of the poorly explored
areas of study in ungulates, particularly antelopes and
cervids (Roberts 1998; Arcese 1999; Lawson et al. 2001).
As research on social animals (hierarchical system) progresses, an increasing number of investigations indicate
that many species produce and secrete a wide variety
of chemical substances, frequently identified as scents.
Although their precise function is still poorly understood, these substances have been frequently associated with different forms of olfactory communication
in ungulates: mate recognition (Novotny et al. 1990;
Miller et al. 1998; Rich & Hurst 1999), territory marking (Gosling 1982; Bowyer et al. 1994) and sexual selection (Roden et al. 2005; Hemelrijk et al. 2008).
Considerable variation and complexity in the
structure of scent glands have been described in different species of ungulates (Schummer et al. 1981; Balakrishnan & Alexander 1985). These structures may
be located on different parts of the body, including
face, fore and hind leg, neck, chest, shoulder and genital preputium area. Most scent glands are normally
composed of sebaceous and apocrine glands that produce different odoriferous molecules (Scully et al. 2000).
For example, in mouse deer Tragulus javanicus Osbeck,
1765 and T. napu Cuvier, 1822, the intermandibular
gland contains both types of secretory glands that can
secrete large amounts of lipids, such as methyl ester and
long-chain hydrocarbon acid (Kalina & Adams 1984;
Agungpriyono et al. 2006); in Japanese serow, the apocrine portion of the infraorbital gland contains large
amounts of glycoconjugates that are released from the
apocrine secretory cells (Atoji & Suzuki 1990).
All cervids and antelopes possess preorbital organs,
which consist of a glandular region in a pouch adjacent
to the nasal (medial) corner of the eye (Schaffer 1940;
Muller-Using & Schloeth 1967). There is no clear evidence for role for this preorbital gland across species
(Gray et al. 1989). The most frequently reported role
* Corresponding author
c 2011 Institute of Zoology, Slovak Academy of Sciences
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Histomorphology of preorbital gland in Antelope cervicapra
of preorbital secretions is territorial marking (Gosling
1987; Gray et al. 1989). In addition to its possible role
in marking (Clutton-Brock et al. 1982), other functions
may exist in red deer (Cervus elaphus L., 1758). Dominant stags open their preorbital organs when they are
fighting (Bartos 1983). Hatlapa (1977) showed that preorbital secretion in red deer has a primary function in
establishing mother-offspring bonds. Further, opening
of the preorbital gland in red deer calves has been reported to be a signal to the mother that her calf is
hungry (Wolfel 1983; Bartos et al. 2005). It is reported
that the preorbital glands are usually open during roaring in red deer stags (Butzler 1974). The expansion of
the preorbital gland opening may be an expression of
aggressive intent in brow-antlered deer (Blakeslee et al.
1979). The preorbital gland secretions have a mucous
emulsion containing white insoluble material and also
volatile and non-volatile organic compounds (Burger et
al. 1997).
The social activity of the Indian blackbuck Antelope cervicapra L., 1758 is similar to that of many
African antelopes with regard to territorial males,
groups of bachelor males and female herds. Adult male
blackbucks only establish territories that are more consistently occupied year-around (Mungall 1977; Ranjitsingh 1989). The males perform scent marking behaviour with their well-developed preorbital glands,
while in females this behaviour is vestigial or functionless. Previous behavioural studies of Indian blackbuck species indicate the response-guided function of
the urine and preorbital gland in marking behaviour
and territorial defence (Bhattacharya & Chattopadhya
1984; Rajagopal & Archunan 2008; Rajagopal et al.
2010). However, no information is available on the histology and the functional aspect of this gland in Indian
antelope. Hence, the aim of this study was to carry
out a detailed histomorphological investigation of the
preorbital glands in territorial and non-territorial male
blackbucks.
Material and methods
Study area
The study was conducted in the conservation and breeding
center of Arignar Anna Zoological Park (AAZP) (13◦ 16 S,
79◦ 54 E. altitude MSL+ 10 m to 100 m) (i.e., Mean Sea
Level), Vandalur, Chennai, Tamilnadu, South India. Chennai has the distinction of having the first zoo in India, which
was started in 1855. In 1976, the zoo moved to the Vandalur
Reserve Forest, an area of about 510 hectares near Chennai. The habitat of AAZP is considered a tropical evergreen
scrub, a degraded forest mostly consisting of thorny bushes.
Average annual rainfall is about 250 mm. Annual average
temperatures is 26 ◦C.
Study animals
Blackbucks were housed in an outdoor enclosure of about 3.5
acres within a dry moat. The blackbuck enclosure consists
of three zones: (i) the edge zone – the visitor area in which
the distance between visitors and the blackbuck is about 7
m, (ii) the rear zone – the access area for zoo employees for
the purpose of cleaning and feeding (twice daily) and, (iii)
371
the enrichment zone – a central area with trees, grass, food
and water troughs and wooden sheds. Water was offered ad
libitum, whereas food was served twice a day (10.30 am and
4.00 pm).
It is strictly prohibited to apply invasive methods such
as sample collection of tissue and blood for academic investigation on the blackbuck. Only the carcass of the blackbuck is
available for examination. The natural death of male blackbuck gave the opportunity for histological examination. Occasionally, the death was due to inter-male fighting.
Social status of male blackbuck
The nomenclature of the male social status is (Mungall
1977; Hogg & Forbes 1997): (1) harem masters (i.e., territorial) which hold harems, (2) challengers (i.e., predominant males) without their own harems, but they challenge
the harem master and try to hold females, (3) the bachelor groups which stay away from the female groups. Indian blackbucks change their social status from ‘bachelor’
to ‘challenger’ and became ‘harem masters’, but some of
the bachelors may never reach the highest social rank during
their lifetime (Mungall 1977). Territorial and non-terriotrial
males were recognized by morphological features (Fig. 1).
Sample collection
Preorbital glands were collected from 18 blackbucks which
included each six territorial males 4–7 years old (a), nonterritorial adult males 4–5 years old (b) and non-territorial
sub-adult males 2–3 years old (c) during June 2002–
December 2007. The specimens (preorbital gland) were collected with the help of a zoo veterinary surgeon following
standard guidelines of Central Zoo Authority, New Delhi,
and glands were fixed in Bouin’s fluid.
Histological studies
The histology of the preorbital gland was studied adopting
the routine paraffin method (Humason 1979). After paraffin
embedding, the specimens were sectioned at a thickness 6–8
µm and stained with Mayer’s acid alum hematoxylin and
eosin.
Measurement of density and diameter of sebaceous and
apocrine glands
Histological parameters such as density of sebaceous and
apocrine glands (number of SG or AG/mm2 ) were measured. In addition, the density and diameter of the sebaceous and apocrine glands were measured by using a calibrated ocular micrometer at × 450 magnification according
to the modified method described by Haffner (1998).
Data analysis
The data of the density and diameter of the sebaceous and
apocrine gland were analysed using one factor analysis of
variance (One-way ANOVA with post hoc test) with SPSS
statistical software 11th version (Anova Solutions Inc., Santa
Clara, USA) to compare the density and diameter of the
sebaceous and apocrine glands in the territorial and nonterritorial males.
Results
Morphological observation
The preorbital gland was located below the eye (Fig. 2)
and measured 2.8–3.5 cm in length, 1.5–1.7 cm in width
and 1.0–1.2 cm in depth, and it weighed 8.5–6.5 g in
territorial males (a); 2.0–2.5 cm in length, 0.8–1.5 cm in
width 0.8–1 cm depth, 3.5–5 g weight in non-territorial
males of adult (b) and 2.0–2.5 cm in length, 0.5–1 cm
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372
T. Rajagopal & G. Archunan
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.
Fig. 2. Opening of an excretory duct on the Indian blackbuck preorbital gland skin surface (arrow). (Photo Credit: T. Rajagopal).
width, 0.5–0.8 cm depth, 2–3.5 g weight in sub-adult
males (c). It is bean shaped with an opening directly
towards the anterior (Fig. 3). The skin surface in the
gland was pink in colour, had an oily appearance and
was covered with densely distributed hair.
Histomorphological observation
In general, the secretory glands were situated under
the skin epidermis and were surrounded by connective tissue containing muscle fibers and blood vessels.
The preorbital gland in territorial and non-territorial
males shows two glandular components: one displaying sebaceous secretory units and the other apocrine
secretory units. The sebaceous component consisted
of irregularly shaped bulbs, the sudoriferous components showed many glomerular apocrine glands. These
glands were surrounded by connective tissue and muscle fibers. It is interesting to note that the amount of
sebaceous glandular lobules was very scarce in nonterritorial adult (b) and sub-adult males (c). In contrast, the lobules were more abundant and had a larger
size in territorial males (Fig. 4). Sebaceous glands had
many glandular lobules which were of this modified
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Histomorphology of preorbital gland in Antelope cervicapra
373
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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374
T. Rajagopal & G. Archunan
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.
The excretory duct of the larger glands bears an epithelium resembling the epidermis and was covered by stratum corneum. The excretory ducts of the small glands
are covered by stratified squamous epithelium.
The blackbuck had both ordinary and modified
type of sebaceous glands in the preorbital gland tissue of territorial and non-territorial males (Figs 5A, B).
The ordinary type was only located in the superficial
lobules and their volume was very small compared to
that of the modified sebaceous glands. Secretory acini
of the modified sebaceous glands were tear-shaped and
very large, as compared to acini in the ordinary type
and their ducts opened into hair follicles. The modified sebaceous glands consisted of four types of cells:
peripheral cells, differentiating cells, mature cells and
necrotic cells. The sebaceous glands emptied directly
on the skin surface and some secretory lobules opened
into the hair follicles (Figs 5C, D). The combined sebaceous alveoli form a kind of excretory duct through
which the secretion is discharged into the pouch lumen (Fig. 6A). The sebaceous gland cells became more
rounded in shape, with a clearly visible cell membrane
and nucleus (Fig. 6B). The cells were closer to the cen-
ter of the alveoli and became progressively large, and
the cytoplasm was distended with fat droplets. The cells
show all gradations of secretory activity from the deposition of single fat globules to the disintegration of
the cells. The nuclei shrank in the process and finally
disappeared altogether. Cells lost in secretion were replaced by the peripheral cells. When the fat of the cells
was extracted by means of fluid, the cytoplasm became
honeycombed in appearance (Figs 6C, D).
The apocrine gland was composed of simple coiled
tubules and it was more abundant in territorial males
(a) than non-territorial adult (b) and sub-adult males
(c). Each tubule exhibited an inner layer of simple
cuboidal secretory cells and an outer layer of myoepithelial cells (Fig. 7). The apocrine processes of the secretory cells were large and visible with hematoxylin
and eosin reaction. Apocrine droplets were found to be
stored in lumina.
Density and diameter of sebaceous (SG) and apocrine
glands (AG)
The density and diameter of sebaceous and apocrine
glands were found to vary in the preorbital gland of
territorial and non-territorial males. One-way ANOVA
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Histomorphology of preorbital gland in Antelope cervicapra
375
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
Test) test clearly showed that the density of sebaceous
and apocrine glands was significantly (SG: F = 72.73, df
= 2,15; AG: F = 64.84, df = 2,15, P < 0.001) higher in
the territorial males (SG: 112.16 units/mm2 ; AG: 97.66
units/mm2 ) followed by non-territorial males of adult
(SG: 53.83 units/mm2 ; AG: 41.50 units/mm2 ) and subadult (SG: 36.00 units/mm2 ; AG: 21.50 units/mm2 ).
Furthermore, the diameter of sebaceous and apocrine
glands varied significantly (One-way ANOVA: SG: F =
14.64, df = 2,15; AG: F = 29.19, df = 2,15, P < 0.001)
in territorial males (SG: 141.91 µm; AG: 134.55µm)
than that of non-territorial males of adult (SG: 86.34
µm; AG: 62.51µm) and sub-adult (SG: 28.76 µm; AG:
22.24 µm)
Discussion
The present study revealed the presence of well developed sebaceous and apocrine glands in the preorbital
gland of territorial and non-territorial male blackbucks.
The sebaceous gland appeared to be larger than the
apocrine gland. For instance, in species such as madoqua, Madoqua kirkii Günther, 1880 (Richter 1971),
steenbok, Raphicerus campestris Thunberg, 1811 (Cohen & Gerneke 1976), and red duiker, Cephalophus natalensis Smith, 1834 (Mainoya 1978) there is a well developed glandular area, in which the sebaceous gland
is significantly larger than the apocrine gland. Light
microscopic observations of the present study showed
that the sebaceous gland in the preorbital gland of the
male blackbuck was of a modified type. This type of sebaceous gland is similar to the infraorbital gland of the
female Japanese serow (Atoji et al. 1989). In addition, it
is reported that the infraorbital gland of Japanese serow
shows sexual dimorphism: the male has the ordinary sebaceous gland, whereas in female it is the modified type
(Atoji et al. 1989). By contrast, the infraorbital gland
of Formosan serow has both types of sebaceous gland
(Atoji et al. 1996).
In many ungulates such as sheep, horse, antelope,
cow and few marsupials, apocrine glands are widely distributed and act as scent glands to produce pheromones
(Robertshaw 1987). In the present study, the apocrine glands frequently appeared between the epidermal and dermal layers. The myoepithelial cells were
observed in apocrine tubules that showed evidence of
apocrine secretion of the secretory cells. Contraction
of the myoepithelial cells facilitates the movement of
secretory product into their ducts (Banks 1993). It has
been reported that mammalian apocrine tubular glands
found in the common integument, scrotal skin and anal
sacs produce secretions containing complex glycoconjugates with broad functional significance as related to
intraspecific communication, and the signaling of sexual activity (Meyer et al. 2001; Yasui et al. 2004). It has
been shown that the apocrine portion of the infraorbital
gland of the Japanese serow secreted large amounts of
glycoconjugates that were released from secretory cells
(Atoji & Suzuki 1990). The findings contrast with a
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376
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 ringtailed 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 subadult 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 responsibility (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. Increase 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 stimulate either sebum production or growth of sebaceous
glands in the mouse (Lapiere 1953), Mongolian gerbil
(Mitchel 1965), and golden hamster (Hamilton & Montagna 1950). Implantation of testosterone in castrated
male rats increased the volume of the glandular cells
and their rate of proliferation (Ebling 1975). Morphometric 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
twice that of non-castrated control rats (Sauter & Lou
1975). Lopez & Martin (2005) reported that fatty acids
could be directly involved in odour production in bats.
Miller et al. (1998) revealed that higher levels of androgens as well as larger quantities of interdigital glandular
fatty acids and ester volatile compounds were noticed
in dominant male white-tailed deer during the breeding season as compared to the non-breeding season.
The present observation suggests that the lipogenesis
T. Rajagopal & G. Archunan
Fig. 8. The development of sebaceous gland in territorial and
non-territorial Indian blackbuck male. More than five branched
sebaceous glands developed in the territorial males (A), doublebranched sebaceous gland in non-territorial adult males (B), and
single-branched sebaceous gland in sub-adult males (C). SGED
– sebaceous gland excretory duct. ×200.
of the preorbital gland and volume increase in density
and diameter of sebaceous and apocrine glands could
depend on the testosterone production. It is further
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Histomorphology of preorbital gland in Antelope cervicapra
suggested that these glands may produce volatiles (i.e.,
pheromones) which seem to allow pheromonal communication in blackbuck.
Precisely, this is the maiden report documenting
the histomorphology of the preorbital gland of territorial and non-territorial male blackbucks. The results
show that territorial and non-territorial male blackbucks possess sebaceous and apocrine glands in their
preorbital gland tissue. However, the oily appearance
observed macroscopically on the surface of the preorbital gland is likely to be the characteristic feature
of the secretion from sebaceous and apocrine glands.
These observations are in agreement with the previous report of the delivery of pheromones from sebaceous and apocrine secretion (Kalina & Adams 1984;
Agungpriyono et al. 2006). Based on the histomorphological observation and the role of sebaceous and apocrine glands in the preorbital gland as documented in
literature, it is possible to conclude that the territorial and non-territorial male blackbucks may produce
pheromonal substances through preorbital gland (secretion) for olfactory communication.
Acknowledgements
We thank Prof. P. Govindarajalu for reading the manuscript, the Chief Wildlife Warden and the Director of
the Arignar Anna Zoological Park, Vandalur, Chennai,
for permission to carry out this study and Prof. Geetha,
Madras Veterinary College, for the histological study. Dr. K.
Senthilkumar and Dr. P.N. Khan of the AAZP are gratefully
acknowledged for the help in the surgical collection of preorbital gland. This investigation was supported by grants from
the UGC -Rajiv Gandhi National fellowship, DST-FIST and
UGC-SAP, New Delhi.
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Received May 12, 2010
Accepted November 5, 2010
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