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THE ROLE OF PHERO MONES IN AN I MAL RE PRO DUC TION – A RE VIEW
A.A. Wani1, S.S. Dhindsa2, T.A. Shafi3, S.R.A. Chowdhary4 and Balwinder Kumar5
1De part ment of Vet er i nary Gy nae col ogy and Ob stet rics, 2, 5De part ment of An i mal Ge net ics and Breed ing,
3De part ment of Vet er i nary Med i cine, 4De part ment of Vet er i nary Phys i ol ogy and Bio chem is try,
Guru Angad Dev Vet er i nary and An i mal Sci ences Uni ver sity, Ludhiana-141004, Punjab, In dia.
Email : shahbazdhindsa76@ya hoo.co.in
ABSTRACT
The pheromones play an important role in animal behavior and reproductive processes.
Pheromones in the urine, feces, or from cutaneous glands can be perceived through the olfactory
system to elicit both behavioral and endocrine responses in various species. These can exert
profound effects on reproductive activity via the hypothalamic system that generates pulses of
gonadotropin-releasing hormone. The role of pheromones in bovine reproduction is not as clearly
defined as that in other species such as sheep, goats and swine. The knowledge acquired on the
effectiveness of biostimulation; the factor which conditions it and the biological mechanism which
produces it in livestock species, allows its use as a breeding management tool. The biostimulation
technique through pheromones, offers a practical way to improve reproductive efficiency of the
domestic animals by enhancing early onset of puberty and reducing postpartum anestrus period.
However, the exact nature of the cues and the role of biostimulation in livestock species especially
swine, sheep, goats and cattle require more attention.
Key Words : Biostimulation, bovine, goat, pheromones, pig, sheep, vomero-nasal or gan.
Animals from same species communicate information
concerning reproduction with each other in order to
co-ordinate reproductive activities. The term
Pheromone was coined by Karlson and Luscher and
the name of first pheromone was proposed as
Bombykal extracted from Honey Bee (Karlson and
Luscher 1959). It is a biologically active substance like
hormone, air borne chemical substance secreted
externally in urine, feces, or by sub-cutaneous glands
and cause specific reactions in a receiving animal. It
causes release of a specific behavior or physiological
changes in recipient’s endocrine or reproductive
system (Izard 1983). Exteroceptive cues that are likely
to play role in male and female interactions include
olfactory, visual, auditory and tactic stimuli (Zalesky et
al., 1984). Extensive studies in insects, rodents, swine,
sheep, goats and cattle have established the
importance of pheromones in the strong influence
exerted by the male on reproductive activity in the
female. It has been demonstrated that the urine of male
mice, rats, feral species and other wild rodents contains
a priming pheromone that is responsible for hastening
puberty in the females. Pheromones in the wool, wax
and urine of a ram are sufficient to stimulate ewes to
ovulate, while the buck has a strong characteristic
seasonal odor. The mere presence of the boar at the
time of insemination of the sow improves sperm
transport and ovulation, while the presence of the
vasectomised bull has been reported to hasten the
onset of puberty in heifers and also early resumption of
ovarian activity in cattle following parturition.
Types of Pheromones
Releaser pheromones
These pheromones elicit an immediate behavioral
response. In the pig, the male stimulates the
immobilization reflex of the sow by using sex
pheromones contained in its saliva. These
pheromones were identified as the steroids
5á-androst-16-en-3-one and 5á- androst-16-en-3á-ol
(Patterson 1966, Patterson 1968), which are
synthesized in the testes and released in boar saliva.
Primer pheromones
These pheromones mediate slow developing and
longer-lasting changes to the endocrine state or
development. In domestic mammals, especially small
ruminants, priming pheromones from the male seems
to have an influence on the induction of puberty, the
termination of seasonal anestrus and shortening of
postpartum anestrus (Gelez and Fabre-Nys 2004).
Pro gres sive Re search 8 (1) : 14-18 (2013) So ci ety for Sci. Dev. in Agric. and Tech.
Signaler pheromones
These pheromones convey the information about the
sender, such as individual or group identity, which are
important for parent-offspring recognition and mate
choice (Pageat and Gaultier 2003, Yamazaki et al.,
2000).
Major urinary proteins (MUPs) and Odorant binding
protein (OBPs)
Major urinary proteins (MUPs) and á2u proteins are
lipocalins that were first described in mouse and rat,
which are synthesized in the liver and excreted in the
urine (Shaw et al., 1983). Their roles are : (1) To
transport the pheromone in biological fluids, (2) To
extend the period of bioavailability of the pheromone by
delaying its liberation, and (3) To modulate the
pheromone activity (Hurst and Beynon 2004). The
odorant binding protein (OBPs) discovered in the nasal
tissues of several vertebrates have strong similarity with
MUPs (Cavaggioni et al., 1987).
Biostimulation in Various Species
Dog and cat
The Perception of pheromones in dog is via vomero
nasal organ (VNO). There are two VNOs situated on
each side of the nasal septum in small fossa. Each VNO
is 4 cm long in the dog (Wada et al., 1991). The suction
of pheromones by VNO follows the flehman or similar
behaviour (raising/movement of upper lip, half open
mouth and movements of the tongue) in dairy animals.
In dog flehman is controversial but shows analogous
behaviour that is panting, raising of upper lip, creasing
the nose or flecking the tongue against papilla.
The expression of flehman induces aspiration of
pheromone into the VNO, where it is mixed with the
mucus. This suction occurs because of vasoconstric-
tion in the wall of the VNO. This increases the diameter
of the lumen of organ and thus creates the fall in
pressure necessary for the suction. The components of
pheromone bind with the pheromone binding proteins
and so can stimulate the receptors located on
membrane of sensory cells (Pageat and Gaultier 2003).
After the suction period the wash out of the VNO
begins. The blood pressure increases and the diameter
of the VNO lumen decreases, thus expelling the mucus.
In cat, five different facial pheromones named F1
to F5 have been isolated from the sebaceous
secretions of cheeks and out of these five types, F2
(Composition: oleic acid, palmitic acid, propanoic acid
and p-hydroxy phenyl acetic acid) has been found to
be involved in sexual marking (MacDonald 1985).
During sexual behaviour male rubs his nose to some
points, around the place where he is with the female
cat and deposits the F2 pheromone. This pheromone
seems to improve the efficiency of sexual display
(Pageat and Gaultier 2003). In the peri-anal area, the
supra-caudal glands are well developed especially in
cat. These consist of high concentration of sebaceous
glands located at the dorsal aspect of the root of tail
(Mac Donald 1985). The sebaceous activity of these
glands is increased during spermatogenesis. Thus,
this secretion is involved in the stimulation of bitch
during sexual display (Pageat and Gaultier 2003). The
circumanal glands include the sebaceous and
modified sweat glands that are disseminated all
around the anus. These glands of male dogs are more
developed and their size increases with age. During
estrus, these glands produce tri-methyl amine rich
secretions in bitches that are highly attractive to male
dogs (Donovan 1969). In bitches during estrus, a
secretion of methyl-dihydroxy benzoate seems to be
highly attractive to male dogs and enhances sexual
excitement. It is interesting to note that this compound
is commonly used as a preservative in many human
cosmetic products. It could be involved in some sexual
behaviour shown by some dogs towards their owners
(Pageat and Gaultier 2003).
Pig
One of the mammalian species in which puberty in
females has been shown to be accelerated by the
presence of the male is the domestic pig. Gilts reared
in confinement that were exposed to a boar reached
puberty at an earlier age than gilts reared without being
exposed to a boar (Books and Cole 1970). The
presence of boars reduces the age of onset of puberty
in gilts and postpartum period in lactating sows
(Kirkwood et al., 1981). The presence of a boar can
accelerate puberty in gilts by about 30 days and also
introduction of boars to gilts at about 190 days of age
(i.e. mean age at puberty) can lead to a marked
The role of pheromones in animal reproduction—A Review 15
synchrony in attainment of the pubertal estrus (Books
and Cole 1970).
The sensory cues involved in the boar’s effect on
puberty are thought to be olfactory cues and that
exposing the gilts to a pen previously occupied by a
boar and presumably permeated with his odor was
effective in inducing early puberty (Signoret and
Lindsay 1982) Apparently, priming pheromones
remaining in the boar’s pen after his removal are
sufficient to induce early puberty. Boar’s presence
provides enough stimulation to overcome some of the
adverse effects of confinement on puberty, lowering
the age at first farrowing, thereby increasing lifetime
productivity (Thomson and Savege). Gilts reaching
early puberty through boar contact have higher
ovulation rates, more estrous cycles therefore higher
reproductive potential than controls (Izard 1983).
Sows go through a period of postpartum anoestrus,
the cause of which is thought to be inhibition of the
synthesis of Luteinizing Hormone (LH) and release of
Follicle Stimulating Hormone (FSH) via the suckling
stimulus. Some researchers have been successful in
reliably inducing estrus in lactating sows by grouping
sows with their litters in the presence of a boar (Izard
1983). Specific boar stimuli are known to be of
importance for the onset of estrus in sows after
weaning (Hughes et al. 1990). It is known that specific
boar stimuli at or around the moment of insemination
can influence reproductive processes such as sperm
transport and ovulation processes and consequently
affect reproductive performance (Soede 1993). This is
an essential management practice in systems of
production that rely on rebreeding at lactation estrus
for efficient operation (Izard 1983). It has also been
hypothesized that the presence of the boar increases
levels of pituitary FSH in lactation and that these
higher FSH at weaning provoke a more rapid onset of
estrus and ovulation. There is a possibility that a
priming pheromone (5á-androstenone) produced by
the boar could shorten the interval between weaning
and breeding (Izard 1983).
Age of the boar has been determined to have an
effect on inducing onset of puberty. Gilts exposed to
either 2 year-old or 11 month-old boars attained
puberty 24 days earlier than gilts exposed to boars
that were 6.5 months of age (Kirkwood et al., 1981).
The inability of young boars to advance puberty in gilts
has been attributed to a lack of production of the
priming pheromone or to a decreased ability to produce
the pheromone as compared to the older boars. There
are age differences in the ability of boars to produce the
gonadal 19-carbon steroids 5á-androstenone and
3á-androstenol (Booth, 1975), as well as age
differences in the morphological and biochemical
development of the sub-maxillary salivary gland from
which priming pheromones are released (Izard 1983).
The primary mechanism initiating onset of puberty in
gilts seems to be the production or release
of pheromone(s) from the boar, which is (are) secreted
in saliva from the sub-mandibular salivary gland
(Kirkwood et al., 1981).
Sheep and goat
Priming pheromones from the ram and buck have been
found to hasten the onset of puberty and estrus in sheep
and goats. “The ram effect” (priming pheromones) has
been reported to accelerate onset of estrus activity and
promote varying degree of estrus synchronization. The
introduction of males before the normal breeding season
hastens the onset of estrus cycle in seasonally anestrus
ewes (Knight et al., 1978). The stimulated ovulation in
ewes following ram introduction were preceded by LH
peaks. This change through olfaction would, suggest the
involvement of the VNO (which has neural connections
with the hypothalamus and is thought to be a mediator of
effects of priming pheromones that influence ovarian
function).
Physical or visual contact may not be necessary for
the ram to induce estrus in ewe. Knight and Lynch
(1980) tested the capacity of ram urine or a combination
of wax, collected from around the eyes and from the
flanks of ram and wool to induce ovulation in ewes early
in breeding season. Urine, wax and wool were as
effective as contact with rams. Similarly, the introduction
of a buck to a group of does resulted in initiation of
synchronized estrus, 5-10 days after onset of exposure
to the buck (Shelton 1960).
Bovine
The role of priming pheromones in bovine reproduction
is not as clearly defined as in sheep, goat and swine
(Robertson et al., 1991). While there are reports
supporting the evidence of priming pheromones or
16 Wani, et al.,
biostimulation in cattle, e.g. the presence of teaser bull
did not hasten puberty in a group of prepubertal heifers
(Berardinelli et al., 1978). Similarly, Wehrman et al.,
(1996) observed that incidence of precocious puberty
in developing beef heifers was not affected by the
presence of bulls. However, it has been reported that
67 per cent of heifers exposed to bull urine (by
oro-nasal treatment i.e. 1 ml of bull urine in each nostril
and 1 ml in oral cavity) and 32 per cent of heifers
exposed to only water attained puberty, supporting the
hypothesis that bull urine contains a priming
pheromone that hastens the onset of puberty in heifers
(Izard and Vandenbargh 1982). Similarly, Robertson et
al., (1991) supported the hypothesis that social
interactions between bulls and prepubertal heifers
results in a decreased age of attainment of puberty. In
another study, it was observed that heifers exposed to
vasectomised bulls attained puberty at 23.1 months,
significantly lower than the age of 26.4 months at onset
of puberty for the non exposed heifers (Rekwot et al.,
2000). The duration of post-partum anestrous in
multiparous cows decreased when cows were exposed
to bulls following parturition (Zalesky et al., 1984). After
bull exposure, interval to estrus was shorter than for
cows isolated from bulls and greater proportion of cows
exhibited estrus by 60-90 days after calving (Custer et
al., 1990). In this study, an increase in progesterone
concentration was observed before first estrus,
whereas LH was not altered by bull exposure
speculating that pre-estrus progesterone rise
associated with bull exposure may be the mechanism
of “bull effect” in postpartum cows. But this does not
preclude the probability that the effect of bull on
resumption of cyclicity is mediated via CNS by
stimulating LH release immediately following exposure.
Acosta et al., (1983) hypothesized that the “bull effect”
acts to increase the sensitivity of the positive feed back
centre for LH release in the hypothalamus to estrogen,
thus overriding inhibitory effects of low concentration of
estrogen on the hypothalamus. Another possible
explanation for this effect may be that stimulus from the
bulls acted directly to alter sensitivity of the ovary to LH
by increasing the number of LH receptors (Custer et al.,
1990).
It seems that cows of average body condition at
calving respond to the presence of bull by having a
shorter duration of postpartum anestrous than they
would have if they were isolated from bulls (Monje et
al., 1983 and Stumpf et al., 1987). Stumpf et al., (1987)
presumed that the presence of bulls stimulated
secretion of LH- releasing hormone in cows of
moderate body conditions.
In conclusion, biostimulation or pheromonal
communication plays an important role in mammalian
reproduction. The role of pheromones in bovine
reproduction is not as clearly defined as that in other
species, possibly due to nutritional and other
environmental stresses. The economic benefits of
using biostimulation through pheromones to enhance
early onset of puberty and the significant reduction of
postpartum anestrus period in domestic animals, may
serve as a management tool in tropical areas, where
livestock production has some constraints.
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18 Wani, et al.,