Introduction

Livestock productivity in the tropical region is generally low relative to temperate climatic condition, mainly due to nutritional and environmental stresses, which leads to low reproductive efficiency (Fitzpatrick, 1996). Various attempts have been made on the regulation and control of bovine reproduction through the use of hormones and its analogues (Peters and Ball, 1995). Although hormonal treatments are highly effective (Diskin et al., 2002; Patterson et al., 2003), but the growing concern about the clean, green and ethical environment and reduced usage of drugs and exogenous hormones (Martin et al., 2004; Martin, 2009), simultaneously lead to adoption of other managemental tools like socio sexual stimuli for improving reproductive efficiency.

Therefore, harnessing the reproductive potential of livestock species in India may require development of management strategies such as biostimulation to effectively improve reproduction. 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 offers a potentially useful and practical way to improve reproductive efficiency in livestock species in the tropics. Biostimulation proved to be a promising tool in hastening puberty and sexual maturity. Also, in domestic animals, through priming pheromones is helpful on the termination of seasonal anoestrus and shortening of postpartum anestrus. Along with effects on female reproduction this technique is found to enhance male sexual performance by stimulating sexual behavior and endocrine functions of males. Thus understanding the role of pheromones could be of potential economic importance in addressing some of the problems associated with livestock production in the tropics.

What is biostimulation?

Biostimulation is a pheromonal communication which plays an important role in mammalian behavior and reproductive processes. Biostimulation (male or bull effect) is the term coined to describe the stimulatory effect of a male on oestrus and ovulation through genital stimulation, priming pheromones, or other less well-defined external cues (Chenoweth, 1983). It was Heape in year 1901 that performed various researches to define term biostimulation. Biostimulation affects reproductive efficiency by hasetening sexual maturity, ovulation induction, reduction of postpartum anoestrus and also in mating (Burns and Spitzer, 1992).

To study about biostimulation it is utmost important to know about the pheromones and its types. Pheromone is derived from greek word, Pherin- to transfer, Hormones- to stimulate. Pheromones are air-borne chemical substances that are secreted externally by various secretions and cause a specific reaction involving either the release of a specific behaviour or physiological change in the recipient’s endocrine or reproductive system in a receiving individual of the same species (Doty, 1976; Izard, 1983).

Pheromones Type

In mammals, based on function pheromones are of two type’s i.e, signalling and priming pheromones which are thought to act either singly or in combination through olfaction, auditory, visual (sight) or tactile stimuli.

Signalling Pheromones

These are substances that cause an immediate short term behavioural response, invoking a classical stimulus — response paradigm mediated by the central nervous system (Izard, 1983). Usually, this involves an olfactory cue that transfers specific information and consequently elicits a specific behaviour. A very good example of this is flehmen reaction shown by male on receiving various secretion of female like urine or vaginal secretion. These odours are present at oestrus and proestrus but not at any other time (Johns, 1980). Hence prove to be helpful in detection of oestrus in females. These signalling pheromones may have more than one behavioural function in that they can serve as attractants and or inducers of sexual activity (Izard, 1983).

In this context lot of research has been done for improving reproductive efficiency in animals. It has been reported that urine and vaginal mucus of oestrus cows, when rubbed on the vaginal membranes of non-oestrus cows, attracts and stimulates males through olfaction and in addition a volatile odour in the cervico-vaginal mucus of oestrus cows is a source of sexual attraction for males (Hart et al., 1946). Odours probably play a significant role in signalling the reproduction of cows and that the male can use a combination of factors associated with the female to determine if she is receptive, including visual, tactile, auditory and olfactory stimuli (Izard, 1983). The behavioural pattern of males and a possible involvement of the olfactory cues, or pheromonal substances, in a group of oestrus synchronised cows has been established (Masaki and Ohta, 1990). Such mating behaviour of males occurred at about the same time of LH and FSH surge in the partner cows; explaining how males choose their optimum partners from the rest of the oestrus cows. It also appears that males especially boars, rams, bucks and bulls emit a sex attractant which oestrus females can detect (Izard, 1983).

Priming Pheromones

These are substances that cause physiological events either through inhibition or stimulation of endocrine, reproductive and other systems (Izard, 1983). Usually, it involves an olfactory cue that elicits a measurable physiological response. In domestic mammals, priming pheromones from the male have an influence on the induction of puberty, the termination of seasonal anoestrus and shortening of postpartum anoestrus. Recently, priming pheromones from females have been shown to affect ovarian activity in other females of the same species (Izard, 1983).

How it Works?

Pheromones and other allelomimetic cues can exert profound effects on reproductive activity via the hypothalamic system that generates pulses of gonadotropin-releasing hormone. The pheromones are perceived by vomeronasal organ (VNO) located in the nasal cavity in almost all terrestrial vertebrate species. The VNO contains specific neuron receptors which are activated by specific ligand pheromones that stimulate a cascade of neuroendocrine responses. The neuroendocrine response is unique to the specific subpopulation of neuron stimulated in VNO. The effect of pheromone on reproduction is mainly due to the release of luteinizing hormone releasing hormone (LHRH) in the hypothalamus. LHRH acts on pituitary and regulate the pulsatile release of luteinizing hormone (LH). In sheep, a pulse of LH is observed within minutes of the presentation of the anestrus female to the male and this pulsatile secretion of LH remains high for several hours and a preovulatory surge takes place within 36 hours.

Brain

Hypothalamus

FSH & LH

Ovary

Testis

Testosterone

Estrogen

Positive or negative feed back

Positive feed back

The increase in LH secretion is thought to probably stimulate the ovarian secretion of estradiol that via positive feed back effect at the hypothalamic level induces the preovulatory LH surge thus overriding the inhibitory effects of low concentration of estrogen on the hypothalamus (Rekwot et al.,2001) and hence ovulation occur (Signoret et al., 1990).

Role of Biostimulation in Reproduction

Hastening Puberty and Sexual Maturity

In domestic animals, priming pheromones from the male have an influence on the induction of puberty in female (Izard, 1983). Positive effects of biostimulation in cyclic activity of cows have been demonstrated with bulls (Fernandez et al., 1993; Berardinelli and Tauck, 2007), androgenized steer (Ungerfeld, 2009; Fiol et al., 2010b) and androgenized cows (Burns and Spitzer, 1992). Before artificial insemination vasectomised bulls for estrus detection may be an effective management tool to decrease age at puberty. Exposing heifers to vasectomised bulls resulted in puberty at significantly lower age (23.1 months) than non-exposed heifers (26.4 months) (Rekwot et al., 2000a). It has also been reported that 67% of heifers exposed to bull urine and 32% 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 Vandenbergh, 1982b). In small ruminants the “ram effect” or “buck effect” (priming pheromone) reported to hasten the onset of oestrus activity and helpful in oestrus synchronization (Schinckel, 1954 a, b). During normal breeding season the introduction of males enhance the onset of oestrous cycles in seasonally anoestrus ewes (Knight et al., 1978; Pearce and Oldham, 1984) and goats (Shelton, 1960). In swine also the “boar effect” has been well documented. The presence of a boar 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 synchrony in attainment of the pubertal oestrus (Brooks and Cole, 1970). Age of male is also important, gilts exposed to mature boar of 11-24 months attained puberty 24 days earlier than gilts exposed to boars of 6.5 months of age (Kirkwood et al., 1981).

However, several other factors also affect the onset of puberty in heifers includes breed (Arije and Wiltbank, 1971), nutrition and growth rate (Grass et al., 1982) photoperiod, environmental temperature and season (Grass et al., 1982) apart from bull and biostimulation (Izard and Vandenberg, 1982, Roberson et al., 1991).

Intensity of Estrus and Reduction of Postpartum Anoestrus

In domestic animals, priming pheromones from the male have an influence on the termination of seasonal anoestrus and shortening of postpartum anestrus (Izard, 1983). Along with this it is also helpful in increasing the intensity and duration of estrus in animals. Primiparous cow showed longer duration of estrus (23.65 h vs 13.50 h) and more intense heat and also shows more mounting behavior (100% vs 52%) when exposed to male continuously (Khanh et al., 2012). 95% gilts displayed a standing response in the presence of boar and in absence of boar 60%. This effect of the bull on resumption of cyclic ovarian activity is mediated via the central nervous system by stimulating LH release immediately following exposure (Custer et al., 1990). The first increase in progesterone, which indicated onset of oestrous cycles, occurred at 43 versus 63 days postpartum in bull-exposure and no bull-exposure cows, respectively. The same study reported that a higher percentage (89 versus 18%) of cows were oestrual in the bull exposure than no exposure groups, respectively. The effect of a teaser bull on ovarian and behavioural activity of suckling beef cows indicated that in the group with the teaser bull, the proportion of cows in heat and ovulation was higher than in the control group (heat: 67.9 versus 32.7%; ovulation: 73.6 versus 40.4%) (Alberio et al., 1987).

In one study it has been proved that it is not the bulls or cows that produce any effect (Berardinelli et al., 2004), but it is their excretory products responsible for biostimulation (Joshi, 2002). Oro-nasally administered bull urine to cows on day 7 postpartum increased mean LH and FSH serum concentrations within 80 min after exposure (Baruah and Kanchev, 1993). Joshi (2002) showed that cows exposed to the excretory products of bulls resumed ovarian cycling activity earlier after calving than cows not exposed to excretory products of bulls. Tauck et al.(2006) evaluated resumption of cyclic activity in postpartum, anovular, primiparous cows exposed to bulls or to excretory products of bulls. Anestrus postpartum length did not differ between females exposed to males or to excretory products of males, but it was shorter than in non-exposed females. On the other hand, continuous exposure (24 h/d) of primiparous cows to male urine using a urine delivery system during 64 d did not affect postpartum anestrus interval compared to cows not exposed to urine (Tauck and Berardinelli, 2007; Tauck et al., 2006). Tauck et al. (2010b) proposed that the alternation of “stimulation” and “relaxation” periods may be necessary to obtain a positive response to biostimulation. Exposure during 6 or 12 h reduced anestrus postpartum compared to isolated females, but the cumulative proportion of cyclic females at 10 days intervals was greater for females exposed during 12 (h) than during 6 h.

Recently in one study found association of biostimulation and temporary weaning which is helpful in increasing follicular development ovulation synchronisation and, consequently, the pregnancy rate in beef cows (Filho et al., 2015).

Enhance Male Sexual Performance

Pheromones are released by females during estrus, thus signalling the stage of the cycle, and stimulating sexual behavior and endocrine functions of males (Dehnhard and Claus, 1988). Male sexual performance can be improved by various sexual stimulation technique (Mader and Price, 1984; Gonzalez et al., 1991; Rosa et al., 2000; Bailey et al., 2005). Sexual stimulation techniques that improve male sexual performance have been reported in several farm animal species (Mader and Price, 1984; Gonzalez et al., 1991; Rosa et al., 2000; Bailey et al., 2005). Studies have demonstrated that the sudden introduction of oestrous ewes in a group of rams induces certain changes in the behavioural and endocrinological state of the rams, a phenomenon which can be referred to as the ‘female effect’. Sexual interaction of males with females tend to increase the plasma levels of testosterone which further associated with rapid rise in LH level and related to a rapid elevation of LH concentration in a variety of species (Hemsworth et al., 1981; Gonzalez et al., 1991; Rosa et al., 2000) which is responsible for libido in males. In one study it was found that the bulls show improved sexual behaviour like sexual aggressiveness (SA) after application of cervical mucus (3.44±0.063) and pherobull (3.45±0.060) as compared to control (2.56±0.061) in adult Sahiwal bulls. Reaction time decreased significantly (p<0.01) in cervical mucus group (207.23±23.33 sec.) and pherobull group (212.45±25.85 sec.) as compared to control group (332.19±32.12 sec.).Further libido score improved significantly (P<0.01) in cervical mucus group (36.51±1.67%) and pherobull group (37.94±1.85%) as compared to control group (25.77±1.20%) (Singh , 2014).The duration of flehmen behaviour and number of mounts of bulls was significantly higher when exposed to the mixture of three synthetic compounds i.e, acetic acid, propionic acid, and 1-iodo undecanethane found in faeces of Bos Taurus than that of individual compounds. Behavioural investigations demonstrated that 1-iodo undecane is primarily involved in attracting the bull whereas acetic acid and propionic acid acts as mounting pheromone in cow (Sankar and Archunan, 2008). Age of male is also one of the important factors for producing effects in an individual. Lunstra (1986) suggested that young, inexperienced bulls must undergo a learning process and (or) acclimation with females and behavior testing paradigms before they exhibit stable reproductive behaviors. Couttie and Hunter (1956) suggested that when young bulls were reared in isolation, many failed to respond or showed less interest in mounting when first exposed to estrual females compared to bulls raised with females. Exposure of ram lambs to ewes during the post-weaning prepubertal period enhanced their sexual performance (Katz et al.,1988). Yearling rams kept close to ewes in oestrus for 6 months found to have larger testes, higher plasma testosterone levels and greater sexual activity than control rams isolated from ewes (Illius et al., 1976).

Exposure to estrual females, viewing copulating herd mates and periodical change of females have been reported to enhance male sexual performance in several species (Mader and Price, 1984; Rosa et al., 2000; Silvestre et al., 2004).Exposure time of females and change of females is also responsible for producing effect in males. In sheep, exposing sexually satiated males to new, unmated, estrous females restores their sexual performance up to 95% of the original ejaculation rate (Pep-elko and Clegg, 1965). Also, in rams, the reaction time was restored when a new female stimulus was presented (Pepelko and Clegg, 1965). Therefore, changing the stimulus female found to shorten the sexual reaction time of males of several species (Thiery and Signoret, 1978) and increase in number of mounts which is indicative of high libido.

Effect on Semen Biology

There is effect of new female stimulus on semen variables which depends on degree of sexual satiation. It was reported that changing the female stimulus after the first ejaculation, semen volume was notably increased (Prado et al., 2003). But semen volume and sperm number decrease as the numbers of successive collections increase (Amir et al., 1986). It has been reported that rams were stimulated with physical contact of a ewe in estrus; an acute increase in semen volume was evident on day 1. These effects were not evident on subsequent days and thus the overall benefits on ram libido and semen quality of exposing rams to ewes in estrus are minimal (Fahey et al., 2012 ).Concerning other semen characteristics, such as motility and live sperm rate, no references were found in the literature on caprine species.

It is reported that boars in contact with the 92- h sows groups produced semen with the highest semen quality and quantity.  Ejaculates collected at the 96-h sow intervals had larger volumes, sperm motility, progressive sperm movement, live sperm, sperm concentration per milliliter, total sperm per ejaculate and normal acrosome morphology than ejaculates collected on the 24-h intervals (Umesiobi, 2010).

Chemical Compound Present in Various Secretory or Excretory Products

The chemical identities of some biostimulatory substances in various secretory and excretory products of different animals have been explored in recent years. The identity of bovine urinary cues is not yet explored fully. Some of the chemical compounds and there function is presented in Table below.

Table: Various chemical compounds in various secretory and excretory products

However, further studies are needed on bioassay and behavioural aspect of these pheromonic compounds in farm animals. The specific urinary compounds after knowing the chemical properties can be purified from urine or prepared synthetically for induction of estrus cyclicity in heifers and postpartum cows.

Conclusion

Biostimulation or pheromonal communication plays an important role in mammalian behaviour and reproductive processes. Pheromones in the urine, feces, or from cutaneous glands can be perceived through the olfactory system to elicit both behavioural and endocrine responses in conspecifics. Bio stimulation can exert profound effects on reproductive activity via the hypothalamic system that generates pulses of gonadotropin-releasing hormone. Biostimulation have effect on both male and female. In females it is helpful in hastening puberty and sexual maturity, termination of seasonal anoestrus and shortening of postpartum anoestrus. Effect on male is on improvement of sexual performance and semen characteristics.

The economic benefits of using biostimulation through pheromones to enhance early onset of puberty and the significant reduction of postpartum anoestrus in domestic animals, may serve as a management tool in India, where livestock production has some constraints. The biostimulation technique offers a potentially useful and practical way to improve reproductive efficiency in livestock species. The exact nature of the cues and the role of bio stimulation livestock species especially swine, sheep, goats and cattle require more attention for better productivity. Therefore, studies are needed on bioassay and behavioural aspect of these pheromonic compounds in farm animals.

Conflict of Interest Statement

The authors do not have any conflict of interest.

References

1. Alberio RH, Schiersmann G, Caron N and Mestre J 1987. Effect of a teaser bull on ovarian and behavioural activity of suckling beef cows. Animal Reproduction Science 14: 263–268.
2. Amir D, Gacitua H, Ron M. and Lehrer AR. 1986. Seasonal variation in semen characteristics and the fertility of Finn cross rams subjected to frequent ejaculation. Animal Reproduction Science. 10: 75–84.
3. Archunan G and Kumar R 2012. 1-Iodoundecane, an Estrus Indicating Urinary Chemo signal in Bovine (Bos Taurus). Journal Veterinary Science and Technology. 3-4.
4. Arije GF, and Wiltbank JN. 1971. Age and weight at puberty in Hereford heifers. Animal Science. 33: 401-406.
5. Bailey JD, Anderson LH and Schillo KK 2005. Effects of novel females and stage of the estrous cycle on sexual behaviour in mature beef bulls. Journal of Animal Science, 83: 613-624.
6. Baruah KK, and Kanchev LN 1993. Hormonal responses to olfactory stimulation with bull urine in postpartum dairy cows. Proceeding VII World Conference Animal Production 3: 356–359.
7. Berardinelli JG, Joshi PS and Tauck SA 2004. Breeding performance of first–calf suckled beef cows exposed to familiar or unfamiliar bulls using a modified co-synch protocol. Postpartum interval in first calf suckled beef cows exposed to familiar or unfamiliar bulls. Proceedings of Western Animal Sciences 55: 291–93.
8. Berardinelli JG, and Tauck SA 2007. Intensity of the biostimulatory effect of bulls on resumption of ovulatory activity in primiparous, suckled, beef cows. Animal Reproduction Science. 99: 24-33
9. Brooks PH and Cole DL 1970. The effect of the presence of a boar on the attainment of puberty in gilts. JOURNAL Reproduction Fertility. 23: 435–440.
10. Burns PD, Spitzer JC, 1992. Influence of biostimulation on reproduction in postpartum beef cows. JOURNAL Animal Science. 70: 358–362.
11. Chenoweth PJ, 1983. Reproductive management procedures in control of breeding. Australian Journal of Animal Production. 15: 28–33.
12. Couttie MA, and Hunter WK 1956. Sexual behaviour of Aberdeen Angus bulls.Proc. 3rd Int. Cong. Animal Reprod. Cambridge, England. 3:98.
13. Custer EE, Berardinelli JG, Short RE, Wehrman M and Adair R 1990. Postpartum interval to oestrus and patterns of LH and progesterone in first-calf suckled beef cows exposed to mature bulls. JOURNAL Animal Science. 68: 1370–1377.
14. Dehnhard M and Claus R 1988. Reliability criteria of a bioassay using rats trained to detect estrus-specific odour in cow urine. Theriogenology 30(6): 1127-1138.
15. Diskin MG, Austin EJL and Roche JF 2002. Exogenous hormonal manipulation of ovarian activity in cattle. Domestic Animal Endocrinology 23(1–2): 211–228.
16. Dorries KM, Adkins-Regan E and Halpern BP 1997. Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs. Brain Behavioural Evolution. 49: 53–62.
17. Doty RL 1976. Mammalian Olfaction, Reproductive Processes and Behaviour. Academic Press, New York, USA
18. Fahey AG, Duffy P and Fair S 2012. Effect of exposing rams to a female stimulus before semen collection on ram libido and semen quality. Journal of Animal Science. 90: 3451-3456.
19. Fernandez D, Berardinelli, JG, Short RE and Adair R 1993. The time required for the presence of bulls to alter the interval from parturition to resumption of ovarian activity and reproductive performance in first-calf suckled beef cows. Theriogenology. 39: 411-419.
20. Filho MLS, Bezerra, LR, Ferreira-Silva, JOURNAL C, Souto FMPP, Oliveira NRP, de Lima PF, Bartholomew CC and de Oliveira MAL 2015. Influence of biostimulation and temporary weaning on follicular dynamics and pregnancy rates in Nelore cows (Bos taurus indicus). Tropical Animal Health andProduction. 47: 1285–1291
21. Fiol C, Quintans G and Ungerfeld R 2010b. Response to biostimulation in peri-puberal beef heifers: influence of male-female proximity and heifer‟s initial body weight. Theriogenology. 74: 569-575.
22. Fitzpatrick LA 1996. Advances in the understanding of postpartum anoestrus in Bos indicus cows. In: Proceedings of the Final Co-ordinated Meeting of IAEA Held in Vienna, Austria.
23. Gonzalez R, Orgeur P, Poindron P and Signoret JP 1991. Female effect in sheep. I. The effect of sexual receptivity of female and the sexual experience of rams. Reproduction Nutr. Dev. 31: 97-102.
24. Grass, JA, Hansen PL and Rutlaedge ER 1982. Genotype X environmental interactions on reproductive traits of bovine females. I. Age at puberty as influenced by breed, breed of sire, dietary regimen and season. Journal of Animal Science 55: 1441–1456.
25. Hart GW, Mead SW and Reagan WM 1946. Stimulating the sex drive of bovine males in artificial insemination. Endocrinology 39: 221–227.
26. Hemsworth PH, Winfield CG and Chamley WA 1981. The influence of the presence of the female on the sexual behaviour and plasma testosterone levels of the mature male pigs. Animal Production. 32: 61-65.
27. Illius AW, Haynes NB and Lamming GE 1976. Effect of ewe proximity on peripheral plasma testosterone levels and behaviour in the ram. Journal of Reproduction and Fertility 48: 25–32.
28. Izard MK and Vandenbergh, JG 1982b. The effects of bull urine on puberty and calving date in crossbred beef heifers. JOURNAL Animal Science 55: 1160–1168.
29. Izard MK 1983. Pheromones and reproduction in domestic animals. In: Vandenbergh, JOURNALG. (Ed.) Pheromones and Reproduction in Mammals. Academic Press, New York, pp. 253–285.
30. Johns MA 1980. The role of vomeronasal system in mammalian reproductive physiology. In: Muller-Schwarz D, Silverstein RM. (Eds.), Chemical Signals, Vertebrates and Aquatic Invertebrates. Plenum Press, New York, pp. 341–364.
31. Joshi PS 2002. ‘Biostimulatory effect of bull: exposure type and day of exposure on resumption of postpartum ovarian cycling activity in first calf suckled beef cows.’ M.S. Thesis submitted to Montana State University
32. Katz LS, Price EO, Wallach SJR and Zenchak JJL 1988. Sexual performance of rams reared with or without females after weaning. Journal of Animal Science 66: 1166–1173.
33. Khanh NP, Roshnina Y, Omar MS, Dhaliwal GK, Wahid H, Khumran AM, Yap KC, Fahmi and Azmil A 2012. Effects of Biostimulation on Oestrus Behaviour, Ovulation time and Conception rate in Primiparous and Multiparous Beef cows. Journal of Animal and Veterinary Advances 11(3): 303-411.
34. Kirkwood RN, Forbes, JM and Hughes PE 1981. Influence of boar contact on attainment of puberty in gilts after removal of the olfactory bulbs. Journal of Reproduction and Fertlity 61: 193–198.
35. Knight TW, Peterson AJ and Payne E 1978. The ovarian and hormonal response of the ewe to stimulation by the ram early in the breeding season. Theriogenology 10: 343–353.
36. Lunstra DD 1986. Libido and serving capacity of beef bulls. Symposium on Male Fertility, Beef Improvement Federation Annual Convention: 20-36.
37. Mader DR and Price EO 1984. The effects of sexual stimulation on the sexual performance of Hereford bulls. Journal of Animal Science 59: 294
38. Martin GB 2009. The “Cleen, Green and Ethical” Concept in Animal Production. Agrociencia. XIII, Nº 3: 1-7.
39. Martin GB, Milton, JTB, Davidson RH, Banchero Hunzicker GE, Lindsay DR and Blache D 2004. Natural methods for increasing reproductive efficiency in small ruminants. Animal Reproduction Science. 83: 231-245.
40. Masaki, J and Ohta M 1990. Mating behaviour of a bull for oestrus synchronised cows and a possible involvement of pheromonal factors. In: Sagara Y, Seto K. (Eds.), Pheromones and Reproduction. The Parthenon Publishing Group Limited, Carnforth, UK, pp. 63–75.
41. Patterson D, JOURNAL, Kojima FN and Smith MF 2003. A review of methods to synchronize estrus in replacement beef heifers and postpartum cows. Journal of Animal Science. 81:166-177.
42. Pearce DT and Oldham CM 1984. The ram effect, its mechanism and application to the management of sheep. In: Lindsay DR, Pearce DJ (Eds.), Reproduction in Sheep. Australian Academy of Science, Australian Wool Corporation, Canberra, pp. 26–34.
43. Pepelko EW and Clegg T 1965. Studies of mating behaviour and some factors influencing the sexual response in the male sheep Ovis aries. Animal Behav. 13: 249–257.
44. Peters AR and Ball PH 1995. The ovarian cycle. In: Peters, AR, Ball, PH (Eds.), Reproduction in Cattle. Blackwell Science, UK, pp. 21–46.
45. Prado V, Orihuela A, Lozano S and Perez-Leon I 2003. Effect on ejaculatory performance and semen parameters of sexually-satiated male goats (Capra hircus) after changing the stimulus female. Theriogenology 60: 261–267.
46. Sankar R, Archunan G and Habara Y 2007. Detection of oestrous-related odour in bovine (Bos taurus) saliva: bioassay of identified compounds. Animal 1:9, 1321–1327
47. Rameshkumar K and Archunan G (2002). 1-iodo undecane:an effective sex attractant from bovine estrus urine. In: Proceedings of the XX Symposium on Reproduction Biol. Comp. Endocrinol, pp. 133–134.
48. Rekwot PI, Ogwu D and Oyedipe EO 2001. The role of pheromones and biostimulations in animal reproduction. Animal Reproduction Science 65: 157–170.
49. Rekwot PI, Ogwu D, Oyedipe EO and Sekoni VO 2000a. Effects of bull exposure and body growth on onset of puberty in Bunaji and Friesian × Bunaji heifers. Reproduction Nutr. Dev. 40: 1–9.
50. Roberson MS, Wolfe MW, Stumpf TT, Werth LA, Cupp AS, Kojima ND, Wolfe PL, Kittok RJ and Kinder JE 1991. Influence of growth rate and exposure to bulls on age at puberty in beef heifers. Journal of Animal Science 69: 292–298.
51. Rosa HJ, Juniper DT and Bryant MJ 2000. The effect of exposure to oestrous ewes on rams sexual behaviour, plasma testosterone concentration and ability to stimulate ovulation in seasonally anoestrous ewes. Applied Animal Behaviour Science. 67: 293-305
52. Rajanarayanan A, Archunan G 2011. Identification of urinary sex pheromones in female buffaloes and their influence on bull reproductive behaviour. Research in Veterinary Science 91: 301–305
53. Sankar R and Archunan G 2008. Identification of putative pheromones in bovine (Bos taurus) faeces in relation to estrus detection. Animal Reproduction Science 103: 149–153.
54. Sankar R and Archunan G 2011. Gas Chromatographic/Mass Spectrometric Analysis of Volatile Metabolites in Bovine Vaginal Fluid and Assessment of Their Bioactivity International Journal of Analytical Chemistry.
55. Schinckel PG 1954a. The effect of the ram on incidence and occurrence of oestrus in ewes. Australian Veterinary Journal 30: 189–195.
56. Schinckel PG 1954b. The effect of the presence of the ram on the ovarian activity of the ewe. Australian Journal of Agriculture. Science 5: 456–469
57. Shelton M 1960. Influence of the presence of a male goat on the initiation of oestrous cycling and ovulation of Angora does. Journal of Animal Science 19: 368.
58. Signoret, JP, Martinat-Botte F, Botte F, Bauteau F, Forgerit Y, Maear C, Moreau A and Terqui M 1990. Control of oestrus in gilts I. Management-induced puberty. Animal Reproduction Science 22(3): 221-225.
59. Silvestre MA, Salvador L, Sanchez, JP and Gómez EA 2004. Effect of changing female stimulus on intensive semen collection in young Murciano-Granadina male goats. Journal of Animal Science, 82: 1641-1645.
60. Singh S 2014. Selected management intervention and biostimulation to augument libido and sperm production in Sahiwal bulls. M.V.Sc Thesis, National Dairy Research Institute, Karnal, Haryana, India.
61. Tauck SA and Berardinelli, JOURNALG 2007. Putative urinary pheromone of bulls involved with breeding performance of primiparous beef cows in a progestin-based estrous synchronization protocol. Journal of Animal Science. 85: 1669-1674.
62. Tauck SA, Berardinelli, JOURNALG, Geary TW and Johnson N JOURNAL 2006. Resumption of postpartum luteal function of primiparous, suckled beef cows exposed continuously to bull urine. Journal of Animal Science. 84: 2708-2713.
63. Tauck SA, Olsen, JR, Wilkinson, JR C and Berardinelli, JG 2010b. Duration of daily bull exposure on resumption of ovulatory activity in postpartum, primiparous, suckled, beef cows. Animal Reproduction Science. 118: 13-18.
64. Thiery, JC and Signoret PJ 1978. Effect of changing the teaser ewe on the sexual activity of the ram. Applied Animal Ethology 4: 87-90.
65. Umesiobi DO 2010. Boar effects and their relations to fertility and litter size in sows. South African Journal of Animal Science 40 (5): Supplement 1.
66. Ungerfeld R 2009. Short-term exposure of high body weight heifers to testosterone-treated steers increases pregnancy rate during early winter bull breeding. Animal Reproduction. 6 (3): 446-449.