Abstract
Producers are facing increasing public scrutiny of the methods used in the production of animal products. Concerns over hormone residues in meat and milk may lead to restricted use of exogenous hormones in the reproductive management of farm animals in the future, so it is important to develop non-pharmacological methods of oestrus synchronisation. The ‘male effect’ was first reported in sheep in the 1940s and describes the capacity of the male to increase the secretion of reproductive hormones and induce ovulation in the female. It is widely accepted that olfactory signals (ostensibly ‘pheromones’) are primarily responsible for the profound shift in the activity of the reproductive centres of the female brain, though the chemical nature of this signal is yet to be conclusively identified for either sheep or goats. On the other hand, our understanding of the mechanism through which socio-sexual stimuli stimulate the hypothalamic-pituitary-gonadal axis of females has been greatly improved through a combination of histological, electrophysiological and endocrinological techniques. It is clear that olfactory stimuli from males are primarily transmitted through the main olfactory system, with audio and visual stimuli playing a synergistic but relatively minor role. In spite of over 60 years of research in this field, there are several areas of current and potential research that should improve our understanding of this remarkable phenomenon and its application to farm animal management.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Al-Gubory KH (1998) Effects of the presence of rams during pregnancy on lambing performance in ewes. Anim Reprod Sci 52:205–211
Boukhliq R, Goodman RL, Berriman SJ, Adrian B, Lehman MN (1999) A subset of gonadotropin-releasing hormone neurons in the ovine medial basal hypothalamus is activated during increased pulsatile luteinizing hormone secretion. Endocrinology 140:5929–5936
Brus M, Meurisse M, Franceschini I, Keller M, Levy F (2010) Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horm Behav 58:737–746
Caraty A, Franceschini GE, Hoffman DL (2010) Kisspeptin and the preovulatory gonadotropin-releasing hormone/luteinising hormone surge in the ewe: basic aspects and potential applications in the control of ovulation. J Neuroendocrinol 22:710–715
Chanvallon A, Fabre-Nys C (2009) In sexually naive anestrous ewes, male odour is unable to induce a complete activation of olfactory systems. Behav Brain Res 205:272–279
Chanvallon A, Blache D, Chadwick A, Esmaili T, Hawken PA, Martin GB, Vinoles C, Fabre-Nys C (2010a) Sexual experience and temperament affect the response of Merino ewes to the ram effect during the anoestrous season. Anim Reprod Sci 119:205–211
Chanvallon A, Scaramuzzi RJ, Fabre-Nys C (2010b) Early sexual experience and stressful conditions affect the response of young ewes to the male. Physiol Behav 99:457–465
Chemineau P (1983) Effect on oestrus and ovulation of exposing creole goats to the male at three times of the year. J Reprod Fertil 67:65–72
Clarke IJ (2011) Control of GnRH secretion: one step back. Front Neuroendocrinol 32:367–375
Clarke IJ, Cummins JT (1982) The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinising hormone (LH) secretion in ovariectomized ewes. Endocrinology 111:1737–1739
Cohen-Tannoudji J, Signoret JP (1987) Effect of short exposure to the ram on later reactivity of anoestrous ewes to the male effect. Anim Reprod Sci 13:263–268
Cohen-Tannoudji J, Lavenet C, Locatelli A, Tillet Y, Signoret JP (1989) Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour. J Reprod Fertil 86:135–144
Cohen-Tannoudji J, Einhorn J, Signoret JP (1994) Ram sexual pheromone: first approach of chemical identification. Physiol Behav 56:955–961
Corotto FS, Henegar JR, Maruniak JA (1994) Odor deprivation leads to reduced neurogenesis and reduced neuronal survival in the olfactory bulb of the adult mouse. Neuroscience 61:739–744
Cushwa WT, Bradford GE, Stabenfeldt GH, Berger YM, Dally MR (1992) Ram influence on ovarian and sexual activity in anestrous ewes: effects of isolation of ewes from rams before joining and date of ram introduction. J Anim Sci 70:1195–1200
Delgadillo JA, Gelez H, Ungerfeld R, Hawken PA, Martin GB (2009) The ‘male effect’ in sheep and goats—revisiting the dogmas. Behav Brain Res 200:304–314
Evans AC, Duffy P, Crosby TF, Hawken PA, Boland MP, Beard AP (2004) Effect of ram exposure at the end of progestagen treatment on estrus synchronisation and fertility during the breeding season in ewes. Anim Reprod Sci 84:349–358
Fletcher IC, Lindsay DR (1971) Effect of rams on the duration of oestrous behaviour in ewes. J Reprod Fertil 25:253–259
Fowler CD, Liu Y, Ouimet C, Wang Z (2002) The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51:115–128
Gelez H, Fabre-Nys C (2004) The “male effect” in sheep and goats: a review of the respective roles of the two olfactory systems. Horm Behav 46:257–271
Gelez H, Fabre-Nys C (2006) Neural pathways involved in the endocrine response of anestrous ewes to the male or its odor. Neuroscience 140:791–800
Gelez H, Archer E, Chesneau D, Campan R, Fabre-Nys C (2004a) Importance of learning in the response of ewes to male odor. Chem Senses 29:555–563
Gelez H, Archer E, Chesneau D, Lindsay D, Fabre-Nys C (2004b) Role of experience in the neuroendocrine control of ewes’ sexual behavior. Horm Behav 45:190–200
Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA (2004) A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073–4077
Hamada T, Nakajima M, Takeuchi Y, Mori Y (1996) Pheromone-induced stimulation of hypothalamic gonadotropin-releasing hormone pulse generator in ovariectomized, estrogen-primed goats. Neuroendocrinology 64:313–319
Hawken P (2005) The role of socio-sexual cues in sheep reproduction. PhD thesis, School of Agriculture Food and Rural Development. University of Newcastle, Newcastle upon Tyne, UK
Hawken PA, Beard AP (2009) Ram novelty and the duration of ram exposure affects the distribution of mating in ewes exposed to rams during the transition into the breeding season. Anim Reprod Sci 111:249–260
Hawken PA, Beard AP, O’Meara CM, Duffy P, Quinn KM, Crosby TF, Boland MP, Evans AC (2005) The effects of ram exposure during progestagen oestrus synchronisation and time of ram introduction post progestagen withdrawal on fertility in ewes. Theriogenology 63:860–871
Hawken PAR, Beard AP, Esmaili T, Kadokawa H, Evans ACO, Blache D, Martin GB (2007) The introduction of rams induces an increase in pulsatile LH secretion in cyclic ewes during the breeding season. Theriogenology 68:56–66
Hawken PAR, Evans ACO, Beard AP (2008a) Prior exposure of maiden ewes to rams enhances their behavioural interactions with rams but is not a pre-requisite to their endocrine response to the ram effect. Anim Reprod Sci 108:13–21
Hawken PAR, Evans ACO, Beard AP (2008b) Short term, repeated exposure to rams during the transition into the breeding season improves the synchrony of mating in the breeding season. Anim Reprod Sci 106:333–344
Hawken PAR, Esmaili T, Jorre de St Jorre T, Jorre T, Martin GB (2009a) Do cyclic female goats respond to males with an increase in LH secretion during the breeding season? Anim Reprod Sci 112:384–389
Hawken PAR, Esmaili T, Scanlan V, Blache D, Martin GB (2009b) Can visual or audio-visual stimuli of a prospective mate stimulate an LH response in sheep? Animal 3:690–696
Hawken PAR, Jorre de St Jorre T, Jorre T, Rodger J, Esmaili T, Blache D, Martin GB (2009c) Rapid induction of cell proliferation in the adult female ungulate brain (Ovis aries) associated with activation of the reproductive axis by exposure to unfamiliar males. Biol Reprod 80:1146–1151
Ichimaru T, Takeuchi Y, Mori Y (1999) Stimulation of the GnRH pulse generator activity by continuous exposure to the male pheromones in the female goat. J Reprod Dev 45:243–248
Iwata E, Kikusui T, Takeuchi Y, Mori Y (2003) Substances derived from 4-ethyl octanoic acid account for primer pheromone activity for the “male effect” in goats. J Vet Med Sci 65:1019–1021
Jorre de St Jorre T, Jorre T, Hawken PA, Martin GB (2012) Role of male novelty and familiarity in male induced LH secretion in female sheep. Reprod Fertil Dev 24(4):523–530
Keller M, Baum MJ, Brock O, Brennan PA, Bakker J (2009) The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav Brain Res 200:268–276
Kendrick KM (1991) How the sheep’s brain controls the visual recognition of animals and humans. J Anim Sci 69:5008–5016
Kendrick KM (2008) Sheep senses, social cognition and capacity for consciousness. In: Dwyer CM (ed) The welfare of sheep. Springer, Dordrecht, pp 135–157
Kendrick KM, Atkins K, Hinton MR, Broad KD, Fabre-Nys C, Keverne B (1995) Facial and vocal discrimination in sheep. Anim Behav 49:1665–1676
Kendrick KM, Da Costa AP, Broad KD, Ohkura S, Guevara R, Levy F, Keverne EB (1997) Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res Bull 44:383–395
Kendrick KM, da Costa AP, Leigh AE, Hinton MR, Peirce JW (2001) Sheep don’t forget a face. Nature 414:165–166
Knight TW, Lynch PR (1980a) Source of ram pheromones that stimulate ovulation in the ewe. Anim Reprod Sci 3:133–136
Knight TW, Lynch PR (1980b) The pheromones that stimulate ovulation in the ewe. Proc Aust Soc Anim Prod 13:74–76
Lane EA, Austin EJ, Crowe MA (2008) Oestrous synchronisation in cattle—current options following the EU regulations restricting use of oestrogenic compounds in food-producing animals: a review. Anim Reprod Sci 109:1–16
Larsen CM, Kokay IC, Grattan DR (2006) The presence of a male mouse initiates mitogenesis in the subventricular zone in virgin C57B6 mice. Front Neuroendocrinol 27:80–81
Larsen CM, Kokay IC, Grattan DR (2008) Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice. Horm Behav 53:509–517
Mak GK, Enwere EK, Gregg C, Pakarainen T, Poutanen M, Huhtaniemi I, Weiss S (2007) Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat Neurosci 10:1003–1011
Martin GB, Kadokawa H (2006) “Clean, green and ethical” animal production. Case study: reproductive efficiency in small ruminants. J Reprod Dev 52:145–152
Martin GB, Oldham CM, Cognie Y, Pearce DT (1986) The physiological response of anovulatory ewes to the introduction of rams—a review. Live Prod Sci 15:219–247
Martin GB, Milton JT, Davidson RH, Banchero Hunzicker GE, Lindsay DR, Blache D (2004) Natural methods for increasing reproductive efficiency in small ruminants. Anim Reprod Sci 82–83:231–245
Moncho-Bogani J, Lanuza E, Hernandez A, Noverjarque A, Martinez-Garcia F (2002) Attractive properties of sexual pheromones in mice: innate or learned. Physiol Behav 77:167–176
Mori Y, Tanaka T (1995) Electrophysiological approach to the hypothalamic GnRH pulse generator. J Reprod Fertil Suppl 49:231–243
Mori Y, Nishihara M, Tanaka T, Shimizu T, Yamaguchi M, Takeuchi Y, Hoshino K (1991) Chronic recording of electrophysiological manifestation of the hypothalamic gonadotropin-releasing hormone pulse generator activity in the goat. Neuroendocrinology 53:392–395
Murata K, Wakabayashi Y, Sakamoto K, Tanaka T, Takeuchi Y, Mori Y, Okamura H (2011) Effects of brief exposure of male pheromone on multiple-unit activity at close proximity to kisspeptin neurons in the goat arcuate nucleus. J Reprod Dev 57:197–202
Murtagh JJ, Gray SJ, Lindsay DR, Oldham CM (1984) The influence of the ram effect in 10–11 month old Merino ewes on subsequent performance when introduced to rams again at 15 months. Proc Aust Soc Anim Prod 15:490–493
Ngere LO, Dzakuma JM (1975) The effect of sudden introduction of rams on oestrous pattern of tropical ewes. J Agric Sci 84:263–264
Oakley AE, Clifton DK, Steiner RA (2009) Kisspeptin signaling in the brain. Endocr Rev 30:713–743
Ohkura S, Takase K, Matsuyama S, Mogi K, Ichimaru T, Wakabayashi Y, Uenoyama Y, Mori Y, Steiner RA, Tsukamura H, Maeda KI, Okamura H (2009) Gonadotropin-releasing hormone pulse generator activity in the hypothalamus of the goat. J Neuroendocrinol 21:813–821
Okamura H, Murata K, Sakamoto K, Wakabayashi Y, Ohkura S, Takeuchi Y, Mori Y (2010) Male effect pheromone tickles the gonadotropin-releasing hormone pulse generator. J Neuroendocrinol 22:825–832
Over R, Cohen-Tannoudji J, Dehnhard M, Claus R, Signoret JP (1990) Effect of pheromones from male goats on LH-secretion in anoestrous ewes. Physiol Behav 48:665–668
Parsons SD, Hunter GL (1967) Effect of the ram on duration of oestrus in the ewe. J Reprod Fertil 1967:61–70
Pearce DT, Oldham CM (1983) ‘Ram effect’ in the breeding season. Proc Aust Soc Reprod Biol 15:49
Pearce DT, Oldham CM (1984) The ram effect, its mechanism and application to the management of sheep. In: Lindsay DR, Pearce DT (eds) Reproduction in sheep. Cambridge University Press, Cambridge, pp 27–34
Pearce DT, Oldham CM (1988) Importance of non-olfactory stimuli in mediating ram induced ovulation in the ewe. J Reprod Fertil 84:333–339
Poindron P, Cognie Y, Gayerie F, Orgeur P, Oldham CM, Ravault J-P (1980) Changes in gonadotropins and prolactin levels in isolated (seasonally or lactationally) anovular ewes associated with ovulation caused by the introduction of rams. Physiol Behav 25:227
Rekwot PI, Ogwu D, Oyedipe EO, Sekoni VO (2001) The role of pheromones and biostimulation in animal reproduction. Anim Reprod Sci 65:157–170
Roberts SA, Simpson DM, Armstrong SD, Davidson AJ, Robertson DH, McLean L, Beynon RJ, Hurst JL (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male’s odour. BMC Biol 8:75–96
Romano JE, Christians CJ, Crabo BG (2000) Continuous presence of rams hastens the onset of estrus in ewes synchronized during the breeding season. Appl Anim Behav Sci 66:65–70
Romano JE, Fernandez Abella D, Villegas N (2001) A note on the effect of continuous ram presence on estrus onset, estrus duration and ovulation time in estrus synchronized ewes. Appl Anim Behav Sci 73:193–198
Rosa HJ, Bryant MJ (2002) The ram effect as a way of modifying the reproductive activity in the ewe: a review. Small Rumin Res 45:1–16
Scaramuzzi RJ, Martin GB (2008) The importance of interactions among nutrition, seasonality and socio-sexual factors in the development of hormone-free methods for controlling fertility. Reprod Domest Anim 43(suppl 2):129–136
Smith JT (2009) Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: comparative aspects. Peptides 30:94–102
Smith JT, Clifton DK, Steiner RA (2006) Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 131:623–630
Tsutsui K, Bentley GE, Kriegsfeld LJ, Osugi T, Seong JY, Vaudry H (2010) Discovery and evolutionary history of gonadotropin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J Neuroendocrinol 22:716–727
Ungerfeld R (2007) Socio-sexual signalling and gonadal function: opportunities for reproductive management in domestic ruminants. Soc Reprod Fertil Suppl 64:207–221
Ungerfeld R, Rubianes E (1999) Estrus response to the ram effect in Corriedale ewes primed with medroxyprogesterone during the breeding season. Small Rumin Res 32:89–91
Ungerfeld R, Forsberg M, Rubianes E (2004) Overview of the response of anoestrous ewes to the ram effect. Reprod Fertil Dev 16:479–490
Van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191–198
Vandenbergh JG (1973) Acceleration and inhibition of puberty in female mice by pheromones. J Reprod Fertil Suppl 19:411–419
Veliz FG, Poindron P, Malpaux B, Delgadillo JA (2006) Maintaining contact with bucks does not induce refractoriness to the male effect in seasonally anoestrous female goats. Anim Reprod Sci 92:300–309
Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H (2010) Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci 30:3124–3132
Whitten WK (1956) Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J Endocrinol 13:399–404
Wyatt TD (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol 196:685–700
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Hawken, P.A.R., Martin, G.B. (2013). Socio-Sexual Stimuli and Reproductive Function: Emerging Perspectives of the Male Effect in Sheep and Goats. In: East, M., Dehnhard, M. (eds) Chemical Signals in Vertebrates 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5927-9_32
Download citation
DOI: https://doi.org/10.1007/978-1-4614-5927-9_32
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-5926-2
Online ISBN: 978-1-4614-5927-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)