Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Nutritional and environmental effects on reproduction in small ruminants

G. B. Martin A B C , J. Rodger A and D. Blache A
+ Author Affiliations
- Author Affiliations

A School of Animal Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, WA 6009, Australia.

B CRC for Plant-based Management of Dryland Salinity, University of Western Australia, Crawley, WA 6009, Australia.

C To whom correspondence should be addressed. email: gmartin@agric.uwa.edu.au

Reproduction, Fertility and Development 16(4) 491-501 https://doi.org/10.1071/RD04035
Accepted: 23 March 2004   Published: 6 July 2004

Abstract

Animals live in environments that are both complex and continually changing, so they have to respond to short- and long-term variations in a wide range of factors, such as photoperiod, nutrition and sociosexual signals. Before they were domesticated, animals developed reproductive strategies that coped with these changes and often took advantage of them. The physiological processes that implement these strategies have been modified to some extent during several millennia of controlled breeding, but most persist. Thus, many genotypes still exhibit profound responses to external inputs, such as the induction of ovulation by sociosexual signals and the doubling of litter size by a change in nutrition. The complexity in these responses is now becoming clearer. For example, with sociosexual signals, we now need to consider the stimulatory effects of males on females, of females on males and of females on females. Similarly, the impact of nutrition has been extended beyond the control of puberty and the production of gametes to include phenomena such as ‘fetal programming’, with its potentially profound effects on the life-long performance of the animals. Fortunately, our capacity to research these phenomena has been greatly enhanced by technical improvements in hormone assays, molecular and cellular biology, and real-time ultrasound. This has brought us a better understanding of several of the environmental influences on reproduction, including: the cellular processes within ovarian follicles that mediate the effect of nutrition on ovulation rate; the neuroendocrine pathways through which nutritional inputs affect the brain centres that control appetite and reproduction; and the intracerebral pathways through which sociosexual signals (olfactory and non-olfactory) stimulate the reproductive axis. Importantly, we are now beginning to realise that, as well as considering interactions between environmental inputs and genotype, we need to take into account interactions between the environmental factors themselves, just as the animals do. We still have a long way to go for a complete understanding, but we are nevertheless in a position where we can begin to use this information to develop new management systems for our animals to improve their productivity.

Extra keywords: female effect, fetal programming, male effect, pheromone, season.


Acknowledgments

For the discussion that led to many of these ideas, we thank our colleagues, particularly Lorenzo Álvarez, Rex Scaramuzzi, John Milton and Carolina Viñoles. Much of the work from our laboratory was funded through the Australian Research Council and the National Health and Medical Research Council of Australia.


References

Allen, D. M. , and Lamming, G. E. (1961). Nutrition and reproduction in the ewe. J. Agric. Sci. 56, 69–79.


Álvarez, R. L. (2000). Efecto de la anosmia y la conducta social sobre la secreción de LH y ovulación de cabras anéstricas inducidas a ciclar mediante el efecto hembra. MSc Thesis. (Universidad Nacional Autónomo de México: Mexico.)

Álvarez, R. L. , and Zarco, Q. L. (2001). Los fenómonos de biostimulatión sexual en ovejas y cabras.  Vet. Méx. 32, 117–129.


Álvarez, R. L. , Ducoing, W. A. E. , Zarco, Q. L. , and Trujillo, G. A. M. (1999). Conducta estral, concentraciones de LH y función lútea en cabras en anestro estacional inducidas a ciclar mediante el contacto con cabras en estro.  Vet Méx. 30, 25–31.


Álvarez, L. , Martin, G. B. , Galindo, F. , and Zarco, L. A. (2003). Social dominance of female goats affects their response to the male effect. Appl. Anim. Behav. Sci. 84, 119–126.
Crossref | GoogleScholarGoogle Scholar |

Banchero, G. E., Quintans, G., Milton, J. T. B., and  Lindsay, D. R. (2002). Supplementation of Corriedale ewes with maize during the last week of pregnancy increases production of colostrum. In ‘Proceedings of the Australian Society of Animal Production Vol. 24’.  pp. 273. (Australian Society of Animal Production: Melbourne, Australia.)

Banchero, G. E., Vazquez, A.,, Gigena, F., Quintans, G., Lamanna, A., Lindsay, D. R., and  Milton, J. T. B. (2004). Supplementation of ewes with maize or barley during the last week of pregnancy doubles production of colostrum. In ‘Proceedings of the 15th International Congress on Animal Reproduction, Porto Seguro, Brazil, August 2004’. (Brazilian College of Animal Reproduction: Belo Horizonte, Brazil.) (In press)

Bartlewski, P. M. , Beard, A. P. , Cook, S. J. , and Rawlings, N. C. (2002). Ovarian activity during sexual maturation and following introduction of the ram to ewe lambs. Small Ruminant Res. 43, 37–44.
Crossref | GoogleScholarGoogle Scholar |

Bell, A. W. (1984). Factors controlling placental and fetal growth and their effects on future production. In Reproduction in sheep (Ed D. R. Lindsay D. T. Pearce)  pp. 144–152. (Australian Academy of Sciences: Canberra, Australia.)

Blache, D. and  Martin, G. B. (1995). Neural and endocrine mechanisms underlying the synchrony of sexual behaviour and ovulation in the sheep. In ‘Oxford Reviews of Reproductive Biology. Vol. 17’. (Ed H. M. Charlton)  pp. 205–254. (Oxford University Press: New York, USA.)

Blache, D. , Chagas, L. , Blackberry, M. A. , Vercoe, P. E. , and Martin, G. B. (2000). Metabolic factors affecting the reproductive axis in male sheep. J. Reprod. Fertil. 120, 1–11.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Blache, D. , Adam, C. L. , and Martin, G. B. (2002). The mature male sheep: a model to study the effects of nutrition on the reproductive axis. Reprod. Suppl. 59, 219–233.
PubMed |

Blache, D. , Zhang, S. , and Martin, G. B. (2003). Fertility in males: modulators of the acute effects of nutrition on the reproductive axis of male sheep. Reprod. Suppl. 61, 387–402.
PubMed |

Blanc, F. , Martin, G. B. , and Bocquier, F. (2001). Modelling reproduction in farm animals: a review. Reprod. Fertil. Dev. 13, 337–353.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Bloomfield, F. H. , Oliver, M. H. , Hawkins, P. , Campbell, M. , Phillips, D. J. , Gluckman, P. D. , Challis, J. R. G. , and Harding, J. E. (2003). A periconceptional nutritional origin for noninfectious preterm birth. Science 300, 606.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Booth, K. K. , and Katz, L. S. (2000). Role of the vomeronasal organ in neonatal offspring recognition in sheep. Biol. Reprod. 63, 953–958.
PubMed |

Boukhliq, R. , Martin, G. B. , White, C. L. , Blackberry, M. A. , and Murray, P. J. (1997). Role of glucose, fatty acids and protein in the regulation of testicular growth and the secretion of gonadotrophin, prolactin, somatotrophin and insulin in the mature ram. Reprod. Fertil. Dev. 9, 515–524.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Boukhliq, R. , Goodman, R. L. , Berriman, S. J. , Adrian, B. , and Lehman, M. N. (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.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Bronson, F. H. (1985). Mammalian reproduction: an ecological perspective. Biol. Reprod. 32, 1–26.
PubMed |

Carlen, M. , Cassidy, R. , Brismar, H. , Smith, G. A. , Enquist, L. W. , and Frisen, J. (2002). Functional integration of adult-born neurons. Curr. Biol. 12, 606–608.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Clark, R. T. (1934). Studies of reproduction in sheep. I. The ovulation rate of the ewe as affected by the plane of nutrition. Anat. Rec. 60, 125–134.


Clutton-Brock, T. H. , Albon, S. D. , and Guinness, F. E. (1986). Great expectations: dominance, breeding success and offspring sex ratios in red deer. Anim. Behav. 34, 460–471.


Cohen-Tannoudji, J. , Locatelli, A. , and Signoret, J.-P. (1986). Non-pheromonal stimulation by the male of LH release in the anoestrous ewe. Physiol. Behav. 36, 921–924.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Cohen-Tannoudji, J. , Lavenet, C. , Locatelli, A. , Tillet, Y. , and Signoret, J. P. (1989). Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour. J. Reprod. Fertil. 86, 135–144.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Downing, J. A. , Joss, J. , and Scaramuzzi, R. J. (1995). Ovulation rate and the concentrations of gonadotrophins and metabolic hormones in ewes infused with glucose during the late luteal phase of the oestrous cycle. J. Endocrinol. 146, 403–410.
PubMed |

Dulac, C. (2000). Sensory coding of pheromone signals in mammals. Curr. Opin. Neurobiol. 10, 511–518.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Fabre-Nys, C. , and Venier, G. (1987). Development and use of a method for quantifying sexual behaviour in ewes. Appl. Anim. Behav. Sci. 17, 289–304.
Crossref | GoogleScholarGoogle Scholar |

Fisher, J. S., Martin, G. B., Oldham, C. M., and  Gray, S. J. (1993). Long-term effects of nutrition on spontaneous ovulation in Merino ewes and their responses to the ‘ram effect’. In ‘Proceedings of the 7th World Congress on Animal Production, Edmonton, Canada. Vol. 2’.  pp. 32–33.

Fowler, C. D. , Liu, Y. , Ouimet, C. , and Wang, Z. (2002). The effects of social environment on adult neurogenesis in the female prairie vole. J. Neurobiol. 51, 115–128.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed |

Gelez, H. , Lindsay, D. R. , Blache, D. , Martin, G. B. , and Fabre-Nys, C. (2003). Temperament and sexual experience affect female sexual behaviour in sheep. Appl. Anim. Behav. Sci. 84, 81–87.
Crossref | GoogleScholarGoogle Scholar |

Gibson, W. R. , and Robinson, T. J. (1971). The seasonal nature of reproductive phenomena in the sheep. I. Variation in sensitivity to oestrogen. J. Reprod. Fertil. 24, 9–18.
PubMed |

Gonzalez, R. , Levy, F. , Orgeur, P. , Poindron, P. , and Signoret, J.-P. (1991a). Female effect in sheep. 2. Role of volatile substances from the sexually-receptive female: implication of the sense of smell.  Reprod. Nutr. Dévelop. 31, 103–109.


Gonzalez, R. , Orgeur, P. , Poindron, P. , and Signoret, J.-P. (1991b). Female effect in sheep. 1. The effects of sexual receptivity of females and the sexual experience of the rams.  Reprod. Nutr. Dévelop. 31, 97–102.


Goubillon, M.-L. , Forsdike, R. A. , Robinson, J. E. , Ciofi, P. , Caraty, A. , and Herbison, A. E. (2000). Identification of neurokinin B-expressing neurons as an highly estrogen-receptive, sexually dimorphic cell group in the ovine arcuate nucleus. Endocrinology 141, 4218–4225.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Goursaud, A. P. , and Nowak, R. (1999). Colostrum mediates the development of mother preference by the new born lamb. Physiol. Behav. 67, 49–56.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hafez, E. S. E. (1952). Studies on the breeding season and reproduction of the ewe. J. Agric. Sci. 42, 189–265.


Hairston, J. E. , Ball, G. F. , and Nelson, R. J. (2003). Photoperiodic and temporal influences on chemosensory induction of brain fos expression in female prairie voles. J. Neuroendocrinol. 15, 161–172.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Halem, H. A. , Baum, M. J. , and Cherry, J. A. (2001). Sex difference and steroid modulation of pheromone-induced immediate early genes in the two zones of the mouse accessory olfactory system. J. Neurosci. 21, 2474–2480.
PubMed |

Hötzel, M. J. , Walkden-Brown, S. W. , Blackberry, M. A. , and Martin, G. B. (1995). The effect of nutrition on testicular growth in mature Merino rams involves mechanisms that are independent of changes in GnRH pulse frequency. J. Endocrinol. 147, 75–85.
PubMed |

Hötzel, M. J. , Walkden-Brown, S. W. , Fisher, J. S. , and Martin, G. B. (2003). Determinants of the annual pattern of reproduction in mature male Merino and Suffolk sheep: responses to a nutritional stimulus in the breeding and non-breeding seasons. Reprod. Fertil. Dev. 15, 1–9.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Huang, L. , DeVries, G. J. , and Bittman, E. L. (1998). Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J. Neurobiol. 36, 410–420.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Iglesias, R. M. R. , Ciccioli, N. H. , Irazoqui, H. , and Giglioli, C. (1996). Ovulation rate in ewes after a single oral glucogenic dosage during a ram-induced follicular phase. Anim. Reprod. Sci. 44, 211–221.
Crossref | GoogleScholarGoogle Scholar |

Jansen, H. T. , Iwamoto, G. A. , and Jackson, G. L. (1998). Central connections of the ovine olfactory bulb formation identified using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Res. Bull. 45, 27–39.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kendrick, K. M. , Da Costa, A. P. , Leigh, A. E. , Hinton, M. R. , and Peirce, J. W. (2001). Sheep don’t forget a face. Nature 414, 165–166.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lamond, D. R. , Gaddy, R. G. , and Kennedy, S. W. (1972). Influence of season and nutrition on luteal plasma progesterone in Rambouillet ewes. J. Anim. Sci. 34, 626–629.
PubMed |

Lévy, F. , Locatelli, A. , Piketty, V. , Tillet, Y. , and Poindron, P. (1995). Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiol. Behav. 57, 97–104.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lévy, F. , Meurisse, M. , Ferreira, G. , Thibault, J. , and Tillet, Y. (1999). Afferents to the rostral olfactory bulb in sheep with special emphasis on the cholinergic, noradrenergic and serotonergic connections. J. Chem. Neuroanat. 16, 245–263.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Martin, G. B. (1984). Factors affecting the secretion of luteinizing hormone in the ewe. Biol. Rev. 59, 1–87.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Martin, G. B. (1995). Reproductive research on farm animals for Australia: some long-distance goals. Reprod. Fertil. Dev. 7, 967–982.
PubMed |

Martin, G. B. , and Walkden-Brown, S. W. (1995). Nutritional influences on reproduction in mature male sheep and goats. J. Reprod. Fertil. Suppl. 49, 437–449.
PubMed |

Martin, G. B. , Oldham, C. M. , Cognié, Y. , and Pearce, D. T. (1986). The physiological responses of anovulatory ewes to the introduction of rams: a review. Livestock Prod. Sci. 15, 219–247.
Crossref | GoogleScholarGoogle Scholar |

Martin, G. B., Walkden-Brown, S. W., Boukhliq, R., Tjondronegoro, S., Miller, D. W., Fisher, J. S., Hötzel, M.-J., Restall, B. J. and  Adams, N. R. (1994). Non-photoperiodic inputs into seasonal breeding in male ruminants. In ‘Perspectives in Comparative Endocrinology’. (Eds. K. G. Davey, R. E. Peter and S. S. Tobe)  pp. 574–585. (National Research Council of Canada: Ottawa.)

Martin, G. B. , Tjondronegoro, S. , Boukhliq, R. , Blackberry, M. A. , Briegel, J. R. , Blache, D. , Fisher, J. A. , and Adams, N. R. (1999). Determinants of the annual pattern of reproduction in mature male Merino and Suffolk sheep: modification of endogenous rhythms by photoperiod. Reprod. Fertil. Dev. 11, 355–366.
PubMed |

Martin, G. B. , Hötzel, M. J. , Blache, D. , Walkden-Brown, S. W. , Blackberry, M. A. , Boukhliq, R. , Fisher, J. S. , and Miller, D. W. (2002). Determinants of the annual pattern of reproduction in mature male Merino and Suffolk sheep: modification of responses to photoperiod by an annual cycle in food supply. Reprod. Fertil. Dev. 14, 165–175.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Martin, G. B., Milton, J. T. B., Davidson, R. H., Banchero, G. E., Hunzicker, G. E., Lindsay, D. R., and  Blache, D. (2004). Natural methods of increasing reproductive efficiency in sheep and goats. In ‘Proceedings of the 15th International Congress on Animal Reproduction, Porto Seguro, Brazil, August 2004’. (Brazilian College of Animal Reproduction: Belo Horizonte, Brazil.) (In press)

Muñoz-Gutiérrez, M. , Blache, D. , Martin, G. B. , and Scaramuzzi, R. J. (2002). Folliculogenesis and the ovarian expression of mRNA for aromatase in anoestrous sheep after 5 days of glucose or glucosamine infusion or supplementary lupin feeding. Reproduction 124, 721–731.
PubMed |

Okolski, A. (1975). Effect of different amounts of protein in the diet on sexual behaviour and properties of semen in rams. Acta agrar. silvest. Ser. zootech. 15, 101–121.


Parker, G. V. , and Thwaites, C. J. (1972). The effects of undernutrition on libido and semen quality in adult Merino rams. Aust. J. Agric. Res. 23, 109–115.


Parr, R. A. (1992). Nutrition–progesterone interactions during early pregnancy in sheep. Reprod. Fertil. Dev. 4, 297–300.
PubMed |

Parr, R. A. , Davis, I. F. , Miles, M. A. , and Squires, T. J. (1993). Liver blood flow and metabolic clearance rate of progesterone in sheep. Res. Vet. Sci. 55, 311–316.
PubMed |

Pearce, G. P. , and Oldham, C. M. (1988). Importance of non-olfactory ram stimuli in mediating ram-induced ovulation in the ewe. J. Reprod. Fertil. 84, 333–339.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Restall, B. J. , Restall, H. , and Walkden-Brown, S. W. (1995). The induction of ovulation in anovulatory goats by oestrous females. Anim. Reprod. Sci. 40, 299–303.
Crossref | GoogleScholarGoogle Scholar |

Rhind, S. M. , Leslie, I. D. , Gunn, R. G. , and Doney, J. M. (1985). Plasma FSH, LH, prolactin and progesterone profiles of Cheviot ewes with different levels of intake before and after mating, and associated effects on reproductive performance. Anim. Reprod. Sci. 8, 301–313.
Crossref | GoogleScholarGoogle Scholar |

Rhind, S. R. , Martin, G. B. , McMillen, S. , Tsonis, C. G. , and McNeilly, A. S. (1989). Effect of level of food intake of ewes on the secretion of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) and on the pituitary response to gonadotrophin-releasing hormone (GnRH) in ovariectomized ewes. J. Endocrinol. 121, 325–330.
PubMed |

Rochefort, C. , Gheusi, G. , Vincent, J. D. , and Lledo, P. M. (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679–2689.
PubMed |

Sharma, T. P. , Blache, D. , Blackberry, M. A. , and Martin, G. B. (1999). Role of peripheral and central aromatization in the control of gonadotrophin secretion in the male sheep. Reprod. Fertil. Dev. 11, 293–302.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shelton, M. (1980). Goats: influence of various exteroceptive factors on initiation of estrus and ovulation. Int. Goat Sheep Res. 1, 156–162.


Stewart, R., and  Oldham, C. M. (1986). Feeding lupins for 4 days during the luteal phase can increase ovulation rate. In ‘Proceedings of the Australian Society of Animal Production Vol. 16’.  pp. 367–370. (Australian Society of Animal Production: Melbourne, Australia.)

Tricoire, H. , Møller, M. , Chemineau, P. , and Malpaux, B. (2003). Origin of cerebrospinal fluid melatonin and possible function in the integration of photoperiod. Reprod. Suppl. 61, 311–321.
PubMed |

Ungerfeld, R. , Forsberg, M. , and Rubianes, E. (2004). Overview of the response of anoestrous ewes to the ram effect. Reprod. Fertil. Dev. 16, 479–490.


Viñoles, C. , Forsberg, M. , Banchero, G. , and Rubianes, E. (2002). Ovarian follicular dynamics and endocrine profiles in Polwarth ewes with high and low body condition. Anim. Sci. 74, 539–545.


Walkden-Brown, S. W. , Restall, B. J. , and Henniawati, H. (1993). The male effect in the Australian cashmere goat. 3. Enhancement with buck nutrition and use of oestrous females. Anim. Reprod. Sci. 32, 69–84.
Crossref | GoogleScholarGoogle Scholar |

Walkden-Brown, S. W. , Restall, B. J. , Norton, B. W. , and Scaramuzzi, R. J. (1994). The ‘female effect’ in Australian cashmere goats. Effect of season and diet quality on the LH and testosterone response of bucks to oestrous does. J. Reprod. Fertil. 100, 521–531.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Walkden-Brown, S. W. , Martin, G. B. , and Restall, B. J. (1999). Role of male–female interaction in regulating reproduction in sheep and goats. J. Reprod. Fertil. 52, 243–257.Suppl.


Williams, S. A. , Blache, D. , Martin, G. B. , Foot, R. , Blackberry, M. A. , and Scaramuzzi, R. J. (2001). Effect of nutritional supplementation on quantities of glucose transporters 1 and 4 in sheep granulosa and theca cells. Reproduction 122, 947–956.
PubMed |

Wright, P. J. , Geytenbeek, P. E. , and Clarke, I. J. (1990). The influence of nutrient status of post-partum ewes on ovarian cyclicity and on the oestrous and ovulatory responses to ram introduction. Anim. Reprod. Sci. 23, 293–303.
Crossref | GoogleScholarGoogle Scholar |

Zarco, Q. L. , Rodríguez, E. F. , Angulo, M. R. B. , and Valencia, M. J. (1995). Female to female stimulation of ovarian activity in the ewe. Anim. Reprod. Sci. 39, 251–258.
Crossref | GoogleScholarGoogle Scholar |