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
Maria J. Hötzel A B , Stephen W. Walkden-Brown A C , James S. Fisher A D and Graeme B. Martin A E FA School of Animal Biology, The University of Western Australia, Crawley, WA 6008, Australia.
B Present address: Laboratório de Etologia Aplicada, Departamento de Zootecnia e Desenvolvimento Rural, Universidade Federal de Santa Catarina, Rodovia Admar Gonzaga, 1346, Itacorubi, Florianópolis, SC 88.034-001, Brazil.
C Present address: Animal Science, School of Rural Science and Agriculture, University of New England, Armidale, NSW 2351, Australia.
D Present address: Centre for Cropping Systems, Agriculture Western Australia, PO Box 483, Northam, WA 6401, Australia.
E CSIRO Division of Animal Production, Private Bag, PO Wembley, WA 6014, Australia.
F To whom correspondence should be addressed. email: gmartin@agric.uwa.edu.au
Reproduction, Fertility and Development 15(1) 1-9 https://doi.org/10.1071/RD02024
Submitted: 12 March 2002 Accepted: 28 November 2002 Published: 28 November 2002
Abstract
This study was designed to test whether an acute improvement in diet would increase gonadotrophin secretion and testicular growth in strongly photoperiod-responsive Suffolk rams and weakly photoperiod-responsive Merino rams in both the breeding (February–March) and the non-breeding (July–August) seasons. Mature rams (n = 5 or 6) of these breeds were fed a maintenance diet (0.9 kg chaff + 100 g lupin grain) or the same diet supplemented with 1.5 kg lupin grain for 42 days in each season. Lupin grain is a rich source of both energy and protein. Testosterone, luteinizing hormone (LH) and follicle stimulating hormone (FSH) were measured in plasma from blood sampled every 20 min for 24 h on Days −1, 12 and 35 relative to the change in feeding. In rams supplemented with lupins, body mass increased in both breeds in both seasons (P < 0.001). Scrotal circumference and LH pulse frequency increased with lupin supplementation in both seasons (P < 0.003) in Merinos, but only during the breeding season (P < 0.003) in Suffolks. Plasma FSH concentrations were affected by diet only during the breeding season, being elevated on Day 12 in lupin-supplemented rams of both breeds (P < 0.05). It was concluded that Merino rams exhibit reproductive responses to improved nutrition irrespective of time of the year, whereas Suffolk rams respond to nutrition only when the hypothalamic reproductive centres are not inhibited by photoperiod. Thus, Suffolks do respond to nutrition, just as Merinos do, but only when photoperiod allows. This difference between breeds appears to be a result of differences in the neuroendocrine pathways that control pulsatile gonadotrophin-releasing hormone secretion.
Extra keywords: breed
Acknowledgments
This study could not have been contemplated without the generous assistance of the students and staff of the Animal Science Group (University of Western Australia), particularly Mrs M. A. Blackberry and Mr L. Cranfield. We are also grateful to the National Institute of Diabetes, Digestive & Kidney Disease and Dr A. F. Parlow (Pituitary Hormones and Antisera Center, Harbour-UCLA Medical Center, 1000 Carson Street, Torrance, CA, USA) for the reagents used for the gonadotrophin assays. We acknowledge Dr R. I. Cox (CSIRO Division of Animal Production, Prospect, NSW, Australia) for the donation of testosterone-3-CMO-HSA. This work was funded by the Australian Research Council; the CSIRO Division of Animal Production; a scholarship from The Australian Wool Corporation (J. S. Fisher); the EHB Lefroy Fellowship (S. W. Walkden-Brown); and the Brazilian Research Council (CNPq) (M. J. Hötzel).
Adam, C. L. (2000). Nutritional and photoperiodic regulation of appetite and reproduction in seasonal domestic mammals Reprod. Dom. Anim. 6, 1–8.(Suppl.)
Alkass, J. E. , Bryant, M. J. , and Walton, J. S. (1982). Some effects of level of feeding and body condition upon sperm production and gonadotropin concentrations in the ram Anim. Prod. 34, 265–7.
Blache, D. , Miller, D. W. , Milton, J. T. B. , and Martin, G. B. (1996). The secretion of gonadotrophins, insulin and insulin-like growth factor I by Merino rams supplemented with different legume seeds Aust. J. Agric. Res. 47, 843–82.
Blache, D. , Tjondronegoro, S. , Blackberry, M. A. , Anderson, S. T. , Curlewis, J. D. , and Martin, G. B. (1997). Gonadotrophin and prolactin secretion in castrated male sheep following subcutaneous or intracranial treatment with testicular hormones Endocrine 7, 235–43.
| PubMed |
Blache, D. , Tellam, R. L. , Chagas, L. M. , Blackberry, M. A. , Vercoe, P. E. , and Martin, G. B. (2000). Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep J. Endocrinol. 165, 625–37.
| 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, 515–24.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
D’Occhio, M. J. , Schanbacher, B. D. , and Kinder, J. E. (1984). Profiles of luteinizing hormone, follicle-stimulating hormone, testosterone and prolactin in rams of diverse breeds: effects of contrasting short (8L : 16D) and long (16L : 8D) photoperiods Biol. Reprod. 30, 1039–54.
| PubMed |
Foster, D. L. , Ebling, F. J. P. , Micka, A. F. , Vannerson, L. A. , Buckholtz, D. C. , Wood, R. I. , Suttie, J. M. , and Fenner, D. E. (1989). Metabolic interfaces between growth and reproduction. I: Nutritional modulation of gonadotropin, prolactin, and female growth hormone secretion in the growth-limited female lamb Endocrinology 125, 342–50.
| PubMed |
Hötzel, M. J. , Martin, G. B. , Walkden-Brown, S. W. , and Fisher, J. S. (1994). Nutritional effects on testicular growth and gonadotrophin secretion in Suffolk and Merino rams in the breeding and non-breeding seasons Proc. Aust. Soc. Reprod. Biol. 26, 48.(Abstract.)
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. , Markey, C. M. , Walkden-Brown, S. W. , and Martin, G. B. (1998). Morphometric and endocrine effects of nutrition on the testis of the ram J. Reprod. Fertil. 113, 217–30.
| PubMed |
Iason, G. R. , Sim, D. A. , Foreman, E. , Fenn, P. , and Elston, D. A. (1994). Seasonal variation of voluntary food intake and metabolic rate in three contrasting breeds of sheep Anim. Prod. 58, 381–7.
Kennaway, D. J. , Gilmore, T. A. , and Seamark, R. F. (1982). Effect of melatonin feeding on serum prolactin and gonadotrophin levels and the onset of seasonal oestrous cyclicity in sheep Endocrinology 110, 1766–72.
| PubMed |
Kile, J. P. , Alexander, B. M. , Moss, G. E. , Halford, D. M. , and Nett, T. M. (1991). Gonadotropin-releasing hormone overrides the negative effect of reduced dietary energy to gonadotropin synthesis and secretion in ewes Endocrinology 128, 843–9.
| PubMed |
Lincoln, G. A. (1979). Use of pulsed infusion of luteinizing hormone releasing hormone to mimic seasonally induced endocrine changes in the ram J. Endocrinol. 83, 251–60.
| PubMed |
Lincoln, G. A. , and Short, R. V. (1980). Seasonal breeding: nature’s contraceptive Recent Prog. Horm. Res. 36, 1–52.
| PubMed |
Lincoln, G. A. , Libre, E. A. , and Merriam, G. R. (1989). Long-term reproductive cycles in rams after pinealectomy or superior cervical ganglionectomy J. Reprod. Fertil. 85, 687–704.
| PubMed |
Lincoln, G. A. , Lincoln, C. E. , and McNeilly, A. S. (1990). Seasonal cycles in the blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild, feral and domesticated breeds of sheep J. Reprod. Fertil. 88, 623–33.
| PubMed |
Lindsay, D. R. , Pelletier, J. , Pisselet, C. , and Courot, M. (1984). Changes in photoperiod and nutrition and their effect on testicular growth of rams J. Reprod. Fertil. 71, 351–6.
| PubMed |
Lubbers, L. S. , and Jackson, G. L. (1993). Neuroendocrine mechanisms that control seasonal changes in luteinizing hormone secretion in sheep are sexually differentiated Biol. Reprod. 49, 1369–76.
| PubMed |
Marie, M. , Findlay, P. A. , Thomas, L. , and Adam, C. L. (2001). Daily patterns of plasma leptin in sheep: effects of photoperiod and food intake J. Endocrinol. 170, 277–86.
| PubMed |
Martin, G. B. , and Walkden-Brown, S. W. (1995). Nutritional influences on reproduction in mature male sheep and goats J. Reprod. Fertil. 49, 437–49.Suppl.
Martin, G. B. , Sutherland, S. R. D. , and Lindsay, D. R. (1987). Effects of nutritional supplements on testicular size and the secretion of LH and testosterone in Merino and Booroola rams Anim. Reprod. Sci. 12, 267–81.
| Crossref | GoogleScholarGoogle Scholar |
Martin, G. B. , Tjondronegoro, S. , and Blackberry, M. A. (1994a). Effects of nutrition on testicular size and the plasma concentrations of gonadotrophins, testosterone and inhibin in mature male sheep J. Reprod. Fertil. 101, 121–8.
| PubMed |
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
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, 355–66.
| PubMed |
Martin, G. B. , Hötzel, M. J. , Blache, D. , Walkden-Brown, S. W. , Blackberry, M. A. , Boukhliq, R. , Fisher, J. A. , 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, 165–75.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Masters, D. G. , and Fels, H. E. (1984). Seasonal changes in the testicular size of grazing rams Anim. Prod. Aust. 15, 444–7.
Miller, D. W. , Blache, D. , and Martin, G. B. (1995). Insulin stimulates LH secretion in rams when infused into the third cerebral ventricle: comparison with the effect of improved nutrition J. Endocrinol. 147, 321–9.
| PubMed |
Murray, P. J. , Rowe, J. B. , Pethick, D. W. , and Adams, N. R. (1990). The effect of nutrition on testicular growth in the Merino ram Aust. J. Agric. Res. 41, 185–95.
Murray, P. J. , Rowe, J. B. , and Pethick, D. W. (1991). Effect of season and nutrition on scrotal circumference of Merino ram Aust. J. Exp. Agric. 31, 753–6.
Poulton, A. L. , and Robinson, T. J. (1987). The response of rams and ewes of three breeds to artificial photoperiod J. Reprod. Fertil. 79, 609–626.
| PubMed |
Ravault, J. P. , and Thimonier, J. (1988). Melatonin patterns in ewes maintained under skeleton or resonance photoperiodic regimens Reprod. Nutr. Dev. 28, 473–486.
| PubMed |
Rhim, T. -J. , Kuehl, D. , and and Jackson, G. L. (1993). Seasonal changes in the relationships between secretion of gonadotropin-releasing hormone, luteinizing hormone, and testosterone in the ram Biol. Reprod. 48, 197–204.
| PubMed |
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, 325–30.
| PubMed |
Ritar, A. J., Adams, N. R. and Sanders, M. R. (1984). Effect of lupin feeding on LH, testosterone and testes In
Schanbacher, B. D. (1988). Responses of market lambs and Suffolk rams to a stimulatory skeleton photoperiod Reprod. Nutr. Dev. 28, 431–41.
| PubMed |
Setchell, B. , Waites, G. M. H. , and Lindner, H. R. (1965). Effect of undernutrition on testicular blood flow and metabolism and the output of testosterone in the ram J. Reprod. Fertil. 9, 149–62.
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 |
Thomas, G. B. , Pearce, D. T. , Oldham, C. M. , Martin, G. B. , and Lindsay, D. R. (1988). Effects of breed, ovarian steroids and season on the pulsatile secretion of LH in ovariectomized ewes J. Reprod. Fertil. 84, 313–24.
| PubMed |
Tjondronegoro, S. , Martin, G. B. , Sutherland, S. R , and Boukhliq, R. (1996). Interactions between nutrition, testosterone and inhibin in the control of gonadotrophin secretion in mature rams Reprod. Fertil. Dev. 8, 855–62.
| PubMed |
Turner, A. I. , Tilbrook, A. J. , Clarke, I. J. , and Scott, C. J. (2001). Progesterone and testosterone in combination act in the hypothalamus of castrated rams to regulate the secretion of luteinising hormone J. Endocrinol. 169, 291–8.
| PubMed |
Walkden-Brown, S. W. , Restall, B. J. , Norton, B. W. , Scaramuzzi, R. J. , and Martin, G. B. (1994). Effect of nutrition on seasonal patterns of LH, FSH and testosterone concentration, testicular mass, sebaceous gland volume and odour in Australian cashmere goats J. Reprod. Fertil. 102, 351–60.
| PubMed |
Xu, Z. Z. , McDonald, M. F. , McCutcheon, S. N. , and Blair, H. T. (1992). Effects of season and testosterone treatment on gonadotrophin secretion and pituitary responsiveness to gonadotrophin-releasing hormone in castrated Romney and Poll Dorset rams J. Reprod. Fertil. 95, 183–90.
| PubMed |
