Plasma Melatonin and Progesterone Profiles of Suffolk and Romney Marsh Ewes Implanted with Melatonin during Anoestrus Season at Lower Latitudes in Southern Hemisphere

Aya Sasa, Paula Almeida Rodrigues, Keico Okino Nonaka, Julio César de Carvalho Balieiro, Lia Alencar Coelho

Abstract


Background: The subcutaneous implants of melatonin are stimulatory and mimic the positive effects of short photoperiod on reproduction in small ruminants. This study investigated the daily plasma melatonin profiles in ewes treated with melatonin implants and kept under natural photoperiod in Southeastern Brazil. The plasma progesterone concentrations were also investigated before and after melatonin implantation.

Materials, Methods & Results: Romney Marsh (n = 11) and Suffolk (n = 10) ewes, which had been isolated from rams for at least 2 months prior to the beginning of the trial, were randomly allocated in two groups based on melatonin implant treatment (with or without melatonin implant). For plasma melatonin concentration, 43 days after melatonin implantation and 3 days before the ram introduction blood samples were collected every 2 hours during 24 hours. For plasma progesterone concentrations, blood samples were collected every once to twice a week for 2 different periods: prior to melatonin implantation and 46 days after the melatonin implantation and at the same day of the introduction of rams. The hormonal concentrations were determined by the radioimmunoassay method (RIA). The data were analyzed according to MIXED procedure (SAS) as repeated measurements for random animal effects. The effect of melatonin treatment on plasma melatonin 24-h period varied according to the breed. At the dark-phase, there were no plasma melatonin differences (P > 0.05) between implanted and no-implanted (228.02 ± 58.39 vs. 169.59 ± 48.39) Romney Marsh ewes whereas for Suffolk ewes the plasma melatonin levels were higher in implanted (305.61 ± 68.39 pg/mL) than no-implanted (151.26 ± 38.35 pg/mL) ones. At the light-phase, melatonin treatment effects could be evidenced and these differences (P < 0.01) consisted of higher melatonin values for implanted ewes and basal values for no-implanted ones in both breed groups. Before the melatonin implantation, the plasma progesterone levels were ˂ 1 ng/mL for Romney Marsh (0.41 ± 0.02 ng/mL) and Suffolk (0.47 ± 0.02 ng/mL) ewes. During the ram introduction period, no melatonin treatment effect was observed on plasma progesterone concentrations in both breed groups, but 2 days after ram introduction the plasma progesterone concentrations increased the mean values > than 1 ng/mL in implanted and no-implanted Suffolk ewes. In implanted Romney Marsh ewes the elevation of progesterone mean values was weak whereas in no-implanted Romney Marsh ewes the progesterone levels were maintained ˂ 1 ng/mL during all the blood sample collection times.

Discussion: The melatonin treatment also produced a similar model of daily melatonin levels as reported previously by others, which is characterized by high plasma melatonin concentrations during the light phase of the day. The effect of melatonin implants on plasma melatonin profiles interacted with breed confirming an individual response to melatonin implantation which is proportional to genetic individual variation pattern of melatonin secretion. Before the melatonin implantation all Romney Marsh and Suffolk ewes were judged to be in non-ovulatory period (anoestrus) with plasma progesterone mean values lower than 1 ng/mL. The melatonin treatment helped to induce the ovulatory activity in most of the ewes that were in anestrous at the time of melatonin implantation and the efficacy of this treatment depends on the individual variation in ovulatory response to ram introduction. In Southeastern Brazil., melatonin implant altered the daily plasma melatonin profiles of Suffolk and Romney Marsh ewes by increasing the melatonin levels during the light-phase of the day. Melatonin implant also induced an ovulatory response in Suffolk and Romney Marsh after the introduction of the rams. For no-implanted Suffolk ewes, the male effect is sufficient to provoke an ovulatory response.


Keywords


implant melatonin; male effect natural photoperiod; progesterone; sheep.

Full Text:

PDF

References


Abecia J.A., Palacín I., Forcada F. & Valares J.A. 2006. The effect of melatonin treatment on the ovarian response of ewes to the ram effect. Domestic Animal Endocrinology. 31: 52-62.

Arendt J., Symons A.M. & Laud C. 1981. Pineal function in the sheep: evidence for a possible mechanism mediating seasonal reproductive activity. Experientia. 37: 584-586.

Arendt J., Symons A.M., English J., Poulton A.L. & Tobler I. 1988. How does melatonin control seasonal reproductive cycles? Reproduction, Nutrition and Development. 28: 387-397.

Celi I., Gatica M.C., Guzmán J.L., Gallego-Calvo L. & Zarazaga L.A. 2013. Influence of the male effect on the reproductive performance of female Payoya goats implanted with melatonin at the winter solstice. Animal Reproduction Science. 137: 183-188.

Cerna C., Porras A., Valencia M.J., Perera G. & Zarco L. 2000. Effect of an inverse subtropical (19º13N) photoperiod on ovarian activity, melatonin and prolactin secretion in Pelibuey ewes. Animal Reproduction Science. 60: 511-525.

Chemineau P., Beltrán De Heredia I., Deveau A. & Bodin L. 1996. High repeatability of the amplitude and duration of the nycthemeral rhythm of the plasma melatonin concentration in the Ile-de-France ewe. Journal Pineal Research. 21: 1-6.

Coelho L.A., Rodrigues P.A., Nonaka K.O., Sasa A., Balieiro J.C.C., Vicente W.R.R. & Cipolla-Neto J. 2006. Annual pattern of plasma melatonin and progesterone concentrations in hair and wool ewe lambs under natural photoperiod at lower latitudes in southern hemisphere. Journal Pineal Research. 41:101-107.

Donovan A., Boland M.P., Roche J.F. & O’Callaghan D. 1994. The effect of supplementary long days, a subcutaneous melatonin implant and exposure to ram on the onset of the breeding season in ewes. Animal Reproduction Science. 34: 231-240.

Durotoye L.A., Rajkumar R., Argo C.M., Nowak R., Webley G.E., McNeil M.E., Graham N.B. & Rodway R.G. 1991. Effect of constant-release melatonin implants on the onset of estrous activity and on reproductive performance in the ewe. Animal Production. 52: 489-497.

English J., Pouton A.L., Arendt J. & Symons A.M. 1986. A comparison of the efficiency of melatonin treatments in advancing oestrus in ewes. Journal Reproduction Fertility. 77: 321-327.

Forcada F., Abecia J.A., Casao A., Cebrián-Perez J.A., Muiño-Blanco T. & Palacín I. 2007. Effects of ageing and exogenous melatonin on pituitary responsiveness to GnRH in ewes during anestrus and the reproductive season. Theriogenology. 67: 855-862.

Forcada F., Abecia J.A., Zúñiga O. & Lozano J.M. 2002. Variation in the ability of melatonin implants inserted at two different times after the winter solstice to restore reproductive activity in reduced seasonality ewes. Australian Journal of Agricultural Research. 53(2): 167-173.

Forcada F., Zarazaga L. & Abecia J.A. 1995. Effect of exogenous melatonin and plane of nutrition after weaning on estrous activity, endocrine status and ovulation rate in Salz ewes lambing in the seasonal anestrus. Theriogenology. 43: 1179-1193.

Frazer S., Cowen P., Franklin M., Franey C. & Arendt J. 1983. Direct radioimmunoassay for melatonin in plasma. Clinical Chemistry. 29: 396-397.

Goldman B.D. 1999. The circadian timing system and reproduction in mammals. Steroids. 64: 679-685.

Guerin M.V., Watson R., McLoughney J., Earle C., Seamark R.F. & Matthews C.D. 1989. The annual patterns of serum melatonin in Romney-Marsh sheep held in natural photoperiodic conditions. Advances in Pineal Research. 3: 137-141.

Kennaway D.J., Gilmore T.A. & Seamark R.F. 1982. Effect of melatonin implants on the circadian rhythm of plasma melatonin and prolactin in sheep. Endocrinology. 110: 2186-2188.

Köppen W. 1948. Climatologia. Buenos Aires: Panamericana, 478 p.

Malpaux B., Moenter S.M., Wayne F.J., Woodfill C.J.I. & Karsch F.J. 1988. Reproductive refractoriness of the ewe to inhibitory photoperiodic is not caused by alteration of the circadian secretion of melatonin. Neuroendocrinology. 48: 264- 270.

Malpaux B., Viguié C., Skinner D.C., Thiéry J.C. & Chemineau P. 1997. Control of the circanual rhythm of reproduction by melatonin in the ewe. Brain Research Bulletin. 4: 431-438.

Matthews C.D., Seamark R.F. & Guerin M.V. 1992. Plasma melatonin profiles of Romney Marsh sheep in natural photoperiod and in acutely extended darkness. Journal of Reproduction and Fertility. 95: 869-875.

Minton J.E., Coppinger T.R., Spaeth C.W. & Martin L.C. 1991. Poor reproductive response of anoestrous Suffolk ewes to ram exposure is not due to failure to secrete luteinizing hormone acutely. Journal Animal Science. 69: 33143320.

Minton J.E. 1990. Role of photorefractoriness in onset of anoestrous in Ramboullet X Dorset ewes. Journal of Reproduction and Fertility. 89: 261-268.

National Research Council. 1985. Nutrient requirements of domestic animals: nutrient requirements of sheep. 6th edn. Washington: D.C. National Academy Press, 99p.

Notter D.R. & Chemineau P. 2001. Nocturnal melatonin and prolactina plasma concentrations in sheep selected for fertility in autumn lambing. Journal of Animal Science. 79: 2895-2901.

Rekik M., Bryant M.J. & Cunningham F.J. 1991. Effects of treatment with melatonin on the response of seasonally anovular ewes to the introduction of rams. Animal Production. 53: 203-217.

Robinson J.J., Wallace J.M., Aitken R.P. & McNeilly A.S. 1993. Effect of chronic treatment with a GnRH agonist to suppress pulsatile LH secretion on the ability of exogenous melatonin to advance oestrous cyclicity in ewes. Journal of Reproduction and Fertility. 99: 601-608.

Robison J.J., Wigzell S., Aitken R.P., Wallace J.M., Ireland S. & Robertson I.S. 1991. The modifying effects of melatonin, ram exposure and plane of nutrition on the onset of ovarian activity, ovulation rate and the endocrine status of ewes. Animal Reproduction Science. 26: 73-91.

Rodrigues P.A., Coelho L.A., Nonaka K.O., Sasa A., Vicente W.R.R., Balieiro J.C.C. & Siqueira E.R. 2007. Annual characteristics of estrous activity in wool and hair ewe lambs under subtropical conditions. Scientia Agricola. 64: 468-475.

Rollag M.D., O’Callagham P.L. & Niswender G.D. 1978. Serum melatonin concentrations during different stages of the annual reproductive cycle in ewes. Biology of Reproduction. 18: 279-285.

Rosa H.J.D. & Bryant M.J. 2002. The ‘ram effect’ as a way of modifying the reproductive activity in the ewe. Small Ruminant Research. 45: 1-16.

Sasa A., Nonaka K.O., Balieiro J.C.C. & Coelho L.A. 2011. Progesterona plasmática de ovelhas submetidas ao efeito-macho e mantidas sob diferentes condições nutricionais. Arquivo Brasileiro de Medicina Veterinária Zootecnia. 63: 1066-1072.

Staples L.D., McPhee S., Kennaway D.J. & Williams A.H. 1992. The influence of exogenous melatonin on the seasonal patterns of ovulation and oestrus in sheep. Animal Reproduction Science. 30: 185-223.

Statistical Analysis System Institute. 1995. SAS User’s Guide, Release 8.0.2, Cary. SAS Institute.

Thimonier J. & Mauléon P. 1969. Variations saisonnières du comportement dóestrus et des activités ovarienne et hypophysaire chez les ovins. Annales de Biologie Animale, Biochimie, Biophysique. 9: 223-250.

Viguié C., Thibault J., Thiéry J.C., Tillet Y. & Malpaux B. 1997. Characterization of the short day-induced decrease in median eminence tyrosine hydroxylase activity in the ewe: Temporal relationship to the changes in luteinizing hormone and prolactina secretion and short day-like effect of melatonin. Endocrinology. 138: 499-506.

Zarazaga L.A., Celi I., Guzmán J.L. & Malpaux B. 2012. Enhancement of male effect on reproductive performance in female Mediterranean goats with long day and/or melatonin treatment. The Veterinary Journal. 192: 441-444.

Zarazaga L.A., Malpaux B., Bodin L. & Chemineau P. 1998. The large variability in melatonin blood levels in ewes is under strong genetic influence. American Journal of Physiology, Endocrinology and Metabolism. 274: 607-610.

Zúñiga O., Forcada F. & Abecia J.A. 2002. The effect of melatonin implants on response to male effect on the subsequent cyclicity of Rasa Aragonesa ewes implanted in April. Journal Animal Science. 72: 165-174.




DOI: https://doi.org/10.22456/1679-9216.81098

Copyright (c) 2018 Aya Sasa, Paula Almeida Rodrigues, Keico Okino Nonaka, Julio César de Carvalho Balieiro, Lia Alencar Coelho

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.