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Reproductive biology and endocrinology : RB&E2011; 9; 130; doi: 10.1186/1477-7827-9-130

Effects of nutritional cues on the duration of the winter anovulatory phase and on associated hormone levels in adult female Welsh pony horses (Equus caballus).

Abstract: Mares have an annual reproductive rhythm, with a phase of inactivity in midwinter. The aim of this study was to determine the impact of food restriction on physiological and metabolic hallmarks of this rhythm. Methods: Over three successive years, 3 groups of 10 mares were kept under natural photoperiod. A 'well-fed' group was fed to maintain the mares in good body condition; a 'restricted' group received a diet calculated to keep the mares thin and a 'variable' group was fed during some periods like the 'restricted' group and during some other periods like the 'well-fed' group, with the aim of mimicking the natural seasonal variation of pasture availability, but a few months in advance of this natural rhythm. Results: Winter ovarian inactivity always occurred and was long in the restricted group. In contrast, in the 'well-fed' group, 40% of mares showed this inactivity, which was shorter than in the other groups. Re-feeding the 'variable' group in autumn and winter did not advance the first ovulation in spring, compared with the 'restricted' group. Measurements of glucose and insulin concentrations in mares from the 'restricted' group during two 24 h periods of blood sampling, revealed no post-prandial peaks. For GH (Growth hormone), IGF-1 and leptin levels, large differences were found between the 'well-fed' group and the other groups. The glucose, insulin, GH and leptin levels but not melatonin level are highly correlated with the duration of ovulatory activity. Conclusions: The annual rhythm driven by melatonin secretion is only responsible for the timing of the breeding season. The occurrence and length of winter ovarian inactivity is defined by metabolic hormones.
Publication Date: 2011-09-29 PubMed ID: 21958120PubMed Central: PMC3195710DOI: 10.1186/1477-7827-9-130Google Scholar: Lookup
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  • Comparative Study
  • Journal Article
  • Randomized Controlled Trial
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates the impact of various dietary restrictions on the winter anovulatory phase and hormone levels in adult female Welsh pony horses. The authors found that feeding restrictions contributed to a more substantial winter ovarian inactivity period and influenced specific metabolic hormone levels.

Objective & Research Methodology

  • The researchers aimed to explore how food restrictions impacted the annual reproductive rhythms in adult female Welsh pony horses, specifically looking at the physiological and metabolic indicators.
  • The experiment was carried out over three years using three groups of 10 mares each under natural photoperiod conditions. These were:
    • A ‘well-fed’ group, where horses were given sufficient food to maintain good bodily conditions.
    • A ‘restricted’ group, which was supplied with limited food to induce thinness.
    • A ‘variable’ group, whose diet varied between restriction and abundance to mimic natural seasonal variations in food availability, slightly ahead of natural rhythm.

Results and Findings

  • Ovarian inactivity during winter was consistent across all groups but was extensive in the ‘restricted’ group.
  • In the ‘well-fed’ group, only 40% of the mares exhibited this inactivity, and it was considerably short compared to other groups.
  • Re-feeding the ‘variable’ group during autumn and winter did not hasten the first ovulation in spring, compared to the ‘restricted’ group.
  • No significant post-prandial (after meals) peak in glucose and insulin levels was observed in mares from the ‘restricted’ group during two 24-hour blood sampling periods.
  • There were notable differences in glucose, insulin, Growth hormone (GH), and leptin levels between the ‘well-fed’ group and the other groups.
  • The researchers discovered a strong correlation between glucose, insulin, GH, leptin levels but not with melatonin level and the duration of ovulatory activity.

Conclusion

  • The study concluded that while the annual rhythm directed by melatonin secretion regulates the timing of the breeding season, the occurrence and duration of winter ovarian inactivity is determined by metabolic hormones.

Cite This Article

APA
Salazar-Ortiz J, Camous S, Briant C, Lardic L, Chesneau D, Guillaume D. (2011). Effects of nutritional cues on the duration of the winter anovulatory phase and on associated hormone levels in adult female Welsh pony horses (Equus caballus). Reprod Biol Endocrinol, 9, 130. https://doi.org/10.1186/1477-7827-9-130

Publication

ISSN: 1477-7827
NlmUniqueID: 101153627
Country: England
Language: English
Volume: 9
Pages: 130

Researcher Affiliations

Salazar-Ortiz, Juan
  • INRA, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France.
Camous, Sylvaine
    Briant, Christine
      Lardic, Lionel
        Chesneau, Didier
          Guillaume, Daniel

            MeSH Terms

            • Adiposity
            • Animals
            • Anovulation / blood
            • Anovulation / pathology
            • Anovulation / physiopathology
            • Anovulation / veterinary
            • Blood Glucose / analysis
            • Body Weight
            • Caloric Restriction / veterinary
            • Circadian Rhythm / radiation effects
            • Female
            • France
            • Growth Hormone / blood
            • Horses / physiology
            • Insulin / blood
            • Insulin-Like Growth Factor I / analysis
            • Leptin / blood
            • Melatonin / blood
            • Ovulation / radiation effects
            • Photoperiod
            • Seasons
            • Subcutaneous Fat, Abdominal / pathology
            • Time Factors

            References

            This article includes 95 references
            1. Langlois B, Blouin C. Effect of a horse's month of birth on its future sport performance. I Effect on annual phenotypic indices.. Ann Zootech 1997;46:393–398.
              doi: 10.1051/animres:19970501google scholar: lookup
            2. Langlois B, Blouin C. Effect of a horse's month of birth on its future sport performance. II Effect on annual earning and annual earning per start.. Ann Zootech 1998;47:67–74.
              doi: 10.1051/animres:19980105google scholar: lookup
            3. Langlois B, Blouin C. Statistical analysis of some factors affecting the number of horse births in France.. Reprod Nutr Dev 2004 Nov-Dec;44(6):583-95.
              pubmed: 15762302doi: 10.1051/rnd:2004055google scholar: lookup
            4. van Niekerk CH, van Heerden JS. Nutrition and ovarian activity of mares early in the breeding season.. J S Afr Vet Med Assoc 1972 Dec;43(4):351-60.
              pubmed: 4677611
            5. Ginther OJ. Occurrence of anestrus, estrus, diestrus, and ovulation over a 12-month period in mares.. Am J Vet Res 1974 Sep;35(9):1173-9.
              pubmed: 4473070
            6. McDaniel JB, Kreider JL, Thrasher DM. The influence of artificial light and a nutritional supplement on the onset of the breeding season in mares [abstract]. J Anim Sci 1979;49(Suppl 1):54–55.
            7. Henneke DR, Potter GD, Kreider JL. Body condition during pregnancy and lactation and reproductive efficiency of mares.. Theriogenology 1984;21:897–909.
            8. Kubiak JR, Crawford BH, Squires EL, Wrigley RH, Ward GM. The influence of energy intake and percentage of body fat on the reproductive performance of nonpregnant mares.. Theriogenology 1987 Nov;28(5):587-98.
              doi: 10.1016/0093-691X(87)90275-5pubmed: 16726341google scholar: lookup
            9. Koskinen E, Katila T. Onset of luteal activity in non-foaling mares during the early breeding season in Finland.. Acta Vet Scand 1991;32(3):319-25.
              pmc: PMC8127913pubmed: 1814181doi: 10.1186/bf03546961google scholar: lookup
            10. Gentry LR, Thompson DL Jr, Gentry GT Jr, Davis KA, Godke RA, Cartmill JA. The relationship between body condition, leptin, and reproductive and hormonal characteristics of mares during the seasonal anovulatory period.. J Anim Sci 2002 Oct;80(10):2695-703.
              pubmed: 12413093doi: 10.2527/2002.80102695xgoogle scholar: lookup
            11. Driancourt MA, Palmer E. Seasonal and individual effects on ovarian and endocrine responses of mares to a synchronization treatment with progestagen-impregnated vaginal sponges.. J Reprod Fertil Suppl 1982;32:283-91.
              pubmed: 6820062
            12. Palmer E, Driancourt MA. Some Interactions of Season of Foaling, Photoperiod and Ovarian Activity in the Equine.. Livest Prod Sci 1983. pp. 197–210.
            13. Koskinen E, Kurki E, Katila T. Onset of luteal activity in foaling and seasonally anoestrous mares treated with artificial light.. Acta Vet Scand 1991;32(3):307-12.
              pmc: PMC8127909pubmed: 1814179doi: 10.1186/bf03546959google scholar: lookup
            14. Fitzgerald BP, McManus CJ. Photoperiodic versus metabolic signals as determinants of seasonal anestrus in the mare.. Biol Reprod 2000 Jul;63(1):335-40.
              doi: 10.1095/biolreprod63.1.335pubmed: 10859276google scholar: lookup
            15. Crowe MA. Resumption of ovarian cyclicity in post-partum beef and dairy cows.. Reprod Domest Anim 2008 Nov;43 Suppl 5:20-8.
            16. Crowe MA, Goulding D, Baguisi A, Boland MP, Roche JF. Induced ovulation of the first postpartum dominant follicle in beef suckler cows using a GnRH analogue.. J Reprod Fertil 1993 Nov;99(2):551-5.
              doi: 10.1530/jrf.0.0990551pubmed: 8107039google scholar: lookup
            17. Armstrong JD, Britt JH. Nutritionally-induced anestrus in gilts: metabolic and endocrine changes associated with cessation and resumption of estrous cycles.. J Anim Sci 1987 Aug;65(2):508-23.
              pubmed: 3114207doi: 10.2527/jas1987.652508xgoogle scholar: lookup
            18. Gentry LR, Thompson DL Jr, Gentry GT Jr, Davis KA, Godke RA. High versus low body condition in mares: interactions with responses to somatotropin, GnRH analog, and dexamethasone.. J Anim Sci 2002 Dec;80(12):3277-85.
              pubmed: 12542169doi: 10.2527/2002.80123277xgoogle scholar: lookup
            19. Schneider JE, Friedenson DG, Hall AJ, Wade GN. Glucoprivation induces anestrus and lipoprivation may induce hibernation in Syrian hamsters.. Am J Physiol 1993 Mar;264(3 Pt 2):R573-7.
            20. Goubillon ML, Thalabard JC. Insulin-induced hypoglycemia decreases luteinizing hormone secretion in the castrated male rat: involvement of opiate peptides.. Neuroendocrinology 1996 Jul;64(1):49-56.
              doi: 10.1159/000127097pubmed: 8811666google scholar: lookup
            21. Cagampang FR, Cates PS, Sandhu S, Strutton PH, McGarvey C, Coen CW, O'Byrne KT. Hypoglycaemia-induced inhibition of pulsatile luteinizing hormone secretion in female rats: role of oestradiol, endogenous opioids and the adrenal medulla.. J Neuroendocrinol 1997 Nov;9(11):867-72.
            22. Downing JA, Scaramuzzi RJ. The effect of the infusion of insulin during the luteal phase of the estrous cycle on the ovulation rate and on plasma concentrations of LH, FSH and glucose in ewes.. Theriogenology 1997 Feb;47(3):747-59.
              doi: 10.1016/S0093-691X(97)00031-9pubmed: 16728025google scholar: lookup
            23. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW. Central nervous system control of food intake and body weight.. Nature 2006 Sep 21;443(7109):289-95.
              doi: 10.1038/nature05026pubmed: 16988703google scholar: lookup
            24. Buff PR, Dodds AC, Morrison CD, Whitley NC, McFadin EL, Daniel JA, Djiane J, Keisler DH. Leptin in horses: tissue localization and relationship between peripheral concentrations of leptin and body condition.. J Anim Sci 2002 Nov;80(11):2942-8.
              pubmed: 12462262doi: 10.2527/2002.80112942xgoogle scholar: lookup
            25. Chen K, Li F, Li J, Cai H, Strom S, Bisello A, Kelley DE, Friedman-Einat M, Skibinski GA, McCrory MA, Szalai AJ, Zhao AZ. Induction of leptin resistance through direct interaction of C-reactive protein with leptin.. Nat Med 2006 Apr;12(4):425-32.
              doi: 10.1038/nm1372pubmed: 16582918google scholar: lookup
            26. Adam CL, Findlay PA, Miller DW. Blood-brain leptin transport and appetite and reproductive neuroendocrine responses to intracerebroventricular leptin injection in sheep: influence of photoperiod.. Endocrinology 2006 Oct;147(10):4589-98.
              doi: 10.1210/en.2006-0576pubmed: 16794008google scholar: lookup
            27. Henry BA, Goding JW, Tilbrook AJ, Dunshea FR, Clarke IJ. Intracerebroventricular infusion of leptin elevates the secretion of luteinising hormone without affecting food intake in long-term food-restricted sheep, but increases growth hormone irrespective of bodyweight.. J Endocrinol 2001 Jan;168(1):67-77.
              doi: 10.1677/joe.0.1680067pubmed: 11139771google scholar: lookup
            28. Polkowska J, Wójcik-Gładysz A, Wańkowska M. The effect of intracerebroventricular infusions of leptin on the immunoreactivity of neuropeptide Y and gonadotrophin releasing hormone neurons in the hypothalamus of prepubertal sheep in conditions of short fasting.. J Chem Neuroanat 2006 Aug;32(1):65-73.
            29. Scacchi M, Pincelli AI, Cavagnini F. Nutritional status in the neuroendocrine control of growth hormone secretion: the model of anorexia nervosa.. Front Neuroendocrinol 2003 Jul;24(3):200-24.
              doi: 10.1016/S0091-3022(03)00014-1pubmed: 14596812google scholar: lookup
            30. Hull KL, Harvey S. GH as a co-gonadotropin: the relevance of correlative changes in GH secretion and reproductive state.. J Endocrinol 2002 Jan;172(1):1-19.
              pubmed: 11786370doi: 10.1677/joe.0.1720001google scholar: lookup
            31. Cingel-Ristic V, Van Neck JW, Frystyk J, Drop SL, Flyvbjerg A. Administration of human insulin-like growth factor-binding protein-1 increases circulating levels of growth hormone in mice.. Endocrinology 2004 Sep;145(9):4401-7.
              doi: 10.1210/en.2003-1742pubmed: 15166120google scholar: lookup
            32. Popot MA, Bobin S, Bonnaire Y, Delahaut PH, Closset J. IGF -I plasma concentrations in non-treated horses and horses administered with methionyl equine somatotropin.. Res Vet Sci 2001 Dec;71(3):167-73.
              doi: 10.1053/rvsc.2001.0505pubmed: 11798290google scholar: lookup
            33. Ortavant R, Bocquier F, Pelletier J, Ravault JP, Thimonier J, Volland-Nail P. Seasonality of reproduction in sheep and its control by photoperiod.. Aust J Biol Sci 1988;41(1):69-85.
              pubmed: 3077741
            34. Chemineau P, Pelletier J, Guérin Y, Colas G, Ravault JP, Touré G, Almeida G, Thimonier J, Ortavant R. Photoperiodic and melatonin treatments for the control of seasonal reproduction in sheep and goats.. Reprod Nutr Dev (1980) 1988;28(2B):409-22.
              pubmed: 3413339doi: 10.1051/rnd:19880307google scholar: lookup
            35. Lincoln GA, Short RV. Seasonal breeding: nature's contraceptive.. Recent Prog Horm Res 1980;36:1-52.
            36. Freedman LJ, Garcia MC, Ginther OJ. Influence of photoperiod and ovaries on seasonal reproductive activity in mares.. Biol Reprod 1979 Apr;20(3):567-74.
              doi: 10.1095/biolreprod20.3.567pubmed: 572238google scholar: lookup
            37. Palmer E. Reproductive management of mares without detection of oestrus.. J Reprod Fertil Suppl 1979;(27):263-70.
              pubmed: 289799
            38. Miller KF, Berg SL, Sharp DC, Ginther OJ. Concentrations of circulating gonadotropins during various reproductive states in mares.. Biol Reprod 1980 May;22(4):744-50.
              doi: 10.1095/biolreprod22.4.744pubmed: 6772244google scholar: lookup
            39. Kooistra LH, Ginther OJ. Effect of photoperiod on reproductive activity and hair in mares.. Am J Vet Res 1975 Oct;36(10):1413-9.
              pubmed: 1238038
            40. Guillaume D, Palmer E. Effect of oral melatonin on the date of the first ovulation after ovarian inactivity in mares under artificial photoperiod.. J Reprod Fertil Suppl 1991;44:249-57.
              pubmed: 1795267
            41. Guillaume D, Arnaud G, Camillo F, Duchamp G, Palmer E. Effect of melatonin implants on reproductive status of mares.. Biol Reprod 1995;1:435–442 Monograph Series.
            42. McManus CJ, Fitzgerald BP. Effect of daily clenbuterol and exogenous melatonin treatment on body fat, serum leptin and the expression of seasonal anestrus in the mare.. Anim Reprod Sci 2003 Apr 15;76(3-4):217-30.
              doi: 10.1016/S0378-4320(02)00246-4pubmed: 12586494google scholar: lookup
            43. Peltier MR, Robinson G, Sharp DC. Effects of melatonin implants in pony mares. 2. Long-term effects.. Theriogenology 1998 Apr 15;49(6):1125-42.
              doi: 10.1016/S0093-691X(98)00061-2pubmed: 10732051google scholar: lookup
            44. Sharp DC, Vernon MW, Zavy MT. Alteration of seasonal reproductive patterns in mares following superior cervical ganglionectomy.. J Reprod Fertil Suppl 1979;(27):87-93.
              pubmed: 289844
            45. Grubaugh W, Sharp DC, Berglund LA, McDowell KJ, Kilmer DM, Peck LS, Seamans KW. Effects of pinealectomy in Pony mares.. J Reprod Fertil Suppl 1982;32:293-5.
              pubmed: 6962863
            46. Palmer E, Driancourt MA, Ortavant R. Photoperiodic stimulation of the mare during winter anoestrus.. J Reprod Fertil Suppl 1982;32:275-82.
              pubmed: 6820061
            47. Scraba ST, Ginther OJ. Effects of lighting programs on onset of the ovulatory season in mares.. Theriogenology 1985;24:667–679.
            48. Guillaume D, Duchamp G, Nagy P, Palmer E. Determination of minimum light treatment required for photostimulation of winter anoestrous mares.. J Reprod Fertil Suppl 2000;(56):205-16.
              pubmed: 20681132
            49. Karsch FJ, Robinson JE, Woodfill CJ, Brown MB. Circannual cycles of luteinizing hormone and prolactin secretion in ewes during prolonged exposure to a fixed photoperiod: evidence for an endogenous reproductive rhythm.. Biol Reprod 1989 Dec;41(6):1034-46.
              doi: 10.1095/biolreprod41.6.1034pubmed: 2624864google scholar: lookup
            50. H N, I E. Notation de l'état corporel des chevaux de selle et de sport.. INRA. Guide pratique. Eds Institut Elevage Publishing 149 rue de Bercy 75595 Paris, France 1997.
            51. Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares.. Equine Vet J 1983 Oct;15(4):371-2.
            52. Vermorel M, Garrige R, Martin-Rosset W. Métabolisme et besoin énergétiques du cheval, le système des UFC.. In: 13eme Journée du Grenier de Theix. Eds INRA Publishing Versailles, France, editor 1981. pp. 239–276. Clermont-ferrand.
            53. Martin-Rosset W, Vermorel M, Doreau M, Tisserand V, Andrieu J. The French horse feed evaluation systems and recommended allowances for energy and protein.. Livest Prod Sci 1994;40:37–56.
            54. Vermorel M, Vernet J, Martin-Rosset W. Digestive and energy utilisation of two diets by ponies and horses.. Livest Prod Sci 1997;51:13–19.
            55. Terqui M, Thimonier J. [New rapid radioimmunologic method for estimation of plasma progesterone. Application to early diagnosis of gestation in the ewe and goat].. C R Acad Hebd Seances Acad Sci D 1974 Sep 23;279(13):1109-12.
              pubmed: 4219319
            56. Tillet Y, Ravault JP, Selve C, Evin G, Castro B, Dubois MP. [Conditions for the use of specific antibodies for immunohistochemical visualization of serotonin and melatonin in the pineal gland of sheep].. C R Acad Sci III 1986;303(3):77-82.
              pubmed: 3093008
            57. Kadish AH, Little RL, Sternberg JC. A New and rapid method for the determination of glucose by measurement of oxygen consumption rate.. Clin Chem 1968;14:144–116.
            58. Guillaume D, Chavatte-Palmer P, Combarnous Y, Duchamp G, Martinat N, Nagy P, Daels PF. Induced lactation with a dopamine antagonist in mares: different responses between ovariectomized and intact mares.. Reprod Domest Anim 2003 Oct;38(5):394-400.
            59. Delavaud C, Bocquier F, Chilliard Y, Keisler DH, Gertler A, Kann G. Plasma leptin determination in ruminants: effect of nutritional status and body fatness on plasma leptin concentration assessed by a specific RIA in sheep.. J Endocrinol 2000 May;165(2):519-26.
              doi: 10.1677/joe.0.1650519pubmed: 10810316google scholar: lookup
            60. Agresti A. Categorical data analysis.. John Willey and Sons Press New-York 1990.
            61. FREEMAN GH, HALTON JH. Note on an exact treatment of contingency, goodness of fit and other problems of significance.. Biometrika 1951 Jun;38(1-2):141-9.
              pubmed: 14848119
            62. Gibbons JD. Nonparametric statistical inference. 2.. Dekker Press New-York 1985.
            63. Littell RC, Henry PR, Ammerman CB. Statistical analysis of repeated measures data using SAS procedures.. J Anim Sci 1998 Apr;76(4):1216-31.
              pubmed: 9581947doi: 10.2527/1998.7641216xgoogle scholar: lookup
            64. Bossis I, Wettemann RP, Welty SD, Vizcarra J, Spicer LJ. Nutritionally induced anovulation in beef Heifers: ovarian and endocrine function during realimentation and resumption of ovulation.. Biol Reprod 2000 May;62(5):1436-44.
              doi: 10.1095/biolreprod62.5.1436pubmed: 10775198google scholar: lookup
            65. Tanaka T, Yamaguchi T, Kamomae H, Kaneda Y. Nutritionally induced body weight loss and ovarian quiescence in Shiba goats.. J Reprod Dev 2003 Feb;49(1):113-9.
              doi: 10.1262/jrd.49.113pubmed: 14967956google scholar: lookup
            66. Zarazaga LA, Guzmán JL, Domínguez C, Pérez MC, Prieto R. Effect of plane of nutrition on seasonality of reproduction in Spanish Payoya goats.. Anim Reprod Sci 2005 Jul;87(3-4):253-67.
            67. Miller KK, Grinspoon S, Gleysteen S, Grieco KA, Ciampa J, Breu J, Herzog DB, Klibanski A. Preservation of neuroendocrine control of reproductive function despite severe undernutrition.. J Clin Endocrinol Metab 2004 Sep;89(9):4434-8.
              doi: 10.1210/jc.2004-0720pubmed: 15356043google scholar: lookup
            68. Miller DW, Harrison JL, Bennett EJ, Findlay PA, Adam CL. Nutritional influences on reproductive neuroendocrine output: insulin, leptin, and orexigenic neuropeptide signaling in the ovine hypothalamus.. Endocrinology 2007 Nov;148(11):5313-22.
              doi: 10.1210/en.2007-0534pubmed: 17702844google scholar: lookup
            69. Allen WR. Endogenous hormonal control of the mare's oestrus cycle.. Proceedings of the Bain-Fallon Memorial 1987, Lectures pp. 2–13.
            70. Carnevale EM, Hermenet MJ, Ginther OJ. Age and pasture effects on vernal transition in mares.. Theriogenology 1997 Apr 1;47(5):1009-18.
              doi: 10.1016/S0093-691X(97)00058-7pubmed: 16728051google scholar: lookup
            71. van Niekerk FE, van Niekerk CH. The effect of dietary protein on reproduction in the mare. III. Ovarian and uterine changes during the anovulatory, transitional and ovulatory periods in the non-pregnant mare.. J S Afr Vet Assoc 1997 Sep;68(3):86-92.
              pubmed: 9408893doi: 10.4102/jsava.v68i3.882google scholar: lookup
            72. Rhind SM, McNeilly AS. Effects of level of food intake on ovarian follicle number, size and steroidogenic capacity in the ewe.. Anim Reprod Sci 1998 Aug 21;52(2):131-8.
              doi: 10.1016/S0378-4320(98)00097-9pubmed: 9776486google scholar: lookup
            73. Nagy P, Huszenicza Gy, Juhasz J, Solti L, Kulcsar M. Diagnostic problems associated with ovarian activity in barren and postpartum mares early in the breeding season.. Reproduction in Domestic Animals 1998;33:187–192.
            74. Martin GB, Hötzel MJ, Blache D, Walkden-Brown SW, Blackberry MA, Boukhliq RC, Fisher JS, Miller DW. 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 2002;14(3-4):165-75.
              doi: 10.1071/RD02010pubmed: 12219938google scholar: lookup
            75. Gu J, Orr N, Park SD, Katz LM, Sulimova G, MacHugh DE, Hill EW. A genome scan for positive selection in thoroughbred horses.. PLoS One 2009 Jun 2;4(6):e5767.
            76. Jousse C, Parry L, Lambert-Langlais S, Maurin AC, Averous J, Bruhat A, Carraro V, Tost J, Letteron P, Chen P, Jockers R, Launay JM, Mallet J, Fafournoux P. Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome.. FASEB J 2011 Sep;25(9):3271-8.
              doi: 10.1096/fj.11-181792pubmed: 21670064google scholar: lookup
            77. Sharp DC, Grubaugh W, Zavy MT, Vernon MW. Seasonal variation in melatonin secretory patterns in mares [abstract]. J Anim Sci 1980;51(Suppl 1):327–328.
            78. Guerin MV, Deed JR, Kennaway DJ, Matthews CD. Plasma melatonin in the horse: measurements in natural photoperiod and in acutely extended darkness throughout the year.. J Pineal Res 1995 Aug;19(1):7-15.
            79. Guillaume D, Rio N, Toutain PL. Kinetic studies and production rate of melatonin in pony mares.. Am J Physiol 1995 May;268(5 Pt 2):R1236-41.
            80. Fitzgerald BP, Schmidt MJ. Absence of an association between melatonin and reproductive activity in mares during the nonbreeding season.. Biol Reprod Monograph 1995;1:425–434.
            81. Diekman MA, Braun W, Peter D, Cook D. Seasonal serum concentrations of melatonin in cycling and noncycling mares.. J Anim Sci 2002 Nov;80(11):2949-52.
              pubmed: 12462263doi: 10.2527/2002.80112949xgoogle scholar: lookup
            82. Sticker LS, Thompson DL Jr, Bunting LD, Fernandez JM, DePew CL. Dietary protein and(or) energy restriction in mares: plasma glucose, insulin, nonesterified fatty acid, and urea nitrogen responses to feeding, glucose, and epinephrine.. J Anim Sci 1995 Jan;73(1):136-44.
              pubmed: 7601726doi: 10.2527/1995.731136xgoogle scholar: lookup
            83. Short RE, Adams C. Nutritional and Hormonal Interrelationships in Beef Cattle Reproduction.. Can J Anim Sci 1988;68:29–39.
              doi: 10.4141/cjas88-003google scholar: lookup
            84. Daniel JA, Thomas MG, Hale CS, Simmons JM, Keisler DH. Effect of cerebroventricular infusion of insulin and (or) glucose on hypothalamic expression of leptin receptor and pituitary secretion of LH in diet-restricted ewes.. Domest Anim Endocrinol 2000 Feb;18(2):177-85.
              doi: 10.1016/S0739-7240(99)00077-6pubmed: 10764974google scholar: lookup
            85. Wettemann RP, Lents CA, Ciccioli NH, White FJ, Rubio I. Nutritional and suckling-mediated anovulation in beef cows.. J Anim Sci 2003;81:E48–E59.
            86. Randel RD. Nutrition and postpartum rebreeding in cattle.. J Anim Sci 1990 Mar;68(3):853-62.
              pubmed: 2180880doi: 10.2527/1990.683853xgoogle scholar: lookup
            87. Dhuyvetter DV, Caton JS. Manipulation of reproduction and lactation with supplementation in beef cattle. In: Am Soc Anim Sci. Suppl 1. Proc 3rd Grazing Livest. Nutr. Conf., MB Judkins, McCollum FT, III, ed. Proc West Sec, editor Vol. 47. 1996. pp. 83–93.
            88. Archer ZA, Rhind SM, Findlay PA, Kyle CE, Barber MC, Adam CL. Hypothalamic responses to peripheral glucose infusion in food-restricted sheep are influenced by photoperiod.. J Endocrinol 2005 Mar;184(3):515-25.
              doi: 10.1677/joe.1.06013pubmed: 15749810google scholar: lookup
            89. Unger JW, Moss AM, Livingston JN. Immunohistochemical localization of insulin receptors and phosphotyrosine in the brainstem of the adult rat.. Neuroscience 1991;42(3):853-61.
              doi: 10.1016/0306-4522(91)90049-Tpubmed: 1720228google scholar: lookup
            90. Miller DW, Blache D, Martin GB. The role of intracerebral insulin in the effect of nutrition on gonadotrophin secretion in mature male sheep.. J Endocrinol 1995 Nov;147(2):321-9.
              doi: 10.1677/joe.0.1470321pubmed: 7490562google scholar: lookup
            91. McManus CJ, Davison LA, Fitzgerald BP. Effect of 2-deoxy-D-glucose on gonadotropins, prolactin and serum glucose concentrations in the mare.. Anim Reprod Sci 2002 Jun 17;71(3-4):217-28.
              doi: 10.1016/S0378-4320(02)00030-1pubmed: 12047930google scholar: lookup
            92. Deichsel K, Hoppen HO, Bruckmaier R, Kolm G, Aurich C. Acute insulin-induced hypoglycaemia does not alter IGF-1 and LH release in cyclic mares.. Reprod Domest Anim 2005 Apr;40(2):117-22.
            93. Butler ST, Marr AL, Pelton SH, Radcliff RP, Lucy MC, Butler WR. Insulin restores GH responsiveness during lactation-induced negative energy balance in dairy cattle: effects on expression of IGF-I and GH receptor 1A.. J Endocrinol 2003 Feb;176(2):205-17.
              doi: 10.1677/joe.0.1760205pubmed: 12553869google scholar: lookup
            94. Breier BH. Regulation of protein and energy metabolism by the somatotropic axis.. Domest Anim Endocrinol 1999 Oct;17(2-3):209-18.
              doi: 10.1016/S0739-7240(99)00038-7pubmed: 10527124google scholar: lookup
            95. Piccione G, Bertolucci C, Foà A, Caola G. Influence of fasting and exercise on the daily rhythm of serum leptin in the horse.. Chronobiol Int 2004 May;21(3):405-17.
              doi: 10.1081/CBI-120038609pubmed: 15332446google scholar: lookup

            Citations

            This article has been cited 8 times.
            1. D'Fonseca NMM, Gibson CME, Hummel I, van Doorn DA, Roelfsema E, Stout TAE, van den Broek J, de Ruijter-Villani M. Overfeeding Extends the Period of Annual Cyclicity but Increases the Risk of Early Embryonic Death in Shetland Pony Mares. Animals (Basel) 2021 Feb 1;11(2).
              doi: 10.3390/ani11020361pubmed: 33535548google scholar: lookup
            2. Mellouk N, Rame C, Naquin D, Jaszczyszyn Y, Touzé JL, Briant E, Guillaume D, Ntallaris T, Humblot P, Dupont J. Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system. PLoS One 2019;14(9):e0222954.
              doi: 10.1371/journal.pone.0222954pubmed: 31557215google scholar: lookup
            3. Peugnet P, Robles M, Mendoza L, Wimel L, Dubois C, Dahirel M, Guillaume D, Camous S, Berthelot V, Toquet MP, Richard E, Sandersen C, Chaffaux S, Lejeune JP, Tarrade A, Serteyn D, Chavatte-Palmer P. Effects of moderate amounts of barley in late pregnancy on growth, glucose metabolism and osteoarticular status of pre-weaning horses. PLoS One 2015;10(4):e0122596.
              doi: 10.1371/journal.pone.0122596pubmed: 25875166google scholar: lookup
            4. Salazar-Ortiz J, Monget P, Guillaume D. The influence of nutrition on the insulin-like growth factor system and the concentrations of growth hormone, glucose, insulin, gonadotropins and progesterone in ovarian follicular fluid and plasma from adult female horses (Equus caballus). Reprod Biol Endocrinol 2014 Jul 31;12:72.
              doi: 10.1186/1477-7827-12-72pubmed: 25078409google scholar: lookup
            5. Peugnet P, Wimel L, Duchamp G, Sandersen C, Camous S, Guillaume D, Dahirel M, Dubois C, Jouneau L, Reigner F, Berthelot V, Chaffaux S, Tarrade A, Serteyn D, Chavatte-Palmer P. Enhanced or reduced fetal growth induced by embryo transfer into smaller or larger breeds alters post-natal growth and metabolism in pre-weaning horses. PLoS One 2014;9(7):e102044.
              doi: 10.1371/journal.pone.0102044pubmed: 25006665google scholar: lookup
            6. Dardente H, Hazlerigg DG, Ebling FJ. Thyroid hormone and seasonal rhythmicity. Front Endocrinol (Lausanne) 2014;5:19.
              doi: 10.3389/fendo.2014.00019pubmed: 24616714google scholar: lookup
            7. Khan IU, Khairullah AR, Khan AY, Rehman AU, Mustofa I. Strategic approaches to improve equine breeding and stud farm outcomes. Vet World 2025 Feb;18(2):311-328.
            8. Tkaczenko H, Lukash O, Kurhaluk N. Analysis of the season-dependent component in the evaluation of morphological and biochemical blood parameters in Shetland ponies of both sexes during exercise. J Vet Res 2024 Mar;68(1):155-166.
              doi: 10.2478/jvetres-2024-0017pubmed: 38525221google scholar: lookup