The influence of photoperiod on reproduction of male goat and ram
DOI:
https://doi.org/10.33448/rsd-v9i10.8243Keywords:
Circadian Rhythm; Gonadotropins; Melatonin; Seasonality; Testosterone.Abstract
Some animal species exhibit reproductive seasonality regulated mainly by the daily photoperiod, may be modulated by climate and food. This physiological characteristic is well known and prominent in females, where happens a period of breeding season and other anestrus. However, in males of species seasonal the reproductive variations are not considered sufficient to prevent reproduction throughout the year, but must consider such changes in some husbandry practices and decision making. The aim of this review is to evaluate the influence of photoperiod on reproduction of male goats and sheep, and also, possible actions of melatonin on sperm conservation directly and indirectly.
References
Abecia, J. A., Forcada, F., González-Bulnes, A. (2012). Hormonal control of reproduction in small ruminants. Animal Reproduction Science, 130, 173-179.
Agawal, A., Probakaran, A. S. (2005). Mechanism, measurements, and prevention of oxidative stress in male reproductive physiology. Indian Journal of Experimental Biology, 43, 963–974.
Aguirre, V., Orihuela, A., Vázquez, R. (2007). Effect of semen collection frequency on seasonal variation in sexual behaviour, testosterone, testicular size and semen characteristics of tropical hair rams (Ovis aries). Tropical Animal Health and Production, 39, 271–277.
Ahmad, N., Noakes, D. E. (1996). Seasonal variations in the semen quality of young british goats. British Veterinary Journal, 152, 225-236.
Amann, R. P., Hammerstedt, R. H., Shabanowitz, R. B. (1999). Exposure of human, boar, or bull sperm to a synthetic peptide increases binding to an egg-membrane substrate. Journal of Andrology, 20, 34–41.
Ashworth, P. J., Harrison, R. A., Miller, N. G., Plummer, J. M., Watson, P. F. (1994). Survival of ram spermatozoa at high dilution: protective effect of simple constituents of culture media as compared with seminal plasma. Reproduction, Fertility and Development, 6, 173–80.
Avdi, M., Banos, G., Stefos, K., Chemineau, P. (2004). Seasonal variation in testicular volume and sexual behavior of Chios and Serres rams. Theriogenology, 62, 275–282.
Azawi, O. I., Ismaeel, M. A. (2012). Effects of seasons on some semen parameters and bacterial contamination of Awassi ram Semen. Reproduction in Domestic Animals, 47, 403-406.
Azerêdo, G. A., Esper, C. R., Resende, K. T. (2001). Evaluation of plasma membrane integrity of frozen-thawed goat spermatozoa with or without seminal plasma. Small Ruminant Research, 41, 257–263.
Barbosa, O. R., Tutida, L., Hubler, M. R. N. O., Akimoto, L. S., Moraes, G. V. (1999). Influência das estações do ano nas concentrações séricas de 3,5,3’ triidotironina (T3), tiroxina (T4) e testosterona (Tes) de carneiros. Acta Scientiarum, 21(3), 599-605.
Barkawi, A. H., Elsayed, E. H., Ashour, G.; Shehata, E. (2006). Seasonal changes in semen characteristics, hormonal profiles and testicular activity in Zaraibi goats. Small Ruminant Research, 66, 209–213.
Barrios, B.; Pérez-Pé, R., Gallego, M., Tato, A.; Osada, J.; Muiño-Blanco, Cebrián-Pérez, J. A. (2000). Seminal plasma proteins revert the cold-shock damage on ram sperm membrane. Biology of Reproduction, 63, 1531–1537.
Barrios, B.; Fernández-Juan, M., Muiño-Blanco, T., Cebrián-Pérez, J. A. (2005). Immunocytochemical localization and biochemical characterization of two seminal plasma proteins that protect ram spermatozoa against cold shock. Journal of Andrology, 26, 539–549.
Bergeron, A., Villemure, M., Lazure, C., Manjunath, P. (2005). Isolation and Characterization of the major proteins of ram seminal plasma. Molecular Reproduction and Development, 71, 461–470.
Bendahmane, M., Lynch, C., Tulsiani, D. R. P. (2001). Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa. Archives of Biochemistry and Biophysics, 390, 1–8.
Benitez-King, G., Anton-Tay, F. (1993). Calmodulin mediates melatonin cytoskeletal effects. Experientia, 49, 35–41.
Boggio, V., Cutrera, R., Carbone, S., Scacchi, P., Ponzo, O. J. (2013). Leptin inhibits the reproductive axis in adult male Syrian hamsters exposed to long and short photoperiod. Reproductive Biology, 13, 203–208.
Casao, A., Luna, C.; Serrano, E. (2009). Quantification of melatonin on oxidized proteins and lipids in ram Semen in the breeding and non-breeding season. XIII Jornadas sobre Produccion Animal, AIDA: Zaragoza, Spain, 723–725.
Casao, A., Veja, S., Palacín, I., Pérez-Pé, R., Laviña, A., Quintín, F. J., Sevilla, E., Abecia, J. A.; Cebrián-Pérez, J. A., Forcada, F., Muiño-Blanco, T. (2010). Effects of melatonin implants during non-breeding season on sperm motility and reproductive parameters in Rasa Aragonesa rams. Reproduction in Domestic Animals, 45, 425–432.
Casao, A., Cebrián, I., Asumpção, M. E., Pérez-Pé, R., Abecia, J. A., Forcada, F., Pérez-Cebrián, J. A., Muiño-Blanco, T. (2010b). Seasonal variations of melatonin in ram seminal plasma are correlated to those of testosterone and antioxidant enzymes. Reproductive Biology and Endocrinology, 8(59), 1-9, 2010.
Casao, A., Mendoza, N., Pérez-Pé, R., Grasa, P., Abecia, J. A., Forcada, F., Cebrián-Pérez, J. A., Muiño-Blanco, T. (2010c). Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate. Journal of Pineal Research, 48, 39–46.
Casao, A., Gallego, M., Abecia, J. A., Forcada, F., Pérez-Pé, R., Muiño-Blanco, T.; Cebrián-Pérez, J. A. (2012). Identification and immunolocalisation of melatonin MT(1) and MT(2) receptors in Rasa aragonesa ram spermatozoa. Reproduction, Fertility and Development, 24, 953–961.
Casao, A., Pérez-Pé, R., Abecia, J. A., Forcada, F., Muiño-Blanco, T., Cebrián-Pérez, J. A. (2013). The effect of exogenous melatonin during the non-reproductive season on the seminal plasma hormonal profile and the antioxidant defence system of Rasa Aragonesa rams. Animal Reproduction Science, 138, 168–174.
Chaves, E. M., Aguilea-Merlo, C., Cruceño A., Fogal, T., Piezzi, R., Scardapane, L.; Dominguez, S. (2012). Seasonal morphological variations and age-related changes of the seminal vesicle of viscacha (Lagostomus maximus maximus): an ultrastructural and immunohistochemical study. The Anatomical Record, 295, 886–895.
Chenoweth, P. J. (1981). Libido and mating behavior in bulls, boars and rams. A review. Theriogenology, 16, 155-177.
Clarke, I. J., Smith, J. T., Caraty, A., Goodman, R. L., Lehman, M. N. (2009). Kisspetin and seasonality in sheep. Peptides, 30, 154-163.
Coloma, M. A., Toledano-Díaz, A., López-Sebastian, A., Santiago-Moreno, J. (2010). The influence of washing Spanish ibex (Capra pyrenaica) sperm on the effects of cryopreservation in dependency of the photoperiod. Theriogenology, 73, 900–908.
Cross, N. L. (1996). Human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist, progesterone: cholesterol is the major inhibitor. Biology of Reproduction, 54, 138–45.
Desnoyers, L., Manjunath, P. (1992). Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. The Journal of Biological Chemistry, 267, 10149–10155.
Dickson, K. A., Sanford, L. M. (2005). Breed diversity in FSH, LH and testosterone regulation of testicular function and in libido of young adult rams on the south eastern Canadian prairies. Small Ruminant Research, 56, 189–203.
Domínguez, M. P., Falcinelli, A., Hozbor, F., Sánchez, E., Cesari, A., Alberio, R. H. (2008). Seasonal variations in the composition of ram seminal plasma and its effect on frozen-thawed ram sperm. Theriogenology, 69, 564–573.
Du Plessis, S. S., Hagenaar, K., Lampiao, F. (2010). The in vitro effects of melatonin on human sperm function and its scavenging activities on NO and ROS. Andrologia, 42, 112–116.
Escott, G. M., Da Rosa, L. A., Loss, E. S. (2011/2). Regulação hormonal do transporte de glicose e aminoácido e sua relação com as funções e o desenvolvimento das células de Sertoli: uma revisão. Ciência em Movimento, 27, 85-98.
Espino, J., Bejarano, I., Ortiz, A., Lozano, G. M., Garcia, J. F., Pariente, J. A.; Rodriguez, A. B. (2010). Melatonin as a potential tool against oxidative damage and apoptosis in ejaculated human spermatozoa. Fertility and Sterility, 94, 1915–1917.
Evans, G., Maxwel, W. M. C. (1987). Artificial insemination of sheep and goats. Butterworth Publishers, 53, 25-29.
Fernandez-Juan, M., Gallego, M., Barrios, B., Osada, J.; Cebrián-Pérez, J. A.; Muiño-Blanco, T. (2006). Immunohistochemical localization of sperm preserving proteins in the ram reproductive tract. Journal of Andrology, 27, 588–595.
Fujinoki, M., Suzuki, T., Takayama, T., Shibahara, H., Ohtake, H. (2006). Profiling of proteins phosphorylated or dephosphorylated during hyperactivation via activation on hamster spermatozoa. Reproduction Medicine and Biology, 5, 123–135.
Fujinoki, M. (2008). Melatonin-enhanced hyperactivation of hamster sperm. Reproduction, 136, 533–541.
Garcia, J. J., Reiter, R. J., Guerrero, J. M., Escames, G., Yu, B. P., Oh, C. S., Muñoz-Hoyos, A. (1997). Melatonin prevents changes in microsomal membrane fluidity during induced lipid peroxidation. FEBS Letters, 408, 297–300.
Gardner, D. L.; Hafez, E. S. E. (2004). Espermatozoide e plasma seminal. In: Hafez, E. S. E. & Hafez, B. (Ed.) Reprodução Animal. 7.ed. São Paulo: Manole, 97-110.
Graham J. (1994). Effect of seminal plasma on the motility of the epididymal and ejaculated spermatozoa of the ram and bull during the cryopreservation process. Theriogenology, 41, 1151–1162.
Goldman, B. D. (2001). Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. Journal of Biological Rhythms, 16, 283-301.
Gündogan, M. (2007). Seasonal variation in serum testosterone, T3 and andological parameters of two Turkish sheep breeds. Small Ruminant Research, 67, 312-316.
Iritani, A.; Nishikawa, Y. (1963). Studies on the egg-coagulating enzyme in goat semen; IV. On the position of yolk consitituents attacked by the coagulating enzyme. Japanese Journal of Animal Reproduction, 8, 113–117.
Itoh, M. T.; Ishizuka, B.; Kuribayashi, Y.; Amemiya, A.; Sumi, Y. (1999). Melatonin, its precursors, and synthesizing enzyme activities in the human ovary. Molecular Human Reproduction, 5, 402–408.
Johnson, L. A. (2000). Sexing mammalian sperm for production of offspring: the state-of-the-art. Animal Reproduction Science, 60–61, 93–107, .
Jou, M. J.; Peng, T. I.; Yu, P. Z.; Jou, S. B.; Reiter, R. J.; Chen, J. Y.; Wu, H. Y.; Chen, C. C.; Hsu, L. F. (2007). Melatonin protects against common deletion of mitochondrial DNA-augmented mitochondrial oxidative stress and apoptosis. Journal of Pineal Research, 43, 389–403.
Kafi, M.; Safdarian, M.; Hashemi, M. (2004). Seasonal variation in semen characteristics, scrotal circumference and libido of Persian Karakul rams. Small Ruminant Research, 53, 133–139.
Kamp, G.; Busselmann, G.; Lauterwein, J. (1996). Spermatozoa: models for studying regulatory aspects of energy metabolism. Experientia, 52, 487-494.
Karagiannidis, A.; Varsakeli, S.; Alexopoulos, C.; Amarantidis, I. (2000). Seasonal variation in semen characteristics of Chios and Friesian rams in Greece. Small Ruminant Research, 37, 125-130.
Karaginnidis, A.; Varsakeli, S.; Karatzas, G. (2000). Characteristics and seasonal variations in the semen of alpine, seamen and Damascus goat bucks born and raised in Greece. Theriogenology, 53, 1285-1293.
Kaya, A.; Aksoy, M.; Baspinar, N.; Yildiz, C.; Ataman, M. B. (2001). Effect of melatonin implantation to sperm donor rams on post-thaw viability and acrosomal integrity of sperm cells in the breeding and non-breeding season. Reproduction in Domestic Animals, 36, 211–215.
Kumar, A.; Farooq, A. (1994). Effect of oxytocin on the concentration of fructose in the accessory glands of mouse. Life Sciences, 55, 19-24.
Kurcer, Z.; Hekimoglu, A.; Aral, F.; Baba, F.; Sahna, E. (2010). Effect of melatonin on epididymal sperm quality after testicular ischemia/reperfusion in rats. Fertility and Sterility, 93, 1545–1549.
Leon, J.; Acuña-Castroviejo, D.; Sainz, R. M.; Mayo, J. C.; Tan, D. X.; Reiter, R. J. (2004). Melatonin and mitochondrial function. Life Sciences, 75, 765–790.
Li, L.; Xu, J. N.; Wong, Y. H.; Wong, J. T. Y.; Pang, S. F.; Shiu, S. Y. W. (1998). Molecular and cellular analyses of melatonin receptor-mediated cAMP signaling in rat corpus epididymis. Journal of Pineal Research, 25, 219–228.
Li, L.; Wong, J. T. Y.; Pang, S. F.; Shiu, S. Y. W. (1999). Melatonin-induced stimulation of rat corpus epididymal epithelial cell proliferation. Life Sciences, 65, 1067–1076, .
Li, X. X.; Yang, X. G.; Lu, Y. Q.; Lu, S. S.; Zhang, M.; Yao, H. I.; Meng, L. J.; Lu, K. H. (2012). Protective effects of melatonin against oxidative stress in flow cytometry-sorted buffalo sperm. Reproduction in Domestic Animals, 47, 299–307.
Lincoln, G. A.; Lincoln, C. E.; 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. Journal of Reproduction and Fertility, 88, 623-633.
Lincoln, G. A.; Clarke, I. J. (1997). Refractoriness to a static melatonin signal develops in the pituitary gland for the control of prolactin secretion in the ram. Biology of Reproduction, 57, 460–467.
Martin, M.; Macías, M.; Escames, G.; Reiter, R. J.; Agapito, M. T.; Ortiz, G. G.; Acuña-Castroviejo, D. (2000). Melatonin-induced increased activity of the respiratory chain complexes I and IV can prevent mitochondrial damage induced by ruthenium red in vivo. Journal of Pineal Research, 28, 242–248.
Martin, M.; Macías, M.; León, J.; Escames, G.; Khaldy, H.; Acuña-Castroviejo, D. (2002). Melatonin increases the activity of oxidative phosphorylation enzymes and the production of ATP in rat brain and liver mitochondria. The International Journal of Biochemistry and Cell Biology, 34, 348–357.
Martin-Hildago, D.; Barón, F. J.; Bragado, M. J.; Carmona, P.; Robina, A.; García-Marín, L. J.; Gil, M. C. (2011). The effect of melatonin on the quality of extended boar semen after long-term storage at 17 °C. Theriogenology, 75, 1550–1560.
Malpaux, B.; Migaud, M.; Tricoire, H.; Chemineau, P. (2001). Biology of mammalian photoperiodism and critical role of pineal gland and melatonin. Journal of Biological Rhythms, 16, 336-347.
Malpaux, B. (2006). Seasonal regulation of reproduction in mammals. In: NEILL, J. D. & Knobil, E. (Ed.). Physiology of Reproduction. 3. ed. London: Elsevier, 2231–2281.
Matsuoka, T.; Imai, H.; Asakuma, S.; Kohno, H.; Fukui, Y. (2006). Changes of fructose concentrations in seminal plasma and glucose and testosterone concentrations in blood plasma in rams over the course of a year. Journal of Reproduction and Development, 52(6), 805-810.
Maxwell, W. M. C.; Graaf, S. P.; Ghaoui, R. E. H.; Evans, G. (2007). Seminal plasma effects on sperm handling and female fertility. Society for Reproduction and Fertility. Supplement, 64, 13–38.
Memon, M. A.; Bretzlaff, K. N.; Ott, R. S. (1985). Effect of washing on motility and acrosome morphology of frozen-thawed goat spermatozoa. American Journal of Veterinary Research, 46, 473–475.
Metz, K. W.; Berger, T.; Clegg, E. D. (1990). Adsorption of seminal plasma proteins by boar spermatozoa. Theriogenology, 34, 691–700.
Nagy, P.; Guillaume, P.; Daels, P. (2000). Seasonality in mares. Animal Reproduction Science, 60-61, 245-262.
Odonnell, L.; Mclachlan, R. I.; Wreford, N. G.; Robertson, D. M. (1994). Testosterone promotes the conversion of round spermatis between stages VII and VIII of the rat spermatogenic cycle. Endocrinology, 135, 2608-2614.
Ortega Ferrusola, C.; González Fernández, L.; Macías García, B.; Salazar-Sandoval, C.; Morillo Rodríguez, A.; Rodríguez Martinez, H.; Tapia, J. A.; Peña, F. J. (2009). Effect of cryopreservation on nitric oxide production in stallion spermatozoa. Biology of Reproduction, 81, 1106–1111.
Pelletier, J.; Almeida, G. (1987). Short light cycles induce persistent reproductive activity in Ile-de-France rams. Journal of Reproduction and Fertility. Supplement, 34, 215–226.
Pellicer-Rubio, M. T., Combarnous, Y. (1998). Deterioration of goat spermatozoa in skimmed milk-based extenders as a result of oleic acid released by the bulbourethral lipase BUSgp60. Journal of Reproduction and Fertility, 112, 95–105.
Pereira, A. S., Shitsuka, D. M., Parreira, F. J., & Shitsuka, R. (2018). Metodologia da pesquisa científica. [e-book]. Santa Maria. Ed. UAB/NTE/UFSM. Recuperado de https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computacao_MetodologiaPesquisa-Cientifica.pdf?sequence=1.
Pérez-Pé, R.; Cebrián-Pérez, J. A.; Muiño-Blanco, T. (2001). Semen plasma proteins prevent cold-shock membrane damage to ram spermatozoa. Theriogenology, 56, 425–434.
Pozo, D.; Reiter, R. J.; Calvo, J. R.; Guerrero, J. M. (1997). Inhibition of cerebellar nitric oxide synthase and cyclic GMP production by melatonin via complex formation with calmodulin. Journal of Cellular Biochemistry, 65, 430–442.
Rao, M. V.; Gangadharan, B. (2008). Antioxidant potential of melatonin against mercury induced intoxication in spermatozoa in vitro. Toxicology in Vitro, 22, 935–942.
Reiter, R. J. (1975). Exogenous and endogenous control of the annual reproductive cycle in the male golden hamster: participation of the pineal gland. Journal of Experimental Zoology, 191, 111–120.
Reiter, R. J.; Rosales-Corral, S. A.; Manchester, L. C.; Tan, D. X. (2013). Peripheral reproductive organ health and melatonin: ready for prime time. International Journal of Molecular Sciences, 14, 7231-7272.
Rigau, T.; Farré, M.; Ballester, J.; Mogas, T.; Peña, A.; Rodríguez-Gil, J. E. (2001). Effects of glucose and fructose on motility patterns of dog spermatozoa from fresh ejaculates. Theriogenology, 56, 801-815.
Rigau, T.; Rivera, M.; Palomo, M. J.; Fernández-Novell, J. M.; Mogas, T.; Ballester, J.; Peña, A.; Otaegui, P. J.; Guinovart, J. J.; Rodríguez-Gil, J. E. (2002). Differential effects of glucose and fructose on hexose metabolism in dog spermatozoa. Reproduction, 123, 579-591.
Ritar, A. J; Salamon, S. (1991). Effects of month of collection, method of processing, concentration of egg yolk and duration of frozen storage on viability of Angora goat spermatozoa. Small Ruminant Research, 4, 29–37.
Ritar, A. J., Salamon, S. (1982). Effects of seminal plasma and of its removal and of egg yolk in the diluent on the survival of fresh and frozen-thawed spermatozoa of the Angora goat. Australian Journal of Biological Sciences, 35, 305–312.
Roca, J; Martinez, E.; Vazquez, J. M.; Coy, P. (1992). Characteristics and seasonal variations in the semen of Murciano-Granadina goats in the Mediterranean area. Animal Reproduction Science, 29, 255-262.
Rodriguez, C.; Mayo, J. C.; Sainz, R. M.; Antolín, I.; Herrera, F.; Martín, V.; Reiter, R. J. (2004). Regulation of antioxidant enzymes: a significant role for melatonin. Journal Pineal Research, 36, 1–9.
Rosa, H. J. D.; Juniper, D. T.; Bryant, M. J. (2000). Effects of recent sexual experience and melatonin treatment of rams on plasma testosterone concentrations, sexual behavior and ability to induce ovulation in seasonally anestrous ewes. Journal of Reproduction and Fertilitity, 120, 169–176.
Rosa, H. J. D.; Bryant, M. J. (2003). Seasonality of reproduction in sheep. Small Ruminant Research, 48, 155–171.
Roselli, C. E.; Stormshak, F.; Stellflug, J. N.; Resko, J. A. (2002). Relationship of serum testosterone concentrations to mate preferences in rams. Biology of Reproduction, 67, 263-268.
Roy, A. (1957). Egg yolk coagulating enzyme in the semen and Cowper’s gland of the goat. Nature, 179, 318–319.
Santiago-Moreno, J., Gómez-Brunet, A., González-Bulnes, A., Toledano-Díaz, A., Malpaux, B.; López-Sebastián, A. (2005). Differences in reproductive pattern between wild and domestic rams are not associated with inter-specific annual variations in plasma prolactin and melatonin concentrations. Domestic Animal Endocrinology, 28, 416–429.
Sarabia, L., Maurer, I., Bustos-Obregon, E. (2009). Melatonin prevents damage elicited by organophosphorous pesticide diazinon on mouse sperm DNA. Ecotoxicology and Environmental Safety, 72, 663–668.
Sarlós, P., Egerszegi, I., Balogh, O., Molnar, A.; Cseh, S.; Ratky, J. (2013). Seasonal changes of scrotal circumference, blood plasma testosterone concentration and semen characteristics in Racka rams. Small Ruminant Research, 111, 90–95.
Sawyer, D. E., Brown, D. B. (1995). The use on an in vitro sperm activation assay to detect chemically induced damage of human sperm nuclei. Reproductive Toxicology, 9, 351–357.
Shang, X. J., Li, K., Ye, Z. Q.; Chen, Y. G., Yo, X., Huang, Y. F. (2004). Analysis of lipid peroxidative levels in seminal plasma of infertile men by high-performance liquid chromatography. Archives of Andrology, 50, 411–416.
Sharpe, R. M., Mckinnell, C., Kivlin, C., Fisher, J. S. (2003). Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction, 125, 769-784.
Shiu, S. Y.; Li, L.; Siu, S. W.; Xi, S. C.; Fong, S. W.; Pang, S. F. (2000). Biological basis and possible physiological implications of melatonin receptor-mediated signaling in the rat epididymis. Biological Signals and Receptors, 9, 172–187.
Siegel, S. F., Finegold, D. N., Urban, M. D., Mcvie, R.; Lee, P. A. (1992). Premature pubarche: etiological heterogeneity. The Journal of Clinical Endocrinology and Metabolism, 74, 239-247.
Silva, C. M., Marcías-García, B., Miró-Morán, A., González-Fernández, L., Morillo-Rodrigues, A., Ortega-Ferrusola, C., Gallardo-Bolaños, J. M., Stilwell, G., Tapia, J. A.; Peña, F. J. (2011). Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. Journal of Pineal Research, 51, 172–179.
Souza, A. F., Leitão, M. C. G., Batista, A. M.; Porto, A. L. F., Lima Filho, J. L., Guerra, M. M. P. (2009). Proteínas do plasma seminal de caprinos relacionadas com o índice pluviométrico e a qualidade do sêmen. Ciência Rural, 39, 1166-1172.
Smith, J. T. (2012). The role of kisspeptina and gonadotropin inhibitory hormone in the seasonal regulation of reproduction in sheep. Domestic Animal Endocrinology, 43, 75-84.
Succu, S., Berlinguer, F., Pasciu, V., Satta, V., Leoni, G. G.; Naitana, S. (2011). Melatonin protects ram spermatozoa from cryopreservation injuries in a dose-dependent manner. Journal of Pineal Research, 50, 310–318.
Tamme, L. A.; Still, D. L.; Acromite, M. T. (2010). Hypoxia and flight performance of military instructor pilots in a flight simulator. Aviation, Space and Environmental Medicine, 81, 654–659.
Tan, D. X., Manchester, L. C., Liu, X., Rosales-Corral, S. A., Castroviejo, D. A., Reiter, R. J. (2013). Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin’s primary function and evaluation in eukaryotes. Journal of Pineal Research, 54, 127–138.
Todini, L.; Malfatti, A.; Terzano, G. M.; Borghese, A.; Pizzillo, M.; Debenedetti, A. (2007). Seasonality of plasma testosterone in males of four Mediterraneangoat breeds and in three different climatic conditions. Theriogenology, 67, 627–631.
Tosini, G., Fukuhara, C. (2002). The mammalian retina as a clock. Cell and Tissue Research, 309, 119-126.
Upreti, G. C., Hall, E. L., Koppens, D., Oliver, J. E., Vishwanath, R. (1999). Studies on the measurement of phospholipase A2 (PLA2) and PLA2 inhibitor activities in ram semen. Animal Reproduction Science, 56, 107-121.
Vargas, A., Bustos-Obregon, E., Hartley, R. (2011). Effects of hypoxia on epididymal sperm parameters and protective role of ibuprofen and melatonin. Biological Research, 44, 161–167.
Villemure, M., Lazure, C., Manjunath, P. (2003). Isolation and characterization of gelatin-binding proteins from goat seminal plasma. Reproductive Biology and Endocrinology, 1:39.
Webster, J. R., Suttie, J. M., Veenvliet, B. A., Manley, T. R., Littlejohn, R. P. (1991). Effect of melatonin implants in secretion of luteinizing hormone in intact and castrated rams. Journal of Reproduction and Fertilitity, 92, 21–31.
Yániz, J. L., Marco-Aguado, M. A., Mateos, J. A., Santolaria, P. (2010). Bacterial contamination of ram semen, antibiotic sensitivities, and effects on sperm quality during storage at 15 °C. Animal Reproduction Science, 122, 142–149.
Zamiri, M. J., Khodaei, H. R. (2005). Seasonal thyroidal activity and reproductive characteristics of Iranian fat-tailed rams. Animal Reproduction Science, 88, 245–255.
Zamiri, M. J., Khalili, B., Jafaroghli, M., Farshad, A. (2010). Seasonal variation in seminal parameters, testicular size, and plasma testosterone concentration in Iranian Moghani rams. Small Ruminant Research, 94, 132–136.
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