Published 2017-09-27
Keywords
- Ungulates,
- Conduct,
- Physiology,
- Melatonin
How to Cite
Abstract
The physiological and behavioral changes in ungulates are an adaptive response to environmental changes. The endogenous biological clock allows each individual animal to produce these changes in response to environmental fluctuations. The daylight is the main factor that modulates this process, and its changes are reflected by variations in the melatonin concentrations. This review describes the translation of the light signal into changes in hormone concentration in ungulates. Then mechanism as photoperiod modifies physiological processes such as reproduction, and physical and behavioral aspects are presented. Finally this review discusses the relationship of genes in the development of biological clock. The understanding of the mechanisms that modulate the physiological and behavioral changes in ungulates facilitates handling of animals, especially those species where management is the key factor to productive and/or conservation captivity systems.
References
- Alila-Johansson, A., Eriksson, L., Soveri, T., & Laakso, M.-L. (2003). Serum cortisol levels in goats exhibit seasonal but not daily rhythmicity. Chronobiology international, 20(1), 65-79.
- Alila-Johansson, A., Eriksson, L., Soveri, T., & Laakso, M. L. (2001). Seasonal variation in endogenous serum melatonin profiles in goats: a difference between spring and fall? Journal of Biological Rhythms, 16(3), 254-263.
- Andersson, H., Johnston, J. D., Messager, S., Hazlerigg, D., & Lincoln, G. (2005). Photoperiod regulates clock gene rhythms in the ovine liver. General and comparative endocrinology, 142(3), 357-363.
- Asher, G. W. (2011). Reproductive cycles of deer. Animal Reproduction Science, 124(3), 170-175.
- Axelrod, J., Wurtman, R. J., & Snyder, S. H. (1965). Control of Hydroxyindole O-Methyltransferase Activity in the Rat Pineal Gland by Environmental Lighting. The Journal of biological chemistry, 240, 949-954.
- Barriga, C., Martín, M. I., Tabla, R., Ortega, E., & Rodríguez, A. B. (2001). Circadian rhythm of melatonin, corticosterone and phagocytosis: effect of stress. Journal of pineal research, 30(3), 180-187.
- Berger, A., Scheibe, K.-M., Eichhorn, K., Scheibe, A., & Streich, J. (1999). Diurnal and ultradian rhythms of behaviour in a mare group of Przewalski horse (Equus ferus przewalskii), measured through one year under semi-reserve conditions. Applied Animal Behaviour Science, 64(1), 1-17.
- Binkley, S., Hryshchyshyn, M., & Reilly, K. (1979). N-acetyltransferase activity responds to environmental lighting in the eye as well as in the pineal gland.
- Bittman, E. L., Dempsey, R. J., & Karsch, F. J. (1983). Pineal Melatonin Secretion Drives the Reproductive Response to Daylength in the Ewe*. Endocrinology, 113(6), 2276-2283.
- Bohák, Z., Szabo, F., Beckers, J. F., de Sousa, N. M., Kutasi, O., Nagy, K., et al. (2013). Monitoring the circadian rhythm of serum and salivary cortisol concentrations in the horse. Domestic animal endocrinology, 45(1), 38-42.
- Brown, B. W. (2000). A review on reproduction in South American camelids. Animal Reproduction Science, 58(3), 169-195.
- Carcangiu, V., Luridiana, S., Mura, M. C., Parmeggiani, A., Giannetto, C., Congiu, F., & Piccione, G. (2014). Melatonin circadian rhythm in three livestock species maintained in the same housed conditions. Biological rhythm research, 45(6), 909-914.
- Carcangiu, V., Giannetto, C., Luridiana, S., Fazio, F., Mura, M. C., Parmeggiani, A., & Piccione, G. (2015). Seasons induce changes in the daily rhythm of plasma melatonin in goats (Capra hircus). Animal Biology, 65(1), 13-20.
- Carrillo-Vico, A., Reiter, R. J., Lardone, P. J., Herrera, J. L., Fernández-Montesinos, R., Guerrero, J. M., et al. (2006). The modulatory role of melatonin on immune responsiveness. Current Opinion in Investigational Drugs, 7(5), 423.
- Charmandari, E., Tsigos, C., & Chrousos, G. (2005). Endocrinology of the stress response 1. Annu.Rev.Physiol., 67, 259-284.
- Chattoraj, A., Liu, T., Zhang, L. S., Huang, Z., & Borjigin, J. (2009). Melatonin formation in mammals: in vivo perspectives. Reviews in endocrine and metabolic disorders, 10(4), 237-243.
- Chemineau, P., Daveau, A., Cognié, Y., Aumont, G., & Chesneau, D. (2004). Seasonal ovulatory activity exists in tropical Creole female goats and Black Belly ewes subjected to a temperate photoperiod. BMC physiology, 4(1), 1.
- Chemineau, P., Malpaux, B., Delgadillo, J. A., Guerin, Y., Ravault, J. P., Thimonier, J., et al. (1992). Control of sheep and goat reproduction: use of light and melatonin. Animal Reproduction Science, 30(1), 157-184.
- Correa, L. M., Urviola, A., & Jl, J. R. (2015). Efecto de melatonina exógena en guanacos (Lama guanicoe) bajo un fotoperiodo de días largos. Revista Investigaciones Altoandinas-Journal of High Andean Research, 17(3).
- Crowell-Davis, S. L., Houpt, K. A., & Carnevale, J. (1985). Feeding and drinking behavior of mares and foals with free access to pasture and water. Journal of animal science, 60(4), 883-889.
- Dahl, G. E., & Thompson, I. M. (2011). Effects of Photoperiod on Domestic Animals. Environmental Physiology of Livestock, 229.
- Dardente, H., Fustin, J.-M., & Hazlerigg, D. G. (2009). Transcriptional feedback loops in the ovine circadian clock. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 153(4), 391-398.
- Darlington, T. K., Wager-Smith, K., Ceriani, M. F., Staknis, D., Gekakis, N., Steeves, T. D., et al. (1998). Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science (New York, N.Y.), 280(5369), 1599-1603.
- de Reviers, M.-M., Ravault, J.-P., Tillet, Y., & Pelletier, J. (1989). Melatonin binding sites in the sheep pars tuberalis. Neuroscience letters, 100(1-3), 89-93.
- Debono, M., Ghobadi, C., Rostami-Hodjegan, A., Huatan, H., Campbell, M. J., Newell-Price, J., et al. (2009). Modified-release hydrocortisone to provide circadian cortisol profiles. The Journal of Clinical Endocrinology & Metabolism, 94(5), 1548-1554.
- DeVries, A. C., Glasper, E. R., & Detillion, C. E. (2003). Social modulation of stress responses. Physiology & Behavior, 79(3), 399-407.
- Dubocovich, M. L. (2007). Melatonin receptors: role on sleep and circadian rhythm regulation. Sleep medicine, 8, 34-42.
- Dubocovich, M. L., Rivera-Bermudez, M. A., Gerdin, M. J., & Masana, M. I. (2003). Molecular pharmacology, regulation and function of mammalian melatonin receptors. Frontiers in bioscience : a journal and virtual library, 8, d1093-1108.
- Dvorkin, A. M., & Cardinali, P. D. (2005). Bases Fisiológicas de la Práctica Médica. 13ª. Editorial Médica Panamericana.México.
- El Allali, K., Achaaban, M. R., Vivien-Roels, B., Bothorel, B., Tligui, N. S., & Pevet, P. (2005). Seasonal variations in the nycthemeral rhythm of plasma melatonin in the camel (Camelus dromedarius). Journal of pineal research, 39(2), 121-128.
- Foster, D. L., & Jackson, L. M. (1994). Puberty in the sheep. The physiology of reproduction, 2, 411-451.
- Gilman, A. G. (1995). G proteins and regulation of adenylyl cyclase. Bioscience reports, 15(2), 65-97.
- Goldman, B. D. (2001). Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. Journal of Biological Rhythms, 16(4), 283-301.
- Golombek, D. (2001). Cronobiología humana: en busca del tiempo perdido. Ciencias(062).
- Gordon, J. G., & McAllister, I. K. (1970). The circadian rhythm of rumination. The Journal of Agricultural Science, 74(02), 291-297.
- Grubaugh, W., Sharp, D. C., Berglund, L. A., McDowell, K. J., Kilmer, D. M., Peck, L. S., et al. (1982). Effects of pinealectomy in Pony mares. Journal of reproduction and fertility.Supplement, 32, 293-295.
- Guesdon, V., Malpaux, B., Delagrange, P., Spedding, M., Cornilleau, F., Chesneau, D., et al. (2013). Rapid effects of melatonin on hormonal and behavioral stressful responses in ewes. Psychoneuroendocrinology, 38(8), 1426-1434.
- Hernández-Rosas, F., & García, J. S. (2010). Ritmos circadianos, genes reloj y cáncer. Archivos de Medicina.
- Ibraheem, M., Galbraith, H., Scaife, J., & Ewen, S. (1994). Growth of secondary hair follicles of the Cashmere goat in vitro and their response to prolactin and melatonin. Journal of anatomy, 185 ( Pt 1)(Pt 1), 135-142.
- Irvine, C. H. G., & Alexander, S. L. (1994). Factors affecting the circadian rhythm in plasma cortisol concentrations in the horse. Domestic animal endocrinology, 11(2), 227-238.
- Janis, C. (1984). Tragulids as living fossils Living fossils (pp. 87-94): Springer.
- Jasnow, A. M., Huhman, K. L., Bartness, T. J., & Demas, G. E. (2000). Short-day increases in aggression are inversely related to circulating testosterone concentrations in male Siberian hamsters (Phodopus sungorus). Hormones and behavior, 38(2), 102-110.
- Kennaway, D. J., & Gilmore, T. A. (1984). Effects of melatonin implants in ewe lambs. Journal of reproduction and fertility, 70(1), 39-45.
- Kohsaka, A., & Bass, J. (2007). A sense of time: how molecular clocks organize metabolism. Trends in Endocrinology & Metabolism, 18(1), 4-11.
- Krieger, D. T., Allen, W., Rizzo, F., & Krieger, H. P. (1971). Characterization of the normal temporal pattern of plasma corticosteroid levels. The Journal of Clinical Endocrinology & Metabolism, 32(2), 266-284.
- Levine, S. (1985). A definition of stress? Animal stress (pp. 51-69): Springer.
- Lincoln, G., Messager, S., Andersson, H., & Hazlerigg, D. (2002). Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proceedings of the National Academy of Sciences of the United States of America, 99(21), 13890-13895.
- Lincoln, G. A. (1992). Photoperiod-pineal-hypothalamic relay in sheep. Animal Reproduction Science, 28(1), 203-217.
- Lucas, R. J., Freedman, M. S., Munoz, M., Garcia-Fernandez, J. M., & Foster, R. G. (1999). Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science (New York, N.Y.), 284(5413), 505-507.
- López Pérez, L. M., Zarco Quintero, L., & Boeta Acosta, A. M. (2010). Inducción de la actividad ovárica en yeguas criollas con un programa de fotoperiodo artificial en la latitud 19° 9'N. Veterinaria México, 41(2), 89-100.
- Maier, R. A. (2001). Comportamiento animal: Un enfoque evolutivo y ecológico.
- Malpaux, B., Migaud, M., Tricoire, H., & Chemineau, P. (2001). Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. Journal of Biological Rhythms, 16(4), 336-347.
- Malpaux, B., Thiéry, J.-C., & Chemineau, P. (1999). Melatonin and the seasonal control of reproduction. Reproduction Nutrition Development, 39(3), 355-366.
- Malpaux, B., Viguie, C., Skinner, D. C., Thiery, J. C., Pelletier, J., & Chemineau, P. (1996). Seasonal breeding in sheep: Mechanism of action of melatonin. Animal Reproduction Science, 42(1), 109-117.
- Manca, M. E., Manunta, M. L., Spezzigu, A., Torres-Rovira, L., Gonzalez-Bulnes, A., Pasciu, V., ... & Naitana, S. (2014). Melatonin deprival modifies follicular and corpus luteal growth dynamics in a sheep model. Reproduction, 147(6), 885-895.
- Masana, M. I., & Dubocovich, M. L. (2001). Melatonin receptor signaling: finding the path through the dark. Science's STKE : signal transduction knowledge environment, 2001(107), pe39.
- Mazzucchelli, C., Pannacci, M., Nonno, R., Lucini, V., Fraschini, F., & Stankov, B. M. (1996). The melatonin receptor in the human brain: cloning experiments and distribution studies. Molecular Brain Research, 39(1), 117-126.
- McMillen, I. C., Nowak, R., Walker, D. W., & Young, I. R. (1990). Maternal pinealectomy alters the daily pattern of fetal breathing in sheep. The American Journal of Physiology, 258(1 Pt 2), R284-287.
- Morgan, P. J., Webster, C. A., Mercer, J. G., Ross, A. W., Hazlerigg, D. G., MacLean, A., et al. (1996). The ovine pars tuberalis secretes a factor(s) that regulates gene expression in both lactotropic and nonlactotropic pituitary cells. Endocrinology, 137(9), 4018-4026.
- Nesse, R. M. (2000). Is depression an adaptation? Archives of General Psychiatry, 57(1), 14-20.
- Nowak, R., Porter, R. H., Levy, F., Orgeur, P., & Schaal, B. (2000). Role of mother-young interactions in the survival of offspring in domestic mammals. Reviews of reproduction, 5(3), 153-163.
- O'Callaghan, D., Karsch, F. J., Boland, M. P., & Roche, J. F. (1991). What photoperiodic signal is provided by a continuous-release melatonin implant? Biology of reproduction, 45(6), 927-933.
- O'Connor, T. M., O'Halloran, D. J., & Shanahan, F. (2000). The stress response and the hypothalamic-pituitary-adrenal axis: from molecule to melancholia. QJM : monthly journal of the Association of Physicians, 93(6), 323-333.
- Panchal, M. T., Gujarati, M. L., & Kavani, F. S. (1995). Some of the reproductive traits in Kathi mares in Gujarat State. Indian J.Anim.Reprod, 16(1).
- Prendergast, B. J., Zucker, I., & Nelson, R. J. (2009). Seasonal rhythms of mammalian behavioral neuroendocrinology. Hormones, brain, and behavior, 1, 507-538.
- Reiter, R. J., Tan, D.-X., & Maldonado, M. D. (2005). Melatonin as an antioxidant: physiology versus pharmacology. Journal of pineal research, 39(2), 215-216.
- Reiter, R. J., Tan, D.-x., Terron, M. P., Flores, L. J., & Czarnocki, Z. (2007). Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. ACTA BIOCHIMICA POLONICA-ENGLISH EDITION-, 54(1), 1.
- Reppert, S. M. (1997). Melatonin receptors: molecular biology of a new family of G protein-coupled receptors. Journal of Biological Rhythms, 12(6), 528-531.
- Reppert, S. M., & Weaver, D. R. (2001). Molecular analysis of mammalian circadian rhythms. Annual Review of Physiology, 63(1), 647-676.
- Reppert, S. M., & Weaver, D. R. (2002). Coordination of circadian timing in mammals. Nature, 418(6901), 935-941.
- Riveros, J. L., Correa, L. M., & Schuler, G. (2017). Daylight effect on melatonin secretion in adult female guanacos (Lama guanicoe). Reproduction in Domestic Animals.
- Roche, J. F., Karsch, F. J., Foster, D. L., Takagi, S., & Dziuk, P. J. (1970). Effect of pinealectomy on estrus, ovulation and luteinizing hormone in ewes. Biology of reproduction, 2(2), 251-254.
- Romero, J. A., Zatz, M., Kebabian, J. W., & Axelrod, J. (1975). Circadian cycles in binding of 3H-alprenolol to ß-adrenergic receptor sites in rat pineal.
- Ryder, M. L. (1960). A study of the coat of the Mouflon Ovis musimon with special reference to seasonal change. Paper presented at the Proceedings of the Zoological Society of London.
- 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(4), 416-429.
- Santiago-Moreno, J., López-Sebastián, A., Del Campo, A., González-Bulnes, A., Picazo, R., & Gómez-Brunet, A. (2004). Effect of constant-release melatonin implants and prolonged exposure to a long day photoperiod on prolactin secretion and hair growth in mouflon (< i> Ovis gmelini musimon). Domestic animal endocrinology, 26(4), 303-314.
- Setchell, B. P. (1992). Domestication and reproduction. Animal Reproduction Science, 28(1), 195-202.
- Silver, M. (1990). Prenatal maturation, the timing of birth and how it may be regulated in domestic animals. Experimental physiology, 75(3), 285-307.
- Simonneaux, V., & Ribelayga, C. (2003). Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacological reviews, 55(2), 325-395.
- Snyder, D. L., Cowan, R. L., Hagen, D. R., & Schanbacher, B. D. (1983). Effect of pinealectomy on seasonal changes in antler growth and concentrations of testosterone and prolactin in white-tailed deer. Biology of reproduction, 29(1), 63-71.
- Stanisiewski, E. P., Ames, N. K., Chapin, L. T., Blaze, C. A., & Tucker, H. A. (1988). Effect of pinealectomy on prolactin, testosterone and luteinizing hormone concentration in plasma of bull calves exposed to 8 or 16 hours of light per day. Journal of animal science, 66(2), 464-469.
- Stott, G. H. (1981). What is animal stress and how is it measured? Journal of animal science, 52(1), 150-153.
- Thun, R., Eggenberger, E., Zerobin, K., LÜScher, T., & Vetter, W. (1981). Twenty-four-hour secretory pattern of cortisol in the bull: evidence of episodic secretion and circadian rhythm. Endocrinology, 109(6), 2208-2212.
- Uno, H., & Kaji, K. (2000). Seasonal movements of female sika deer in eastern Hokkaido, Japan. Mammal Study, 25(1), 49-57.
- Walton, J. C., Weil, Z. M., & Nelson, R. J. (2011). Influence of photoperiod on hormones, behavior, and immune function. Frontiers in neuroendocrinology, 32(3), 303-319.
- Weems, P. W., Goodman, R. L., & Lehman, M. N. (2015). Neural mechanisms controlling seasonal reproduction: principles derived from the sheep model and its comparison with hamsters. Frontiers in neuroendocrinology, 37, 43-51.
- Woodfill, C. J., Wayne, N. L., Moenter, S. M., & Karsch, F. J. (1994). Photoperiodic synchronization of a circannual reproductive rhythm in sheep: identification of season-specific time cues. Biology of reproduction, 50(4), 965-976.
- Yu, H.-S., & Reiter, R. J. (1992). Melatonin: biosynthesis, physiological effects, and clinical applications: CRC Press.
- Zarazaga, L. A., Chemineau, P., Malpaux, B., & Forcada, F. (2000). La melatonina: síntesis, ritmo de secreción y catabolismo. Ovis(71), 25-35.
- Zemdegs, I. Z., McMillen, I. C., Walker, W., Thorburn, G. D., & Nowak, R. (1988). Diurnal Rhythms in Plasma Melatonin Concentrations in the Fetal Sheep and Pregnant Ewe during Late Gestation*. Endocrinology, 123(1), 284-289.
- Zerbe, P., Clauss, M., Codron, D., Bingaman Lackey, L., Rensch, E., Streich, J. W., et al. (2012). Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation, photoperiodic control, and life history. Biological Reviews, 87(4), 965-990.
- Zhdanova, I. V., Cantor, M. L., Leclair, O. U., Kartashov, A. I., & Wurtman, R. J. (1998). Behavioral effects of melatonin treatment in non-human primates. Sleep research online : SRO, 1(3), 114-118.