Résumé

La chèvre présente une reproduction saisonnière. Cette saisonnalité permet de coïncider la parturition avec la période adéquate de la nutrition et les conditions climatiques pour la survie de la progéniture. La présente revue analyse à travers les différents biotopes, les facteurs intervenants dans l'expression de cette saisonnalité de l'activité sexuelle chez cette espèce. Sous les différentes latitudes, la photopériode est le principal modulateur de cette saisonnalité chez la chèvre. D'autres facteurs environnementaux comme les changements saisonniers des cycles de la température ambiante semblent également induire un effet de synchronisation de cette saisonnalité. De plus, la disponibilité de la nourriture affecte de manière sensible la physiologie de la reproduction chez cette espèce. En effet, un état de bonne nutrition renforce le comportement sexuel chez la chèvre, alors que la sous-nutrition et en particulier un bilan énergétique négatif ont un impact négatif sur cette saisonnalité. D'autre part, l'interaction sociale chez cette espèce affecte également l'expression de la physiologie et le comportement sexuel pendant la saison de la reproduction. La chèvre présente une bonne adaptation à tous les biotopes, y compris les chauds, froids, humides et secs. Cette particularité semble dépendre du génotype et peut être cruciale pour une anticipation efficace des changements climatiques globaux.


Mots clés: Chèvre, reproduction saisonnière, photopériode, température ambiante, disponibilité alimentaire, facteurs sociaux, génotype.

INTRODUCTION

To ensure survival, animals must adapt to different abiotic seasonal changes. Such adaptation involves physiological processes, like as hibernation, molt of skin, fur and plumage, migration and reproduction in order to anticipate seasonal variations (Gwinner, 1981). Breeding activity is considered to be very seasonal, to ensure the survival of offspring by coinciding parturition with optimal seasonal nutritional and climate conditions. In temperate environments, the daylength (photoperiod) seems to be the main environmental factor driving seasonal reproduction in mammals. In non-temperate climates, other factors such as ambient temperature cycles, rainfall and food availability seem to be the most factors implicated in this process (Vázquez-Armijo et al., 2011). Goats are known to express seasonal variations in their sexual behavior. In high latitudes (> 30°, > 35° and > 40°), photoperiod and ambient temperature cycles are considered the major regulators of seasonal breeding in this species. In contrast, in low latitudes, seasonal breeding activity in goats seems to be regulated by rainfall and food availability (Vázquez-Armijo et al., 2011). However, other factors such as social and sexual interactions are also involved in the control of goat reproduction seasonality. Goat husbandry has a great economic impact in many parts of the world (Devendra and Coop, 1982) and can adapt to various climatic conditions (Delgadillo et al., 1997). Most experimental studies on breeding seasonality involve the effect of a single environmental factor. To our knowledge, there is no multifactorial analysis on the control of goat seasonality in temperate, desert or tropical regions. The present paper reviews the effect of abiotic and biotic factors on the seasonality of reproduction in this species by analyzing the impact of photoperiod, temperature and rainfall with subsequent food availability in a various zoogeographical areas where goats are raised (60°N to 40°S). The social and climate change effects on reproduction of goats are also discussed in this review.

MECHANISMS OF PHOTOPERIOD IN REGULATION OF SEASONAL BREEDING IN GOATS

When reproductive physiology is considered, most species can be classified as seasonal or non-seasonal breeders. In seasonal breeders, we can distinguish short days breeders and long days breeders. Goats, like sheep are considered seasonal breeders (Jainudeen et al., 2000) being short or long days breeders depending on their geographical location. In high latitudes, a great variability exists in the onset of sexual activity in goats, depending on geographic origin. For example, in France (40°N), the breeding season starts in September and finishes in March which corresponds to a short days breeder (Bodin et al., 2007). This pattern of seasonality is also observed in many other goat breeds such as the Spanish Payoya goat (Zarazaga et al., 2005), the Portuguese Serrana goat (Mascarenhas et al., 2006), the United kingdom goat (Ahmad et al., 1996), the North American goat (Mohammad et al., 1984; Amoah et al., 1996), the Italian goat (Luca et al., 2007), the Cyprus goat (Mavrogenis et al., 2006), the Greek goat (Karagiannidis et al., 2000), but also the Northern Moroccan indigenous goats (Chentouf et al., 2011), the Algerian Bedouine goat (Charallah et al., 2000), the Tunisian Maure goat (Lassoued and Rekik, 2005), the Jordan goat (Kridli et al., 2007), the Egyptian goat (Farrag et al., 2012) and the Iranian goat (Farshad et al., 2008). In subtropical regions, such as Mexico (26°N) (Delgadillo et al., 2004), and in the southern latitudes regions like Argentina (30ºS) (Rivera et al., 2003), Australia (Restall, 1992), southern Brazil (Balaro et al., 2016) and South Africa (Muller, 2005), the breeding season is also observed during the short days. At lower latitudes, in tropical regions, like Kenya (Ndeke et al., 2015), Indonesia (Sodiq et al., 2003), Brazil (Simplício et al., 1986) and in subtropical regions like Tanzania (Safari et al., 2012) and Nigeria (Trevor, 1991), goats do not seem to be seasonal breeders.

When examining the breeding seasons together with the environmental cues (including photoperiod) (Figure 1) and by month of the year worldwide (Figure 2), we see a relationship between environmental cues and zoogeographical distribution of goats. Results show that under high and moderate latitudes (Figure 1), the breeding season is closely related to the changes of photoperiod. Indeed, in northern hemisphere countries, the patterns are always a mirror image of those seen in the southern hemisphere (Figure 2). Reproductive activity is always observed during short days.

In tropical regions (Figures 1 and 2), goats tend to show sexual activity throughout the whole year. This is mainly due to the absence of annual changes in photoperiod (and probably ambient temperature). Under these latitudes, goats are not able to detect seasonal changes in the environment and therefore are not able to limit their reproductive activity to a specific season. In equatorial regions and nearby tropical zones there are seasonal cycles in the annual rainfall and subsequently in food availability (Vivien-Roels and Pévet, 1983). Analysis of data of figure 1 shows no breeding season in the equatorial geographical zone in Kenya and Brazil despite seasonal cycles of rainfall. This indicates that the absence of seasonality in equatorial regions is likely to be related to photoperiod length and probably ambient temperature too.

It is also interesting to note that although goats are known as seasonal breeders; there are some specific breeds that do not express seasonal breeding. These include different breeds over the world such the Drâa goats in Morocco (Boukhliq and Lahlou-Kassi, 1989), goats in China (Lui et al., 2015), in India (Harikrishna et al., 2013), in Pakistan (Ahmad et al., 2014) and in Soudan (Ismail et al., 2011) (Figures 1 and 2). The extended breeding season in such breeds does not seem to be related to the environment because other goat breeds seem to show reproductive cyclicity in the same latitudes (Figures 1 and 2). We think that such peculiarities could be explained by the goat genotypes and feeding level (Zarazaga et al., 2009).

Photoperiod was long considered as the main environmental cue driving the breeding seasonality in small ruminants. Several experiments have demonstrated the effect of adaptation to environmental lighting (Reiter, 1978, 1974; Hoffman, 1965; Lincoln, 1979 and 1992; Lincoln and Short, 1980; Lincoln and Richardson, 1998; Lincoln et al., 2001). Over the last few decades, photoperiodic treatments were used to control seasonal breeding in sheep, horses and goats (Chemineau et al., 2008). In goats, artificial light treatments (e.g., a regimen of one month of long days and one month of short days), were found to induce ovulation, estrous behavior and to achieve high fertility rates during the out-of-season period. This treatment can be potentiated by the so-called “male effect” (Chemineau et al., 2008). The control of the seasonal breeding in goats by artificial lighting indicates that under natural conditions, photoperiod may be the main modulator of breeding seasonality.

Photoperiod was also shown to act on reproduction through the pineal hormone, melatonin. The use of melatonin implants can modify the breeding season in goats. Melatonin treatment induces higher fecundity and maintains estrous and ovulatory activities beyond the normal breeding season and is able to induce reproductive activity during the non-breeding season (Chemineau et al., 1992; Zarazaga et al., 2009). Melatonin is secreted at night and acts on the hypothalamo-pituitary-gonadal axis by providing a time signal to the brain (Vivian-Roels and Pévet, 1983). Mammals perceive information about photoperiod through changes in the duration of the melatonin nocturnal peak (Bartness et al., 1993; Goldman, 2001). The secretion of melatonin includes reception of light by the retina. The photic signal is conveyed to the pineal gland through mutlisynaptic pathways including the retino-hypothalamic tract, the suprachiasmatic nuclei, the hypothalamic paraventricular nuclei, the intermediolateral cell column of the spinal cord and the superior cervical ganglia (Tournier et al., 2003; Larsen et al., 1998; Teclemariam-Mesbah et al., 1999). Norepinephrine released during night time from sympathetic innervation of the pineal gland induces synthesis of melatonin by pinealocytes (King and Steinlechner, 1985; Stehle et al., 2001). The duration of the nocturnal melatonin peak is proportional to the duration of the night (Illnerova et al., 1984; Pévet et al., 1991; Tast et al., 2001; El Allali et al., 2005).

During the long days, the peak of melatonin in goats is short, which inhibits sexual activity whilst during short days the melatonin peak is large, which stimulates reproductive function via the control of the pulsatile secretion of GnRH/LH (Chemineau et al., 2010). Recent data brought evidence that melatonin acts on GnRH/LH neurons through a new discovered population of neurons called the Kisspeptins and RFRP neurons (Revel et al., 2006; Clarke et al., 2009; Desroziers et al., 2010; Dardente et al.,2016). In goats, kisspeptin signaling plays an important role in the pulsatile secretion of GnRH and LH to control the breeding season in this species (Wakabayashi et al., 2010).

EFFECT OF AMBIENT TEMPERATURE

When ambient temperatures are high, reproductive activity in animals seems to be limited to a specific period of the year, to ensure the survival of the offspring (Nakao et al., 2008). Excessive high ambient temperatures may prevent reproductive activity (Ungerfeld and Bielli, 2000). In fact, heat stress was found to induce a decline in follicular responsiveness to LH in goats (Kanai et al., 1995), a decrease in plasma concentrations of estradiol and LH receptors, while the ovulation is delayed (Ozawa et al., 2005). However, even if high temperature affects negatively reproduction activity, goats, like camels in arid and semi-arid areas, are more adapted to reduce the effect of heat stress on their physiological processes (Louw, 1984). Unlike European breeds, goats raised in arid and semi-arid regions are relatively smaller in size and have a conformation that minimizes water expenditure (Silanikove, 2000) and their breeding season is longer than in temperate or subtropical regions. The long breeding season increases the chance of conception under these environments. The breeding season often starts when the ambient temperatures are low (Figure 1). This is important because ambient temperature affects hormonal pattern and folliculogenesis as stated above.

Most studies on the effect of ambient temperature focused on heat stress and reproduction, and like the photoperiod, ambient temperature exhibits seasonal changes that could be integrated by the nervous system. Indeed, it was suggested that the pineal indoles like 5-methoxytryptophol (5ML) were responsible for the possible effect of ambient temperature on reproduction (Vivien-Roels and Pévet, 1983). 5ML is secreted by the pineal gland and is capable of modifying sexual development and reproduction in several species, where this molecule exerts a remarkable effect on the gonads of mature and immature animals (Mullen et al., 1979). For example in chicks, it stimulates the development of the testes and ovaries, while in adults it shows anti-gonadal activity. 5ML has a circadian rhythm in both the pineal gland and serum which is in phase with that for melatonin, with high levels in the dark and low in the day (Mullen et al., 1979). The question of the effect of the seasonal variation in the light and the ambient temperature on reproduction through 5ML remains open for large animals like goats.

The seasonal message of the nocturnal peak of melatonin, which is able to inform the body about the season, is initially built from its daily and circadian rhythm. It’s been demonstrated for the first time in the camel, that the daily variations in ambient temperature are able to induce a plasmatic rhythm of melatonin secretion (El Allali et al., 2013). This is evidence that the ambient temperature is a real Zeitegeber (Timer). This means that daily and seasonal biological rhythms such as reproduction could be synchronized by daily and seasonal cycles of ambient temperature. In a recent study, it was established as in the camel, melatonin in Moroccan goats is also driven by ambient temperature cycles (Farsi and El Allali; unpublished data). Ambient temperature and photoperiod have a synchronized pattern during the seasons of the year (Figure 1). Our recent work revealed that melatonin is higher when ambient temperature is low (El Allali et al., 2013). Thus, it seems that photoperiod and ambient temperature are agonists in their action; with reproduction being activated when photoperiod is short and ambient temperature is low.

EFFECT OF FOOD AVAILABILITY AND RAINFALL

In goats, besides photoperiod and probably ambient temperature, other environmental cues, such as rainfall and food availability, are likely to be involved in the control of the breeding season (Mani et al., 1996). Food availability, which is important for the offspring survival, is considered as an ultimate factor controlling the breeding season (Lofts, 1975; Gwinner, 1981). Other environmental cues, such photoperiod and temperature, are just proximate factors allowing the prediction of the best period of food availability and better climate conditions. In order to understand how environment drives the breeding season in mammals, food availability should not be considered on the same grounds as photoperiod and ambient temperature. Feeding is able to drive circadian rhythms (Feillet et al., 2008) but there is no evidence that food availability can provide a direct signal to the brain to modulate the predictive homeostasis. Moreover, food seems to be directly involved in the reparative adaptation of reproductive physiology. It is well known that nutrition and body condition score are major factors affecting breeding season. Indeed, a body scoring below 40-60% of normal weight was found to cause a delay in follicular growth (Blanc et al., 2004), and to affect the onset of ovarian cyclicity (Walkden-Brown et al., 1994). Sustained undernutrition induces a delay in estrous behavior for a shorter period, compared to normally fed goats. Similarly, fasting causes large changes in concentrations of reproductive hormones and ovulation rate in goats (Al-Azraqi et al., 2007). In Payoya bucks, higher nutritional plane induces better sexual behavior (Zarazaga et al., 2009), indicating that feeding is an important factor for normal breeding season in goats.

In the ewe, the follicular growth passes through two major stages. Basal folliculogenesis, which affects follicles less than 2 mm for 6 months, is closely dependent on insulinemia and not to pituitary hormones (Monget, 1998). The energy status and dietary supplementation at the end of the luteal phase (just before estrus) significantly increases the ovulation rate. This practice, called “flushing”, leads to an increase in the ovulation rate by increasing the insulinaemia and without changing the plasma concentration of pituitary hormones (Monget 1998; Martin et al., 1994). At the end of pregnancy: an energetic deficiency accompanied by high energy requirements, especially at the end of gestation, can lead to an increased mobilization of fatty acids to produce energy. This mobilization leads to an accumulation of ketone bodies which creates a state of toxemia in the ewe and directly affects the viability of the female and her fetus. In arid and semi-arid regions (i.e. high solar radiation, high ambient temperatures, limited water availability and unpredictable food resources), the breeding season is usually longer than in temperate regions (Hamadeh et al., 1996, Amoah et al., 1996) and, therefore, kidding occurs when food and climate become more favorable for the offspring.

SOCIAL CUES

Besides above cited factors, other environmental stimuli including social interactions are also considered regulators of the breeding season in goats (Walkden-Brown et al., 1993). These social cues are mainly related to the presence of males. Interaction with males during the breeding season stimulates the secretion of GnRH pulses in females and can also stimulate ovulation (Scaramuzzi and Martin, 2008) (Figure 3). A similar effect of females on males was reported (Martin et al., 1994). In fact, exposure to estrus females can induce an increase of testosterone levels in males. Female-female interaction effect also exists as estrous females can induce ovulation in anestrous ones (Walkden-Brown et al., 1993; Restall et al., 1995). One of the characteristics of this social interaction in goats is that when the dominant does get in contact with new introduced males, they ovulate earlier than non-dominant does (Alvarez et al, 2003). Indeed, in addition to the behavioral changes, the interaction between male and female seems capable to induce some physiological changes in the goat, like in the sudoriferous glands in the skin, the site of production of the putative pheromones that stimulate the reproductive system (Martin et al., 1994), through olfactory bulbectomy that can trigger the onset of the breeding season (Martin et al., 1994). In natural conditions, goats are simultaneously exposed to several environmental factors including photoperiod, ambient temperature, food availability and social cues. The interaction between these factors allows the synchronization of the reproductive rhythm (Figure 3). Social cues, like other factors, induce pulsatile secretion of GnRH. However, this hormonal response is largely dependent on the genotype of the goat (Martin et al., 2004).

EFFECT OF GENOTYPE AND BIOTOPE CHANGES ON SEASONAL REPRODUCTION IN GOATS

For a better understanding of the seasonality of reproduction in goats, it is necessary to consider the interactions between all environmental cues but also the genotype of the animal. In small ruminants, the dominant response of the hypothalamic-pituitary system to an environmental factor is dependent on the genotype of the animal. For example, in Suffolk rams, seasonal breeding is linked to photoperiod; while in Merino rams it seems to follow changes in food availability. This variation may also concern goats in the different latitudes (Martin et al., 2004). When the photoperiod is a dominant inducer of the breeding season, the effect of other factors such as nutrition and social cues depend on the degree to which the genotype considers the response to photoperiod (Martin et al., 2004). This interaction between intrinsic factors (such as genotype) and extrinsic factors makes it possible to explain the responsiveness of goats to a dominant cue in their environment. On the other hand, Chemineau et al., (1992) have shown that seasonal activity in temperate Alpine goats was unchanged when females were experimentally exposed to a simulated tropical photoperiod (Figure 4), showing insensitivity to different stimuli compared to the usual biotope of native goats. In contrast, María et al. (2011) have shown that, under natural conditions, does of different origin and genotypes (Alpine goat, Nubian and Criollo × Nubian), present a seasonal reproductive pattern similar to that of subtropical does in Mexico (22° N, Figure 4). Another example illustrating such adaptation is seen in sheep. It is known that the reproductive cycle begins in the northern hemisphere when daylength decreases and starts in the southern hemisphere when daylength increases. However, the transfer of ewes from southern to northern hemisphere induces a resynchronization of reproduction to the new northern location, starting breeding in autumn (Lofts, 1975). It can be concluded that, under natural environmental conditions, several factors are involved in the synchronization of breeding seasonality in goats.

CONCLUSION

It appears that the photoperiod is the main modulator of the seasonality of reproduction in goats in the different latitudes. Other cues such as seasonal changes in ambient temperature cycles, food availability, social interactions and genotype are also thought to modulate seasonality of reproduction in this species. As compared to other domestic animals, goats show a good adaptive plasticity, depending upon to the genotype, which allows it to anticipate climate changes to adapt its physiology, specifically that of reproduction.

REFERENCES

Ahmad N., Javed K., Abdullah M., Hashmi A.S., Ali A. (2014). Estrus induction in beetal goats during low breeding season. J. Anim. Pla. Sci., 24: 1283-1287.

Ahmad N., Noakes D.E. (1996). Seasonal variations in the semen quality of young British goats. Br. Vet. J., 152: 225-236.

Al-Azraqi A.A. (2007).Effect of fasting on luteal function, leptin and steroids concentration during oestrous cycle of the goat in natural photo-status. Anim. Reprod. Sci., 98: 343-349.

Alvarez L., Martin G. B., Galindo F. Zarco L. A. (2003). Social dominatce of female goats affects their response to the male effect. Appl. Anim. Behav. Sci., 84: 119-126.

Amoah E.A., Gelaye S., Guthrie P., Rexroad J.R. (1996). Breeding season and aspects of reproduction of female goats. J. Anim. Sci.,74: 723-728.

Balaro M.F.A., Santos A.S., Mello S.G.V., Cavalcanti L.M.,.Gonçalves L.H.S,.Moura L.F.G.M, Souza Fabjan1 J.M.G., Fonseca J.F., Brandao F.Z. (2016). Reproductive seasonality in Saanen goats managed in south-east Brazil. Proceedings of the 30th Annual Meeting of the Brazilian Embryo Technology Society (SBTE); Foz do Iguaçu, PR, Brazil, August 25th to 27th, 2016, and 32nd Meeting of the European Embryo Transfer Association (AETE); Barcelona, Spain, September 9th and 10th(Abstracts).

Bartness T.J., Powers, J.B., Hastings M.H., Bittman E.L., Goldman B.D. (1993). The timed infusion paradigm for melatonin delivery: what has it taught us about the melatonin signal, its reception, and the photoperiodic control of seasonal responses. J. Pineal. Res.,15:161-190.

Blanc F., Bocquier F., Debus N., Agabriel J., D’hour P., Chilliard Y. (2004). La pérennité et la durabilité des élevages de ruminants dépendent des capacités adaptives des femelles. INRA Prod. Anim., 17: 287-302.

Bodin L., Dion S., Malpaux B., Bouvier F., Caillat H., Baril G., Leboeuf B., Manfredi E. (2007). Sexual seasonality of Alpine and Creole goats and maintained without reproduction. In: 58th Annual Meeting of the European Association for Animal Production, Dublin, Ireland, Session 25, Poster 21.

Boukhliq R., Lablou-Kassi A. (1989).Evaluation of the reproductive performance of Draa goats in Morocco.Proceedings of a conference held at bamenda, Cameroon 18-25 janury. African small ruminant research and development. 310-315.

Feillet C.A., Mendoza J., Pévet P., Challet E. (2008). Restricted feeding restores rhythmicity in the pineal gland of arrhythmic suprachiasmatic-lesioned rats. Eur. J. Neurosci., 28: 2451-2458.

Charallah S., Khammara F., Amirat Z., Lakhdari Y., (2000). Evaluation de l’activite sexuelle male et femelle: caracterisation zootechnique et nutritionnelle chez la chèvre Bédouine. In: Gruner, L., Chabert, Y. (Eds.), Proceeding 7e conference internationale sur les caprins. Tours, France, p. 460.

Chemineau P., Bodin L., Migaud M, Thiéry J.C., Malpaux B. (2010). Neuroendocrine and Genetic Control of Seasonal Reproduction in Sheep and Goats. Reprod. Dom. Anim., 45: 42-49.

Chemineau P., Guillaume D., Migaud M., Thiéry J.C., Pellicer-Rubio M.T., Malpaux B. (2008). Seasonality of Reproduction in Mammals: Intimate Regulatory Mechanisms and Practical Implications. Reprod. Dom. Anim., 43: 40-47.

Chemineau P., Malpaux B., Delgadillo J.A., Guérin Y., Ravault J.P., ThimonierJ., Pelletier J. (1992). Control of sheep and goat reproduction: Use of light and melatonin. Anim. Reprod. Sci., 30:157-184.

Chentouf M., Bister J.L., Boulanouar B. (2011). Reproduction characteristics of North Moroccan indigenous goats.Small. Rumin. Res., 98: 185-188.

Chemineau P., Daveau A., Maurice F. Delgadillo J.A. (1992). Seasonality of estrus and ovulation is not modified by subjecting female Alpine goats to a tropical photoperiod. Small. Rumin. Res., 8: 299-312.

Clarke I.J., Smith J.T., Caraty A., Goodman R.L., Lehman M.N. (2009). Kisspeptin and seasonality in sheep.Peptides 30: 154-163.

Dardente H., Lomet D., Vincent R., Caroline D. Beltramo M., Pellicer-Rubio M. T.(2016). Seasonal breeding in mammals: From basic science to applications and back. Theriogenology. 86: 324-332.

Delgadillo J.A., Malpaux B., Chemineau P., (1997). La reproduction des caprins dans les zones tropicales et subtropicales. INRA Prod. Anim., 10: 33-41.

Delgadillo J.A., Fitz-Gonzlez G., Duarte G., Véliz F.G., Carrillo E., Flores J.A., Vielma J., Hernndez H., Malpaux B., (2004). Management of photoperiod to control caprine reproduction in the subtropics. Reprod. Fert. Develop., 16: 471-478.

Devendra C., Coop I.E., (1982). Ecology and distribution. In: Coop, I.E. (Ed.), Sheep and Goat Production. World Animal Science C1. Elsevier Publishers. 1-14.

Desroziers E., Mikkelsen J., Simonneaux V., Keller M., Tillet Y., Caraty A., Franceschini I. (2010). Mapping of kisspeptinfibres in the brain of the pro-oestrous rat. J. Neuroendocrinol., Oct; 22: 1101-12.

El Allali K., Achaâban M. R., Bothorel B., Piro M, Bouâouda H., El Allouchi M, Ouassat M., Malan A., et Pévet P. (2013). Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am. J. Physiol. Regul. Integr. Comp. Physiol., 304: R1044-R1052.

El Allali K., Achaaban M.R., Vivien-Roels B., Bothorel B., Tligui N.S., Pévet P. (2005). Seasonal variations in the nycthemeral rhythm of plasma melatonin in the camel (Camelusdromedarius): Seasonal plasma melatonin in the camel. J. Pineal. Res., 39: 121-128.

Farrag F. H. H., Shalaby N. A., Metawi H. R., Mona A. O., Desoky A. L. I. (2012). characterization of zaraibi goat production systems in delta region of Egypt. J. Anim. Poultry. Prod., Mansoura Univ., 3: 47- 57.

Farshad A., Akhondzadeh S., Zamiri M. J., Sadeghi GH. (2008). The Estrous Cycle of the Markhoz Goat in Iran, Asian-Aust. J. Anim. Sci., 21: 1411-1415.

Goldman B. D. (2001) Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J. Biol. Rhythms., 16: 283–301.

Gwinner E, (1981). Annual rhythms: perspectives. Handbook of behavioral Neurobiology. in Aschoff J (ed): Biological rhythms. 4: 381-389.

Hamadeh S.K., Shomo F., Nordblom T., Goodchild A., Gintzburger G. (1996). Small ruminant production in Lebanon’s Beka’a Valley. Small. Rumin. Res., 21: 173-180.

Harikrishna C.h., Raghunandan T., GnanaPrakash M.(2013). Effect of Season on Kidding and Birth Weight in Osmana badi Goats, reared in an Organized Farm. Int. J. Livest. Res., 3 (2) May.

Hoffman R.A., Reiter R.J. (1965). Pineal gland: influence on gonads of male hamsters. Sci., 148:1609-1110.

Illnerova H., Hoffman K., Vanecek J. (1984). Adjustment of pineal melatonin and N-acetyltransferase rhythms to change from long to short photoperiod in the Djungarian hamster Phodopussungorus. Neuroendocrinology, 38: 226-231.

Ismail A .M., Yousif I.A., Fadlelmoula A .A.( 2011). Phenotypic Variations in Birth and Body Weights of the Sudanese Desert Goats. Liv. Res. Ru. Develop.,Volume 23, Article #34. Retrieved March 25, 2017, from http://www.lrrd.org/lrrd23/2/isma23034.htm.

Jainudeen M.R., Wahid H., Hafez E.S.E. (2000). Sheep and goats. In: Reproduction in farm animals, Seventh Edition (eds ESE Hafez and B Hafez), Wiley-Blackwell, Iowa, U.S.A. 172-181.

Karagiannidis A., Varsakeli S., Karatzas G. (2000). Characteristics and seasonal variations in the semen of alpine, saanen and damascus goat bucks born and raised in Greece. Theriogenology, 53: 1285-1293.

Kanai Y., Yagyu, N., Shimizu, T. (1995). Hypogonadism in heat stressed goats: poor responsiveness of the ovary to the pulsatile LH stimulation induced by hourly injections of a small dose of GnRH. J. Reprod. Dev., 41: 133-139.

Kridli R. T., Tabbaa M. J., Barakeh F. S. (2007). Seasonal Variation in Scrotal Circumference and Semen Characteristics of Black Bedouin and Black Bedouin-Damascus Crossbred Bucks. Asian-Aust. J. Anim. Sci., 20: 359-364, March.

King T.S., Steinlechner S. (1985). Pineal indolalkylamine synthesis and metabolism: kinetic considerations. Pineal. Res. Rev., 3: 69-113.

Lassoued N., Rekik M. (2005). Variations saisonnières de l’œstrus et de l’ovulation chez la chèvre locale Maure en Tunisie. Elev. Med. Vet., Pays trop. 58: 69-73.

Larsen P.J., Enquist L.W., Card J.P. (1998). Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing. Eur. J. Neurosci.,10:128-145.

Lincoln G.A. (1979). Photoperiodic control of seasonal breeding in the ram: Participation of the cranial pathetic nervous system. J Endocrinol., 82: 135-147.

Lincoln G. A., Short R.V. (1980). Seasonal breeding: nature’s contraceptive. Recent. Prog. Horm. Res., 36: 1-52.

Lincoln G. A. (1992). Administration of melatonin into the mediobasal hypothalamus as a continuous or intermittent signal affects the secretion of follicle stimulating hormone and prolactin in the ram. J. Pineal. Res., 122: 135-144.

Lincoln G. A et M. Richardson. (1998). Photoneuroendocrine control of seasonal cycles in body weight, pelage growth and reproduction: lessons from the HPD sheep model. Comp. Biochemphysiol Part C Pharmacol. Toxicol. Endocrinol., 119: 283-294.

Lincoln G. A., S. M. Rhind., S. Pompolo., I. J. Clarke (2001). Hypothalamic control of photoperiod-induced cycles in food intake, boody weight, and metabolic horomones in rams. AMJ. Am. J. Physiol. Regul. Integr. Comp. Physiol., 281: R76-90.

Lofts B. (1975). Animal Photoperiodism. In Arnold E (ed): “The institute of Biology’s Studies in Biology”.

Louw G. N. (1984).Water deprivation in herbivores under arid conditions. Pages 106–126 in F. M. C. Gilchrist and R. I. Mackie, editors. Herbivore nutrition in the subtropics and tropics. Science, Craighall, South Africa.

Luca T., Alessandro M., Giuseppina M.T., Antonio B., Michele P., Alessandro D. (2007). Seasonality of plasma testosterone in males of four Mediterranean goat breeds and in three different climatic conditions, L. Todini et al. / Theriogenology, 67: 627-631.

Lui G., lui S., Jiang X., Hu J.,Wu X. (2015). Black-bone goat: An investigation report on new genetic resource of farm animal. Afri. J. Agri. Res., 10: 1714-1718.

Mani A.U., McKelvey W.A.C., Watson E.D. (1996). Effect of under-nutrition on gonadotropin profiles in non-pregnant, cycling goats. Anim. Reprod. Sci., 43: 25-33.

Martin G.B., Rodger J., Blache D. (2004). Nutritional and environmental effects on reproduction in small ruminants.In: Reprod. Fertil. Develop., 16: 491-501.

Martin G. B.,, Walkden-Brown S.W., Boukhliq R., Tjondronegoro S.,Miller D.W., Fisher J. S., Hötzel M. J., Restall B. J., Adams N.R. (1994). Non-photoperiodic inputs into seasonal breeding in male ruminants. Perspectives in Comparative Endocrinology, 574-585.

María T.R.L., Martha O.D.G., Jorge U. M., Héctor V. Á., Héctor G. V . Eugenio V.A. M., Carlos F.A.F., Francisco J.E.M. (2011). Seasonal variation in ovulatory activity of nubian, alpine and nubian × criollo does under tropical photoperiod (22°N). Tropical and Subtropical Agroecosystems,14: 973-980.

Mascarenhas R., Fresno M., Milena A., Avdi M., Terqui M. ( 2006). Estacionalidad de la actividad sexual de las razas caprinas autoctonas del Sur de Europa. REDVET, 4: 1-7.

Mavrogenis A.P., Antoniades N.Y., Hooper R.W. (2006). The Damascus (Shami) goat of Cyprus. AGRI. 38: 57-65.

Mohammad W. A., Grossman M., Vatthauer J. L. (1984). Seasonal Breeding in United States Dairy Goats. J. Dairy Sci., 67: 8.

Monget P.h., Caraty A., Bruneau G., Martin G. B. (1998). Les interactions métabolisme-reproduction chez les animaux domestiques. Contracept. Fenil. Sec. 26 (6’ 7-8): 554-563.

Mullen P. E., Leone R. M., Hooper J., Ivor Smith, Silman R. E., Finnie M., Carter S., Linsell C. (1979). Pineal 5-Methoxy Tryptophol in Man. Psychoneuroendocrinology, 2: 117-126.

Muller C.J.C. (2005). Genetic parameter estimation and breeding plans for the South African dairy goat herd, PhD: Dissertation submitted to the Department of Animal Sciences, Faculty of Agricultural and Forestry Sciences, University of Stellenbosch, in partial fulfillment of the requirements for the degree.

Nakao N., Ono H., Yoshimura T. (2008). Thyroid hormones and seasonal reproductive neuroendocrine interactions.Reprod., 136: 1-8.

Ndeke A.N., Mutembei H.M., Tsuma V.T., Mutiga E.R. (2015). Reproductive Performance of the Galla and Toggenburg Goats and their Crosses in Mwingi Sub-county of Kenya. J. Agri. Sci. Food. Tech., 1: 78-83.

Ozawa M., Tabayashi D., Latief T. A., Shimizu T., Oshima I., Kanai Y. (2005).Alterations in follicular dynamics and steroidogenicabilities induced by heat stress during follicular recruitment in goats. Reproduction, 129: 621-630.

Pévet P., Vivien-Roels B., Masson-Pévet M. (1991). Annual changes in the daily pattern of melatonin synthesis and release. In: Role of Melatonin and Pineal Peptides in Neuroimmunomodulatin. Fraschini F, Reiter RJ, eds. Plenum press, New York. 147-158.

Reiter R.J. (1974). Circannual reproductive rhythms in mammals related to photoperiod and pineal function: A review. Chronobiologia, 1: 365-394.

Reiter R. J. (1978). Interaction of photoperiod, pineal and seasonal reproduction as exemplified by finding in the hamster. Prog. Reprod. Biol., 4: 169-190.

Restall B.J. (1992). Seasonal variation in reproductive activity in Australian goats. Anim. Reprod. Sci., 27: 305-318.

Restall B.J., Restall H.,Walkden-Brown S.W. (1995). The induction of ovulation in anovulatory goats by oestrous females. Anim. Reprod. Sci., 40: 299-303.

Revel F.G., Saboureau M., Masson-Pevet M., Pevet P., Mikkelsen J.D., Simonneaux V. (2006). KiSS-1: a likely candidate for the photoperiodic control of reproduction in seasonal breeders. Chronobiol. Int., 23: 277-287.

Rivera G.M., G.A. Alanis , M.A. Chaves , S.B. Ferrero, H.H. Morello. (2003). Seasonality of estrus and ovulation in Creole goats of Argentina. Small. Rumin. Res., 48: 109-117.

Safari J., Kifaro G.C., Mushi D.E., Mtenga L.A, Adnøy T., Eik L.O. (2012). Influence of flushing and season of kidding on reproductive characteristics of Small East African goats (does) and growth performance of their kids in a semi arid area of Tanzania. Afr. J. Agri. Res., 7: 4948-4955.

Scaramuzzi R.J., Martin G.B. (2008). The Importance of Interactions Among Nutrition, Seasonality and Socio-sexual. Factors in the Development of Hormone-free Methods for Controlling Fertility. Reprod. Dom. Anim., 43: 129-136.

Seo S.N., Mendelsohn R. (2006). Climate change adaptation in Africa: A microeconomic analysis of livestock choice. CEEPA Discussion Paper No. 19. Centre for Environmental Economics and Policy in Africa, University of Pretoria, South Africa.

Silanikove N. (2000). The physiological basis of adaptation in goats to harsh environments. Small. Rumin. Res., 35: 181-193.

Simplício A.A., Riera G.S., Nunes J.F., Foote W.C. (1986). Frequency and duration of oestrous cycle and period in genetically non-descript (SRD) type of goats in the tropical Northeast of Brazil. Pesq. Agropec. Bras., 21: 535-540.

Sodiq A., Adjisoedarmo S.,Tawfik E.S. (2003). Reproduction Rate of Kacang and Peranakan Etawah Goats under Village Production Systems in Indonesia. International Research On Food Security Natual Resource. Management And Rural Development, Gottingen.

Stehle JH, von Gall C, Schomerus C. (2001) Of rodents and ungulates and melatonin: creating a uniform code for darkness by different signaling mechanisms. J. Biol. Rhythms,16: 312-325.

Tast A., Halli O., Ahlstrom S., Andersson H., Love R.J., Peltoniemi O.A.T. (2001). Seasonal alterations in circadian melatonin rhythms of the European wild boar and domestic gilt. J. Pineal. Res., 30: 43-49.

Taylor C.R. (1969). Metabolism, respiratory changes and water balance of an antelope, the eland. Am. J. Physi., 217: 317-320.

Teclemariam-Mesbah R., Ter Horst G.J, Postema F. (1999). Anatomical demonstration of the supra chiasmatic nucleus pineal pathway. J. Comp. Neurol., 406: 171-182.

Trevor W.R. (1991). Small ruminant production and the small ruminant genetic resource in tropical Africa. Food and agriculture organization of the United Nations. Rome.

Tournier B.B., Menet J.S., Dardente H., Poirel V.J., Malan A., Masson-Pévet M., Pévet P., Vuillez P. (2003). Photoperiod differentially regulates clock genes expression in the supra chiasmatic nucleus of Syrian hamster. Neuroscience, 118: 317-322.

Ungerfeld U., Bielli A. (2000). Seasonal and Social Factors Affecting Reproduction. Animal Reproduction in Livestock. Animal reproduction in Livestock.Encyclopedia of Life Support Systems.

Vázquez-Armijo J.F, Rojo R., Salem A.Z.M., López D., Tinoco J.L., González A., Pescador N., Domínguez-Vara I.A. (2011). Trace elements in sheep and goats reproduction: A review. Trop. Sub. Agro., 14: 1-13.

Vivien-Roels B., Pévet P. (1983).The pineal Gland and the synchronization of reproductive cycles with variations of the environmental climatic conditions, with special reference to temperate. Pineal. Res. Rev., 1: 91-143.

Wakabayashi Y., Nakada T., Murata K., Ohkura S., Mogi K., Navarro V.M., Clifton D.K., Mori Y., Tsukamura H., Maeda K., Steiner R.A., Okamura H. (2010). Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J. Neuros., 30: 3124-3132.

Walkden-Brown S.W., Restall B.J., Henniawati (1993). The male effect in Australian cashmere goats 1.Ovarian and behavioural response of seasonally anovulatory does following the introduction of bucks. Anim. Reprod. Sci., 32: 41-53.

Walkden-Brown S.W., RestallB.J., Norton B.W., Scaramuzzi R.J., 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: 351-360.

Walkden-Brown S.W., Martin G.B., Restall B. J. (1999). Role of male-female interaction in regulating reproduction in sheep and goats. Journal of Reproduction & Fertility Supplement, 52: 243-257.

Zarazaga L.A., Gatica M.C., Celi I., Guzman J.L. ,Malpaux B. (2009). Effect of melatonin implants on sexual activity in Mediterranean goat females without separation from males. Theriogenology, 72: 910–918.

Zarazaga L.A.,GuzmánJ.L., Domínguez C., Pérez M.C., Prieto R. (2009). Effects of season and feeding level on reproductive activity and semen quality in Payoya buck goats. Theriogenology,71: 1316-1325.

Zarazaga L.A.,Guzmán J.L., Domínguez C., Pérez M.C., Prieto R. (2005). Effect of plane of nutrition on seasonality of reproduction in Spanish Payoya goats. Anim. Reprod. Sci., 87: 253-267.