Seasonality

Seasonality of reproduction has long been suggested for the female camelidae. This is based mainly on the seasonal distribution of birth, both in the wild and in domesticated animals, or on the status of ovarian activity in slaughtered females.^{(39, 77, 108, 170, 186, 207, 212-215, 269)} However, very few studies have demonstrated the endocrinological and physiological bases of seasonality in the female camel. Seasonal pattern of reproduction in the female camelid is probably largely due to nutritional conditions.

Many investigators consider the dromedary camel a seasonally polyestrous animal with a relatively short breeding season.^{(33, 94, 95, 182, 184, 186, 212 213, 215, 274)} Outside of the breeding season, mating activity ceases and the ovaries are inactive or show a limited number of small follicles.^{(86, 176, 184, 213)} The anestrous period, which is characterized by small and hard ovaries, lasts for about six months.⁽¹⁸²⁾

In a survey of births in different zoos throughout Europe and South Africa, the dromedary camel displayed the same birth-season pattern as the Bactrian camel with 72.3% of all births falling in the months February to May (late winter and spring).⁽²⁰⁷⁾ Three dromedary x Bactrian hybrids were also bom in March and April. In a South African zoo (Pretoria), 78% of all births were recorded from August to November which is exactly six months apart from the birth season in the northern hemisphere zoos. Mating occurs in the northern hemisphere from January to March.⁽²¹¹⁾
 

There are still conflicting reports as to the beginning and length of the seasonal activity in the dromedary (Table 1). In some countries, breeding activity seems to be limited to a few months of the year, whereas in others, breeding is continuous without a real distinction between an anestrous period and a breeding season. As a general rule, breeding activity is increased during the period of rain, low temperature, and better grazing conditions. In Morocco, parturitions are observed during most of the year but they increase significantly during the period of February to May.⁽²¹¹⁾ In Saudi Arabia, it was shown that conception can occur at any time of the year but there is a clear increase of pregnancy loss during spring and early summer.⁽¹⁰²⁾ In Egypt, high ovarian activity is noted between December and May.⁽²¹²⁾ However, this was established on the basis of the presence of a corpus luteum or a pregnancy in slaughtered animals. In our opinion, photoperiod is not the primordial factor in the seasonality of the dromedary as seen in other species. According to our observations in the United Arab Emirates, well-fed and well-watered dromedary females show ovarian activity throughout the year and the determinant factors of the observed seasonality in conception dates are due to a decrease in libido in the male and an increase in early embryonic death during the summer months. When males were kept in a controlled environment (temperature not exceeding 30°C and humidity less than 40%), breeding and conception were possible even during the extreme heat and humidity of August in Abu Dhabi. However, all the bred females experienced an early embryonic death and resorption within the first 45 days of pregnancy (Anouassi and Tibary, personal observations). The effect of heat and humidity on embryo survival is also well illustrated by embryo transfer results. In a study in the United Arab Emirates, no pregnancies were obtained after transfer of embryos during July and August.⁽¹⁵⁹⁾

It is still not clear from these studies on monthly birth distribution whether the seasonal trend of reproduction in the dromedary is due to the failure of the female to cycle or due to the failure of mating on the part of the male. The answer to this question can only be reached by a clinical and endocrinological study of ovarian activity. There is very limited information on the endocrinological aspects of seasonality in the dromedary focusing only on the study of estrogen and LH levels.^{(42, 44, 94, 95)} Plasma levels of estradiol-17ß vary considerably from one month to the other but do not demonstrate any association of the level of this hormone with the breeding activity.^{(42, 44)} In Tunisia, regular estradiol peaks (every 15 days) of an average 7 days duration were found during the period from December to April which corresponds to the normal breeding season of dromedaries in this area.⁽¹⁴²⁾ These estradiol peaks probably correspond to regular follicular waves in cycling females.!94) None of the females showed complete anestrus during the summer months.⁽¹⁴²⁾ In Morocco, weekly rectal palpation showed that 2 out of 5 females had follicular activity throughout the year (Anouassi and Ennassiri, unpublished).

Pituitary activity in the female dromedary is well correlated to ovarian activity and tends to be lower in fall and high in winter (breeding season).⁽¹⁴²⁾ Luteinizing hormone (LH) levels in female dromedaries are higher during the breeding season than during the non-breeding season.^{(42, 44, 142, 157)} During the breeding season the pituitary is more sensitive to, and releases more LH after, GnRH challenge.^{(40, 41)}

The breeding season of the Bactrian camel begins in China in mid December for a few females but the majority do not show estrus until January.^{(69, 72, 73)} Breeding activity in this species lasts until mid April. However, this conclusion about the end of the breeding season was based on lack of breeding activity which could be due to male seasonality and not to ovarian inactivity. Seasonality of reproduction in the Bactrian camel is also confirmed by the distribution of births.⁽²⁰⁷⁾ In this species, 95.8% of all parturitions take place between February and May.⁽²⁰⁷⁾ The same distribution of parturitions is observed in wild herds. Some authors have associated seasonality in this species to the variation in photoperiod.^(69, 260)

Based on the monthly distribution of births, breeding activity in the New World camelidae is reported to be seasonal.^{(207, 210, 256, 257)} However, in the llama and alpaca, this seasonality is only apparent not because it is due to ovarian inactivity but due instead to a management decision by breeders to insure births during the most appropriate time of the year in terms of nutrition and climatic conditions compatible with survival of young (November to April).^{(107, 109, 186, 205, 206, 235)} Alpacas and llamas show follicular activity throughout the year with monthly incidence of ovulation and conception rates ranging from 60 to 90% and 67 to 100% respectively.^{(116, 117)} Absence of seasonality in the female alpaca is also confirmed by laparoscopic observation which shows no significant effect of the season on the number of large follicles present on the ovary.⁽⁵⁹⁾ However, in a recent study, sexual behavior of the female alpaca was found to be affected by both season and elapsed time since parturition.⁽¹⁹⁶⁾ Female alpacas in this study were less receptive in spring vs. fall and when the time from parturition until joining was increased. Seasonality seems to be more marked in the wild New-World camelidae (guanaco and vicuna).^{(207, 208, 210, 255-257)}

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