Seasonality in the Male

The question of seasonality of reproduction in the camelids has been addressed by many authors but has not been fully investigated given the wide variability of environment under which the animals are studied. Male camelid seasonality seems to be a widely accepted principle based on a few behavioral and endocrinological studies as well as on the basis of reproductive patterns in the wild.^{(14, 66, 68, 109)} Given the wide geographical distribution of the dromedary, the breeding season is very variable but coincides in general with the period of low temperature, low humidity, and increased rainfall (Table 1 ).^{(17,18, 43, 61, 111)} Seasonality in the male is evidenced by changes in sexual behavior, morphology and function of the genital and associated organs, and endocrinological profile.^{(1, 13, 42, 61)}
 

It is suggested that seasonality is more pronounced in the Bactrian camel, lasting throughout the winter months and into early spring. According to Chen and Yuen,⁽²⁷⁾ dominant males start their activity earlier than young or subordinate males. Individual variations exist and breeding activity can last from 50 to 100 days depending on the male.

Background of seasonal reproduction in the wild

All camelids, with the exception of the llama which tends to breed continuously throughout the year, show a seasonal breeding activity illustrated by the concentration of all parturition in a relatively narrow window of months. Parturition data collected from different zoos throughout the world shows that the Bactrian camel, the dromedary, the guanaco, and the vicuña have well-defined breeding seasons.⁽⁸⁰⁾ Seasonality in camelids is certainly more pronounced in the wild than under modem management systems. At our facility, attempts to breed dromedaries during the hot summer months have resulted in a very high embryo mortality. Behavioral, histological and endocrinological studies corroborate the seasonal pattern of reproductive activity in some camelids.

Behavioral evidence of seasonality

Seasonal breeding was first recognized and described on the basis of the peculiar sexual behavior displayed by the dromedary camel.⁽⁵⁷⁾ As early as 1927, Leese⁽⁵⁶⁾ noticed that this sexual behavior appeared only during a few months (described as the rutting season) which corresponds to the cool season. The length of this breeding season depends both on climatic and nutritional parameters. In India, the breeding season varies from late September to March which corresponds to the monsoon season and early summer. In Saharan and sub-Saharan regions the breeding season is somewhat longer and runs from October until May.^{(28, 81)} In the Middle East, the breeding season goes from late October until late April depending on the country (Table 1). All the declared rutting seasons share at least two major characteristics: decreased temperature and increased quality of pasture. Another factor that could be of importance in the Gulf areas and the Asian subcontinent is the relative humidity. Onset and duration of the rutting season is also affected by type of management and the individual male. Males that are loose in the herd tend to come to season earlier and remain in rut for a longer period than confined males.^(48-49)

The Bactrian camel exhibits behavioral changes during the breeding season similar to those described for the dromedary which include aggressiveness, marking behavior, gurgling, frothing, and teeth grinding. However, exteriorization of the soft palate has not been described in this species. Secretions of the poll gland are increased as is the frequency of rolling.^{(26, 27)}

In the male alpaca, sexual behavior is increased during the breeding season, especially in males that are kept separate from females.⁽³⁷⁾

Anatomical and Endocrinological evidence of seasonality

Testicular and accessory sex gland activity.

Anatomical features sustaining the presence of seasonal reproduction in the male dromedary are well illustrated by the increase in size and activity of the testis and accessory glands during the coolest months of the year (rutting season) (cf. Male Anatomy).^{(1, 22, 23, 72, 76- 83-85, 108)} Significant seasonal variations in weight of the ampullae, prostate, and bulbo-urethral glands were also reported in Egyptian dromedaries, with maximum values observed during spring. The same authors reported a peak of fructose and citric acid contents of the accessory glands during the same period.⁽²⁾ However, the most obvious anatomical change in the dromedary during the rutting season is the increased secretory activity of the poll glands giving the characteristic smell of the rutting male (cf. Male anatomy).^{(55, 64, 77, 97, 100, 103)} Poll-gland weight increases from 40-100 g in the non-breeding season to 200-240 g in the rutting season.⁽⁶¹⁾

Histological studies of the testes also show an increased spermatogenic and secretory activity in the dromedary.^{(102, 104)} Leydig cell number as well as the number of spermatozoa in the epididymis are increased during the breeding season.^{(101, 104, 107, 108)} In a few individuals, degenerating germ cells can be observed in the lumen of the seminiferous tubules during the summer months, particularly in the aged camels.^{(84, 85)}

The head and body of the epididymis show seasonal morphological changes in Indian dromedaries. These are especially illustrated by the change in the height of the epithelial lining of the head and body of the epididymis. During the peak of the hot season (June and July) the epithelium becomes distorted and its height ranges from 30 to 50 µm. However, during the months April and May and August to November, the epithelium height is increased (50-80 µm). The epithelial height in the tail region ranges from 30 to 80 µm and remains unchanged throughout the year.⁽⁸⁶⁾ The number, size, and activity of Leydig cells decrease during the months of August to November. The volume ratio between interstitial tissue and seminiferous tubules increases during the period of December to March to 60%. 70% and 40% in the camels of 4-8, 9-15, and 16-20 years of age.⁽⁸⁴⁾ This ratio decreases to 30%, 36%, and 35% in the three respective age groups with increasing temperatures between April and July.⁽⁸⁴⁾ Ultrastructural analysis of the testes of the dromedary reveals remarkable differences between the mating and non-mating seasons in both the types of Leydig cells present and the volume occupied by the interstitial tissue. Maximal activity of Leydig cells is seen during the rutting season and it is suggested that this activity correlates with that of seminiferous epithelium and accessory sex glands.⁽¹⁰²⁾ In contrast, no differences were encountered between the seasons in either the appearance and abundance of the different types of spermiogenic cells, including mature spermatozoa, or in the diameter of the seminiferous tubules. These data indicate that in the dromedary the relatively low level of testosterone found during the non-mating season is sufficient to maintain regular functioning of the seminiferous epithelium and normal spermatogenesis. This implies that the relatively high level of testosterone found during the mating season is not correlated with the support of normal spermatogenesis but with other capacities relevant to sexual drive and behavior.⁽⁴²⁾ Some authors have suggested that the Leydig cells developing during the mating season originate from "new" undifferentiated cells and not from "old" differentiated Leydig cells which were active in testosterone synthesis during the previous season. In the dromedary', however, the last stage of Leydig cell development during the mating period is characterized by the formation of densely packed clusters of myelin figures containing lipochrome pigment.⁽⁴²⁾ Moreover, three types of secretory units of different activities have been observed throughout the year in the bulbourethral glands of the camel, and the most active units are particularly abundant during the rutting season.⁽⁹⁾ This suggests that camel Leydig cells maintain some degree of activity throughout the year, being maximal during the rutting season, and that this activity parallels that of the spermatogenetic epithelium and accessory sex glands.⁽¹⁰²⁾

Based on histochemical observations of the testis and studies on the accessory glands, some authors refer to the dromedary as a non-typical seasonal breeder.^{(8, 71)} This is largely due to the fact that there is no period of the year where the testis is devoid of spermatogenesis.⁽²³⁾ The non-breeding season in the camel is characterized by reduced spermatogenesis but never complete aspermatogenesis.⁽¹⁾ Furthermore, there are no seasonal fluctuations of the frequency of the stages of the cycle of seminiferous epithelium.^{(71, 72)}

Similar seasonal changes in testicular size were reported for the male vicuña. In the southern hemisphere, testicular size (longitudinal and transverse testes diameters) was greater in February than in August.^{(105, 106)} Testicular histology showed that the seminiferous tubules had greater diameters in February (163.5 ± 29.6 µm) than in August (137.9 ± 25.2 µm); Leydig cell nuclei diameters were also greater (5.9 ± 0.97 µm vs. 4.2 ± 0.03 µm). February is an active spermatogenetic phase and August a regression phase.⁽¹⁰⁵⁾ The differences of testicle size, seminiferous tubule diameter, and Leydig cell nuclei diameter observed between late February and August are in accordance with seasonal variations that have already been reported.⁽¹⁰⁶⁾ In spite of the fact that spermatogenetic activity appeared to be lower in August, all germ-cell types were observed in the histology. Although a quantitative evaluation of spermatogenesis is not yet complete it can be said at this stage that there was no complete aspermatogenesis in the non-breeding season. These results, involving an increase in testicular size that can be attributed mainly to increases in the diameter of the seminiferous tubules and enlarged Leydig cells, appear similar to those found in the one-humped camel during the rutting season.⁽¹⁰⁵⁾

Endocrinological evidence of seasonality

Testosterone

The major endocrinological change in the male camel during the rutting season is the increased secretion of androgen (especially testosterone). In Morocco, testosterone levels increase from 2 ng/ml in October to 24 ng/ml in January' and return to 4 ng in May.⁽⁶¹⁾ In the Negev and Judian desert, androgen levels in the dromedary are increased up to 10 fold during the rutting season.⁽¹¹¹⁾ High plasma testosterone levels in rut are about 30 ng/ml compared to 2 ng/ml during the remainder of the year.⁽¹¹¹⁾ Also, in Nigeria, Gombe and Oduor-Okelo⁽⁴³⁾ reported a monthly variation of testosterone level in the dromedary with a negative correlation with the temperature-humidity ratio. In Somalia, Bono et al.⁽¹⁷⁾ observed similar trends in that androgen secretion by the testes is increased as pasture condition improves during the rainy season. During the same period, males begin to show the typical rutting behavior and increased interest in females. The mean testosterone concentrations in the non-rutting animals were similar to those observed in prepubertal males (adults: 0.81 ± 0.78 ng/ml; prepubertal: 0.99 ± 0.17 ng/ml) but were doubled for the mature studs during the breeding season (1.96 ± 0.18 ng/ml). Results from different geographical locations indicate that there could be a difference in endocrinological response to the breeding season amongst breeds of dromedaries.⁽³¹⁾

The differential androgen synthesis between the seasons in the dromedary is not only quantitative but also qualitative. According to Bedrak et al,⁽¹³⁾ androgen synthesis is through both the 4-ene and 5-ene pathways during the rutting season, whereas during the non-mating season the synthesis occurs mainly, and at a lower rate, through the 5-ene pathway.^{(42, 79)} Testes excised during the non-mating season were found to have a relatively high activity of the 3ß-hydroxysteroid dehydrogenase systems of pregnenolone, 17α-hydroxypregnenolone, and dehydro epiandrosterone, but the 4-ene-17-hydroxylase and 4-ene-17,20-lyase systems were apparently less active than the 5-ene-17α-hydroxyiase and 5-ene-17,20-lyase systems. This situation is reversed during the breeding season.⁽¹³⁾

Higher testosterone in the breeding season may be due to increased synthesis and release of testosterone either by an increased sensitivity of Leydig cells to LH, or an enhanced secretion of LH from the pituitary gland, or both.^{(3, 6)} However, Frielander et al.⁽⁴²⁾ did not find significant positive correlation between the configuration of the smooth endoplasmic reticulum or its abundance in Leydig cells and levels of testosterone.

In the male vicuña, individual testosterone values tend to be higher in summer but some high values are also noted in August.⁽¹⁰⁵⁾ Seasonal changes in plasma testosterone concentrations have also been reported in alpaca males; samples taken in March have the highest monthly mean value and in June the lowest.^(60,105) The higher plasma testosterone levels in vicuña in summer are probably responsible for the behavioral changes observed in males at this period of the year. High levels of testosterone are consistently found in dominant males and young males that are trying to constitute a harem. Leaders invariably have higher hormonal plasma concentrations.⁽¹⁰⁵⁾

Thyroid activity

Concentration of thyroid hormones are high during the non-breeding season in the dromedary.⁽¹¹²⁾ Thyroid metabolism in the one-humped camel is higher in the heat of the summer if water is available. The levels of these hormones are not affected by age.⁽³⁾ The seasonal variation of thyroid hormones can also be explained by influence of food availability. This would explain the higher concentrations observed in the dromedary in the summer.⁽¹¹²⁾

Unlike the dromedary, the llama in North America does not appear to be a seasonal breeder, although it does have a distinct breeding season in South America. It has been suggested that the seasonal breeding patterns in South America are related to food availability.⁽⁴¹⁾ Studies on thyroid-gland activity in the llama show that basal T3 and T4 concentrations are similar to those measured in the male dromedary during the non-rutting season, but higher than concentrations reported for the male dromedary during the rutting season.^{(4, 32, 88)} However, a thorough investigation of seasonal variation of thyroid hormone in the llama is not yet available.

Pituitary activity and seasonality

The most likely explanation for the increased secretion of androgens during the breeding season in the dromedary is a change in pituitary function.⁽⁶⁾ To test this hypothesis, Fat-Halla & Ismail⁽³⁵⁾ studied the changes in weight and gonadotropin content in the pituitary as well as variation of plasma concentrations of LH and FSH. These authors found significant changes in FSH but not in circulating and hypophysal LH. The highest concentrations were found during the season when the temperature was at its lowest and day length at its shortest. Marie⁽⁶¹⁾ in Morocco, and Bono et al.⁽¹⁷⁾ in Somalia, found that LH plasma levels and pulsatility showed fluctuations throughout the year. The highest frequency and amplitude was seen in males during the cooler months (December-January.⁽⁶¹⁾ In another study, Bono et al,⁽¹⁸⁾ showed that the dry and rainy seasons influence the pituitary response to GnRH stimulation. During the rainy season, both male and female dromedaries showed a greater sensitivity to GnRH stimulation with more significant LH pituitary release.^(15-18) In both the male and female, pituitary refractoriness to GnRH stimulation became evident at the end of March, after the hot, arid months. Responsiveness to GnRH stimulation then increases during the reproductive season.⁽¹⁸⁾

Pituitary' and circulating FSH levels are significantly affected by season in the male dromedary.^{(12, 35)} FSH concentration is at its highest during winter and tends to drop reaching a minimum in summer before increasing again in autumn. No active correlation was found between FSH levels and daylight and the atmospheric temperature.⁽³⁵⁾

Cortisol

The correlation between blood corticoid levels in both sexes and climatic parameters seems to be more interesting. Adrenal function is stimulated both in extreme drought and heavy rainfall conditions.⁽¹⁸⁾ The influence of meteorological parameters on adrenal function may be involved in the control of hypothalamo-hypophyseal axis sensitivity.⁽¹⁸⁾ The mean cortisol concentration is is 13.2 ± 4.04 ng/ml. 3.2 ± 1.1 ng/ml, and 2.7 ± 1.0 ng/ml in the rutting adult, the non-rutting adult and prepubertal animals, respectively. Non-rutting animals show a diurnal rhythmicity.⁽³¹⁾ Thus a clear biphasic pattern is shown as opposed to a non-modal rhythm in non-rutting animals. The reason for this difference between non-rutting and rutting males is unknown at this stage. The testosterone pattern in the rutting animals is an inverse relationship to that of cortisol pattern in the same animals.⁽³¹⁾

Cortisol level in the dromedary camel is affected by mating. The basal cortisol concentration increases significantly after mating. Maximal rise is observed in Arabi followed by Bikaneri and Kutchi breeds. This increase has been explained by the effect of physical exhaustion due to excitation and mating stress which triggers the ACTH corticoid mechanism.⁽⁵⁾

Prolactin

Serum prolactin levels are high during the non-breeding season and decrease significantly with transition into the rutting season.^{(12, 44)} On the basis of this observation, it was proposed that hyperprolactinemia is a causative factor of reduced fertility and libido in the male dromedary during the non-breeding season, probably due to its inhibitory action on the synthesis and secretion of FSH and LH.⁽¹²⁾

Mechanisms regulating the onset of the breeding season

It is obvious from the above-mentioned studies that the dromedary camel can be characterized as a seasonal breeder at least with respect to its behavior. The mechanisms of onset of this seasonality are far from clear. However, most authors agree that cooler temperatures and food availability are the most important factors. The exact pathway by which nutritional and climatic changes affect reproduction in this species are not yet completely understood. Bedrak et al.⁽¹³⁾ suggested that the low reproductive activity of the male camel during the non-mating season is due to the high activity of the pineal gland provoked by the long summer days. We do not think it is likely that the photoperiod plays a big role in seasonality of reproduction in the camel - first, because the daylight hours at the latitude where the dromedary lives do not vary significantly and second, because the female does not seem to be as affected by seasonality as the male. It should be kept in mind, however, that the dromedary is capable of fertilization throughout the year^{(11, 22, 23, 83-85)} and therefore cannot be considered as a true seasonal breeder. We have obtained pregnancies in the hottest months (July and August); however, pregnancy loss is high and survival of the young is low.

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