16 Applied Andrology in Camelids Ahmed Tibary,1* Lisa K. Pearson1 and Abelhaq Anouassi2 The reproductive system of the male camelid presents several anatomical and physiological peculiarities compared with other domestic species. Understanding these peculiarities is a prerequisite for thorough breeding soundness evaluation, male infertility investigation and research on sperm biotechnologies of camelids. The family Camelidae includes six species, two Old World Camelids (OWC) and four New World Camelids (NWC) (aka South American Camelids, SAC). The OWC are Camelus dromedarius (the dromedary or single humped camel) and C. bactrianus (the Bactrian or double-humped camel), which are more adapted to the deserts of central Asia, the Arabian Peninsula and Africa than to other regions. The NWC are represented by two domesticated species, the llama (Lama glama) and the alpaca (Vicugna pacos), and two wild species, the guanaco (L. guanacoe) and the vicuña (V. vicugna). Each of the domesticated species of camelid presents a variety of ‘breeds’ or ‘types’ that presents specific production characteristics (pack animal versus the production of fibre, meat or dairy products, etc). Despite great differences in their phenotypic appearance, these species share many genetic and biological characteristics. However, because of the differences in their evolution, they have developed slightly different reproductive patterns. All species of domesticated camelids are considered to be important production animals in their respective native geographic areas. Alpacas and llamas in North American and European countries, and racing camels in some countries of the Middle East, benefit from a high standard of individual veterinary medical care owing to their sentimental or economic value. This chapter reviews the major aspects of the reproductive anatomy, physiology and common abnormalities of the male camelid. Breeding soundness examination is emphasized, with special reference to semen characteristics and factors that may affect its quality. The chapter is largely inspired by previous complete reviews by the authors (Tibary and Vaughan, 2006; Tibary et al., 2007; Tibary, 2008), to which the reader is referred for more complete references. The male reproductive organs have been well described for the llama, alpaca (Collazos, 1972; Delhon and Lawzewitsch, 1987, 1994; Tibary and Anouassi, 1997a; Fowler, 1998), guanaco and vicuña (Delhon et al., 1983; Urquieta and Rojas, 1990; Urquieta et al., 1994), as well as the dromedary (El-Wishy, 1988; Tibary and Anouassi, 1997a) and Bactrian camel (Tibary and Anouassi, 1997a). The mechanism and chronology of testicular descent remains unstudied in the Camelidae. In most males, the testes are present in the scrotum at birth, but they are usually soft and difficult to palpate. According to some authors, testicular descent is not complete until the second or third year of life in the dromedary and Bactrian camel. The scrotum is non-pendulous and situated high in the perineal region at the level of the ischial arch. The testicles are relatively small compared with those of other domestic livestock and are directed caudo-dorsally (Tibary and Vaughan, 2006; Tibary et al., 2007). Season does not seem to affect the size of the testes and scrotum in llamas and alpacas. In the vicuña, testicular size is greater in the summer than in the winter (Urquieta et al., 1994). There is great seasonal variation in testicular size in the dromedary and Bactrian camel. Testicular size is an important parameter in the evaluation of the breeding potential of males and can be used to predict daily sperm production. South American camelid testicles are ovoid and exhibit age-related size variation (Table 16.1). In adult llamas, the length, width and depth are respectively 5–7, 2.5–3.5 and 3–4 cm (Fowler, 1998). In the alpaca, the length and width of the testes are 4–5 and 2.5–3, cm respectively. In the vicuña, longitudinal and transverse testes diameters are, respectively, 3.3 and 1.69 cm in summer and 2.64 and 1.50 cm in winter (Urquieta and Rojas, 1990; Urquieta et al., 1994). The average individual testicular weight recorded in 3.5-year-old llamas (average body weight of 133 kg) is 24 g (Johnson, 1989). In the dromedary, reported testicular dimensions vary greatly according to different studies. This variation is probably due to the effect of age, sexual activity and even the ‘breed’ or strain of camels studied. In India, the long axis and diameter of the dromedary testes range respectively from 6 to 13 cm and 3 to 6 cm. Smaller values were reported for dromedaries in Egypt. The mean testicular length and width are respectively 9.3 ± 0.7 and 4.5 ± 0.4 cm in the rainy season and 9.5 ± 0.6 and 4.5 ± 0.5 cm in the dry season in Nigeria (Djang et al., 1988). The mean scrotal circumference reported for 197 dromedaries was 32.4 ± 2.4 cm and this was positively correlated with age. As a general rule, the average testicular length, width and depth are 9.1, 5.1 and 4.3 cm, and the average weight is 92 g for male dromedaries 3 years of age and older. In contrast to domestic NWC, camels exhibit a large seasonal variation in testicular size (Tibary and Anouassi, 1997a,c; Tibary et al., 2007). Reference ranges for testicular length, depth and breadth have recently been determined for Egyptian dromedaries of various age groups (Table 16.2) (Derar et al., 2012). Testicular size during the breeding season (usually the coolest or rainy months of the year) is 150 to 200% of that recorded outside the breeding season (during the hottest or driest months of the year) (Tibary and Anouassi, 1997a,c). In a study in India, the effect of season on the weight of the testicle was more pronounced in dromedaries between 9 and 14 years of age than in dromedaries younger than 9 or older than 14 years. The maximum weight of the testicle was observed during the period December to March (36–225 g) compared with the periods of April to July (32–181 g) and August to November (32–191 g). Season also has a marked effect on the consistency of the testis. During the breeding season, dromedary testicles are usually turgid but they become soft during the period of sexual rest. There is a need for further characterization of testicular descent and testicular growth in various breeds of camel. The histomorphology of the camelid testis is similar to that of other domestic livestock (Flores, 1970; Delhon and Lawzewitsch, 1987). The diameter of the seminiferous tubules varies from 174 to 240 μm (Tibary and Anouassi, 1997a). In the camel, the interstitial tissue occupies a larger area than the seminiferous tubules, particularly during the winter months, and seems to be the major factor in the seasonal variation of testicular size and weight. The increased amount of interstitial tissue observed during the breeding season is due to an increase in the number and volume of Leydig cells (Tibary and Anouassi, 1997b). The outer diameter of the seminiferous tubules in adult dromedaries varies according to the study and has been found to be in the range of 113 to 250μm. This variability could reflect an effect of the type of dromedary studied and/or the effect of age and season. The diameter of the seminiferous tubules is greatest during the breeding season (Tibary and Anouassi, 1997a). Early studies in the dromedary indicated a complete arrest of spermatogenic activity during the summer season. However, later studies showed the presence of spermatogenesis throughout the year (Tibary et al., 2007). Blood is supplied to the testicle primarily via the testicular artery. Along its trajectory, the testicular artery gives off several branches that supply blood successively to the testicular cord envelopes, the epididymis and the testicular parenchyma. The most distinct features of the artery during its trajectory are its enlargement as it approaches the testis and the distribution of its branches. The epididymal branch arises from the upper part of the vascular cone (the pampiniform plexus) and runs along the body of the epididymis, which it supplies before dividing into several branches at the level of the cauda epididymis, which anastomose with the deferential artery (artery of ductus deferens). The head of the epididymis is supplied by branches of the testicular artery given off at the level of the pampiniform plexus. The epididymis is composed of three distinct parts: the caput (head), corpus (body) and cauda (tail), as illustrated by Plates 46 and 47, which show a dromedary testicle and epididymis. The epididymis faces laterally along the dorsal border of the testis, with the head curving around the cranial pole of the testis. It is adherent to the cranial surface (caput) and both poles of the respective testis, and allows the corpus epididymis to form a sinus with the testis situated externally. In llamas, all three parts of the epididymis can be palpated, although in most instances only the small tail of the epididymis is easily palpable dorsal to the testis. In the dromedary, the cauda epididymis is round and well protruded – about 3–4 cm above the respective extremity of the testis. The total weight of the epididymis is approximately 10–40 g, and the weight ratio between the testis and the epididymis varies from 3:1 to 6:1. (Tibary and Anouassi, 1997a; Tibary et al., 2007). Histological and histochemical studies on llamas defined six segments of the epididymis (Delhon and Lawzewitsch, 1994). These regional differences represent different secretory functions that may play a role in the process of sperm maturation (Delhon and Lawzewitsch, 1994). On the basis of histological appearance, the dromedary epididymis is divided, into three segments: initial, middle and terminal. The middle segment is further divided into proximal, intermediate and distal parts. In the llama, the ductus deferens is 1 mm in diameter at the junction of the epididymis. It widens to 2 mm in the abdominal cavity towards the pelvic urethra (ampulla). The length of the ductus deferens is about 40 cm (Smith et al., 1994). In the dromedary, the ductus deferens enters the abdominal cavity via the medial angle of the inguinal canal then turns caudally in the genital fold, where it becomes straight and thick, forming the ampulla; it then passes deep into the prostate and opens directly into the colliculus seminalis via an ostium ejaculatorium (ejaculatory orifice) (Tibary and Anouassi, 1997a). The prepuce is located in the inguinal region. It is flattened from side to side and triangular in shape when viewed laterally. The prepuce adheres to the glans penis until 2 or 3 years of age, making exteriorization of the penis impossible in young males. In the absence of sexual stimulation, the small preputial orifice (ostium praeputiale) is directed caudally. The prepuce has a well-developed muscular apparatus, consisting of the cranial, the lateral and the caudal preputial muscles. These muscles allow movement of the preputial orifice cranially during erection and mating behaviour (Tibary and Anouassi, 1997c; Fowler, 1998). In the dromedary, the preputial skin is usually darker in colour than that in the rest of the body. It is covered with short fine hair and presents two nipples on either side of the base of the prepuce, near its caudal border. In males that are used intensively for breeding, a callus may develop at the lower part of the cranial curvature. The average length of the base, cranial and caudal borders is 28.0, 17.5 and 19.7 cm, respectively (Tibary and Anouassi, 1997a). The camelid penis is fibroelastic. In the absence of erection, the penis is retracted into its sheath via a pre-scrotal sigmoid flexure. The length of the penis ranges from 35 to 45 cm in llamas and alpacas, and from 59 to 68 cm in camels. The penis is cylindrical, gradually decreasing in diameter from its root at the ischial arch (1.2–2 cm in the llama; 2.2 cm in the dromedary) to the neck of the glans penis (collum glandis, preputial reflection), which is 0.8–1 cm in diameter in the llama and 0.4–1 cm in the dromedary) (Tibary and Anouassi, 1997a; Fowler, 1998). The glans penis is long (9–12 cm) and the distal tip consists of a cartilaginous process that has a slight clockwise curvature (Plate 48). The end of the urethra is located at the base of the cartilaginous process, not at the tip. The curved nature of the cartilaginous process of the camelid penis allows both penetration of the cervical rings, through combined rotational and thrusting movements, and the intrauterine deposition of semen. The retractor penis muscles (Musculus retractor penis) continue on the ventral aspect of the penis and are attached to the ventral convexity of the sigmoid flexure of the penis. There is a dorsal urethral diverticulum at the level of the pelvic symphysis that prevents passage of a catheter into the bladder (Tibary and Anouassi, 1997a; Fowler, 1998). The most notable feature in the anatomy of the internal genitalia of camelids is the absence of seminal vesicles (Tibary and Anouassi, 1997a). The prostate is usually described as a small H-shaped gland firmly attached to the dorsolateral aspect of the pelvic urethra near the trigone of the bladder. Its ventral aspect is slightly concave. Numerous prostatic ducts direct the secretion of this gland directly into the colliculus seminalis. The length, width and height of the prostate are respectively 3, 3 and 2 cm in the llama and 3, 2 and 2 cm in the alpaca. The two bulbourethral glands are spherical to ovoid and located on the dorsolateral aspect of the pelvic urethra, above and just cranial to the ischial arch. The bulbourethral gland diameter is 1.5 to 2 cm in the llama and 0.8 to 1.5 cm in the alpaca (Tibary and Vaughan, 2006). In the dromedary, the size and weight of all glands vary significantly and tend to reach a maximum at 10.5 to 15 years of age. During the breeding season, the average weights of the ampullae, prostate and bulbourethral glands are respectively 3.0, 12.0 and 3.6 g for animals between 4.5 and 6 years of age, and 4.2, 16.1 and 4.9 g for males aged 10.5 to 15 years. Size and weight of the accessory sex glands show a large seasonal variation. Maximum gland weight is recorded during the breeding season (winter and spring) and the minimum values are recorded during summer (Tibary and Anouassi, 1997a,b). One of the most noticeable anatomical characteristics related to reproduction in camels is the presence of modified sweat glands called poll glands (Taha et al., 1994). In the adult, they are oval and slightly elevated skin areas situated about 5 cm below the apex of the head, on the back of the poll, on each side of midline (Plate 49). The poll glands are identified as two dark spots, especially during the rutting season. This colour is due to oxidation of their secretions, which increase in amount during the rutting season. Activity of the poll glands is highly seasonal and closely follows testicular activity (Tibary and Anouassi, 1997b). Studies on puberty in the male camelid are scarce. Reported age at puberty is variable and may reflect genetic, nutritional and climatic changes, as well as the effect of season of birth. Male llamas and alpacas can display mounting behaviour at a young age (<1 year) (Sumar, 1985). However, complete erection and intromission is only possible when the penis is completely freed from its preputial attachments. The process of preputial detachment usually begins at the age of 12–13 months and coincides with an increase in plasma testosterone concentration (Bravo and Johnson, 1994). Plasma testosterone concentrations in 11-month-old alpaca males are similar to those found in adult males (Losno and Coyotupa, 1979). In llamas, plasma testosterone is <90 pg/ml from birth until 20 months old, and then increases to more than 1000 pg/ml. Preputial adhesions are lost in up to 10% of males by 1 year of age, in 70% of males by 2 years and in all males by 3 years of age, which corresponds to the recommended age for breeding (Sumar, 1996; Tibary and Vaughan, 2006). The variation in age at which penile preputial attachments are lost may be partially explained by plane of nutrition as there is a correlation between body size and mean testicular length, although the wide variation in testicular size at any one age or body size suggests that other factors, probably genetic, are also important (Galloway, 2000). Appearance of a lumen in the seminiferous tubules and the presence of spermatozoa were reported respectively at 12 months and 15–18 months of age in the alpaca (Montalvo et al., 1979). Other authors have reported that sperm production starts as early as 10–12 months of age in a few male alpacas and llamas, and is usually present by the age 1.5–2 years (Smith et al., 1994). Testicular growth in these species is slow and maximum size is not reached until 3 years of age (Bravo and Johnson, 1994). The male llama is not mature until 2.5–3 years of age but pregnancies have resulted from younger males (Johnson, 1989). Alpacas reach sexual maturity at 5 years of age, which corresponds to a body weight of 62.5 kg. The testicles at this age should be at least 4–5 cm in length and 2.5–3 cm in width (Sumar, 1996). In the wild, guanaco and vicuña males may reach puberty at an early age, but they live in a bachelor group until they reach maturity between 4 and 6 years of age. At this point, they start seeking a harem and become territorial. In a study of two animals, the testes of a 16-month-old vicuña male were aspermatogenic, whereas those of 2-year-old male were producing spermatozoa (Koford, 1957). The age at puberty in the dromedary, is poorly defined. Display of sexual behaviour has been reported as early as 2 years of age, but field observations by the authors suggest that sperm production and fertilizing ability are not achieved until 3–4 years of age for this camel (Rahim, 1997). Indian dromedaries seem to be slower in reaching puberty than their Arabian or African counterparts (Khan and Kohli, 1972; Sharma, 1981; Tibary and Anouassi, 1997b; Al-Qarawi et al., 2001; Tibary et al., 2005, 2007). In the traditional management of dromedary herds, males are not used for breeding until 5–6 years of age (Abdel Raouf et al., 1975; Azouz et al., 1992). This allows maximum fertility as both sperm production and interstitial tissue (Leydig cell) activity reach a plateau at 6 years old, which corresponds to the age of sexual maturity according to most authors. Normal sexual activity continues until 20 years old, when some males begin to show signs of senile changes in their sexual behaviour or sperm production. In the authors’ experience, breeding males have been successfully used up to 25–28 years of age (Tibary and Anouassi, 1997b). In the Bactrian camel, puberty is believed to occur around 4 years of age, though some males may enter breeding activity as early as 3 years old (Chen et al., 1980). Sexual maturity is reached at an age similar to that observed in the dromedary (5–6 years) and then declines after 15 years of age, although some males continue to breed until they are 20 years old (Chen et al., 1980). The seasonality of reproductive activity in male camels is widely accepted based on several behavioural and endocrinological studies, as well as on the basis of reproductive patterns in the wild (Novoa, 1970; Mukasa-Mugerwa, 1981). Given the wide geographical distribution of the dromedary, the breeding season is highly variable but, in general, it coincides with the period of lower temperature, lower humidity and increased rainfall (Table 16.3) (Gombe and Oduor-Okelo, 1977; Marie, 1987; Tibary et al., 2007). Seasonality in the male is evidenced by changes in sexual behaviour, morphology and function of the genital and associated organs, and endocrinological profiles (Bedrak et al., 1983; Frieländer et al., 1984; Marie, 1987; Azouz et al., 1992; Deen et al., 2005; Zia ur et al., 2007; Deen, 2008; Riaz et al., 2011). Table 16.3. Reported breeding season in camels (Camelus spp.) by country.
1Washington State University, Pullman, Washington, USA;
2Veterinary Research Centre, Abu Dhabi, United Arab Emirates
Introduction
Anatomy of the Reproductive Tract
Scrotum and testicles
Testicular size
Testicular histology
Epididymis
Ductus deferens
Prepuce and penis
Accessory sex glands
The poll glands of the dromedary and Bactrian camel
Reproductive Physiology
Puberty and sexual maturation
Seasonality
Species | Country | Breeding season |
C. dromedarius | Egypt | March to April |
|
| March to May |
| India | Mid-September to mid-February |
|
| November to February |
|
| October to March |
| Israel | January to April |
| Kenya | November–May (with peak in rainy seasons November–December, March–May) |
| Morocco | December to May |
| Nigeria | Wet season |
| Pakistan | December to March |
| Saudi Arabia | November to July |
| Somalia | October to March |
| Sudan | October to March |
| Tunisia | November to April |
| Turkmenistan | Mid-January to the end of May |
C. bactrianus | China | Mid-December to mid-April |
Seasonality is more pronounced in the Bactrian camel, with the rutting season lasting throughout the winter months and into early spring. Dominant males demonstrate reproductive activity earlier than young or subordinate males. Individual variations exist, and each male can exhibit breeding activity lasting from 50 to 100 days (Chen et al., 1980).
Spermatogenesis and sperm production
Spermatogenesis is similar to that described for other species (Tibary and Anouassi, 1997b). The cycle of the seminiferous tubule epithelium in dromedary camels and llamas consists of eight stages. Some differences exist between the two species in the percentage frequencies of cells representing each stage. In the dromedary, the most frequent stages of the seminiferous tubule epithelium cycle are stage 1 (22%) followed by stage 8 (16.4%), whereas in the llama, the most frequent cellular association is that of stage 8 (19%) followed by stage 3 (18%). The least frequent cellular association is that of stage 4 (8.2%) in the dromedary and stage 5 (5.8%) the llama. Stages 1–4 represent 54% of all the cellular associations in both species (Delhon and Lawzewitsch, 1987; Bustos-Obregon et al., 1997).
The llama epididymis presents six different segments based on histological and histochemical characteristics. Three of these segments are located in the head of the epididymis (I, II, III), two are located in the body (IV and V), and the sixth includes the distal part of the body and the tail of the epididymis. The major differences among these segments are the height of the epithelial cells, the positive intraepithelial periodic acid-Schiff reaction (PAS), alkaline phosphatase activity (ALP) and lactate dehydrogenase activity (LDH).
Segment I represents a short region where efferent ductules enter the epididymal duct. Segments II and III are characterized by high epithelial cell mitotic activity and weak LDH activity. The epithelial lining increases in height from 50 μm in Segment I to 60–140 μm in Segment II, and then decreases progressively to reach an average of 67, 65, 35 and 27 μm for Segments III, IV, V and VI, respectively. Epithelial cells in Segment IV contain amylase and PAS-positive and neuraminidase-resistant secretory granules. Segment V is characterized by strong ALP and LDH activities. Segment VI is characterized by moderate ALP and high LDH activities, and is highly packed with spermatozoa. The PAS reaction is absent in all but Segment IV and is weak in Segment VI. ALP activity is present in the proximal part of Segment V and, to a lesser extent, in the distal part of Segment V and in Segment VI (Delhon and Lawzewitsch, 1994).
Epididymal transit of camelid sperm is associated with a shift in the position of the cytoplasmic droplet of the sperm, which, in the llama, becomes distal but remains present in more than 60% of the spermatozoa in the terminal segment. The cytoplasmic droplet is lost when each spermatozoon reaches the ductus deferens (Delhon and Lawzewitsch, 1994). There is a decrease in the percentage of abnormal spermatozoa (bent midpiece and tail) during epididymal transit.
Sperm production is correlated with testicular size in SAC (Table 16.4). Mean testicular length is also correlated with testicular weight and may be used as a simple means of assessing testicular size in alpacas (Galloway, 2000).
Spermatogenesis occurs throughout the year in all camelids and shows wide seasonal variation. Sperm production is affected by geographical location (including nutritional, climatic and other environmental factors), herd management, extent of domestication and social structure of the camelid group (El-Wishy, 1988; Tibary and Vaughan, 2006).
In South America, the size of testicles in the male vicuña is affected by season and is greater in summer than in winter (Urquieta and Rojas, 1990; Urquieta et al., 1994). Spermatogenesis is not completely arrested during winter because all germ cell types are still observed at this time. The larger testicular size in summer has been attributed mainly to the increase in diameter of the seminiferous tubules and Leydig cells.
Mean testicular length (cm) | Proportion of males (%) | % Testicular tissue producing elongated spermatids |
<3 | 100 | 0 |
3–4 | 68 | <10 |
| 31 | 30–60 |
>4 | 36 | <10 |
| 31 | 10–60 |
| 31 | >60 |
In the male vicuña, individual testosterone values tend to be higher in summer, but some high values have also been noted in winter (Urquieta et al., 1994). Seasonal changes in plasma testosterone concentrations have also been reported in male alpacas; samples collected in late summer had the highest monthly mean values, whereas those collected in winter had the lowest (Losno and Coyotupa, 1979). The higher plasma testosterone levels in vicuñas in summer are probably responsible for the behavioural changes observed in males during this period of the year. High levels of testosterone are consistently found in dominant males and young males that are trying to recruit their own harem (Urquieta et al., 1994). Outside their normal habitat, llamas show a strong effect of season on sperm production, with low production in the summer (Gauly, 1997).
While many authors have not found any seasonal effects on spermatogenesis in the dromedary (Singh and Bharadwaj, 1978; Osman et al., 1979), others have reported reduced spermatogenic activity during the non-breeding season (Abdel Raouf et al., 1975). A steady drop of spermatogenic activity was observed in Egyptian dromedaries in the summer, manifested by an increasing number of exfoliated cells, increasing number and size of cytoplasmic vacuoles, and a decrease in sperm content. Spermatogenetic activity was at its lowest rate from June to August, and then increased in September, reaching a peak by November to January (Tingari et al., 1984). Activity fell in March, and decreased steadily from April onwards. Presumably, camels living south of the equator would exhibit activity in different months, although in a similar climatic season (Tingari et al., 1984).
The average daily sperm production in the dromedary was estimated at 0.751 × 109 for mature camels (8–10 years old; Ismail, 1982). The average gonadal sperm reserve and daily sperm production per gram of testicular parenchyma were estimated at 1.7–3.4 × 109 and 30.0–61 × 106, respectively (Osman and El Azab, 1974; El Wishy and Omar, 1975; Ismail, 1982, 1988). This is a low sperm production rate compared with other species. The sperm production rate is at its highest during the breeding season (Osman and El Azab, 1974; Abdel Raouf et al., 1975; Ismail, 1982; Tingari et al., 1984; Osman and Plöen, 1986; Tibary et al., 2007). Morphometric studies showed that testicular volume, weight of the testis, average diameter of Sertoli cells, volume of the intertubular compartment, relative and total volume and numbers of Leydig per testis, and percentage interstitial tissue in the parenchyma of the testis, were significantly higher during the winter and spring seasons (Riaz et al., 2011). Sperm reserve increases with age until 10 years old and then remains constant until 15 years old (Abdel Raouf et al., 1975; Ismail, 1982). A decrease in sperm production is noticed starting at 20 years old.
The epididymal sperm reserve of the dromedary averages 2.3 to 6.1 × 109 spermatozoa. Half to two thirds of this reserve is located in the body of the epididymis, with the head and tail contributing only 5.2–12.3 and 21–36%, respectively. The reported relative distribution of epididymal sperm differs according to the study (Akingbemi and Aire, 1991; Tibary and Anouassi, 1997b).
Epididymal transit and sperm maturation
Epididymal sperm transit is poorly studied in SAC. In the llama, as already noted, epididymal transit causes a shift in the position of the cytoplasmic droplet, which becomes distal. However, droplets were present in more than 60% of the spermatozoa in the terminal segment of the epididymis and were not completely lost until spermatozoa reached the ductus deferens (Delhon and Lawzewitsch, 1994).
In the dromedary, sperm transport through the epididymis lasts on average 4.3 days (0.22 days in the head, 2.5 days in the body and 1.5 days in the tail) (Ismail, 1982, 1988). The fertilizing capacity of the dromedary sperm is acquired during the transit in the head and body of the epididymis, which lasts about 2.9 days (Ismail, 1982). Morphological changes of the spermatozoa were observed as the spermatozoa moved through the epididymis, signifying a maturation process (Osman and Plöen, 1986). The dromedary contrasts with other domestic species in that a high number of epididymal spermatozoa are morphologically abnormal. The migration of the cytoplasmic droplet is slow and a large proportion of spermatozoa in the tail of the epididymis still have such a droplet (Osman and Plöen, 1986).
Mating Behaviour and Ejaculation
All male camelids display the flehmen response after smelling freshly excreted urine and faeces of the female. The head is lifted, the upper lip is elevated without curling and the mouth is opened slightly (Tibary and Anouassi, 1997b; Tibary, 2003). When introduced into a female herd, the male will chase a sexually receptive female and try to force her down by mounting her and putting pressure on her pelvis (llamas and alpacas) or neck (camels). Some males may protrude the penis and display rotation of the glans as they are attempting to mount. Erection and copulation occur with the female sitting in sternal recumbency. The penis is fully extended after successful vaginal penetration (Tibary and Anouassi, 1997b; Tibary, 2003).
Mating behaviour in South American Camelids (SAC)
During copulation, llamas and alpacas produce a low guttural sound known as ‘orgling’. This sound is produced as air is expired through the mouth while the cheeks are inflated. Males can display all aspects of copulatory behaviour without achieving intromission (Fernandez-Baca, 1970).
The duration of copulation is variable, averaging 20–25 min and ranging from a few minutes to more than an hour (Table 16.5). There is no correlation between copulation time and conception rate (Vaughan, 2001). Factors affecting the length of copulation are species and breed, age of male and female, sire, season, frequency of mating and presence of other males (Bravo et al., 1997c). Duration of copulation tends to be shorter for younger males and decreases in all males with increased frequency of mating (Vaughan, 2001; Vaughan et al., 2003a,b; Tibary and Vaughan, 2006). Length of copulation is longer for multiparous females (21.5 min) than for maiden females (14.7 min). Also, when several males are present in the same herd, copulation is shorter than when no other males are present (8 versus 21.5 min) (Smith et al., 1994).
Table 16.5. Mating duration in camelids.
Alpaca males exhibit different sexual behaviour patterns if they are maintained with females all year round from when they are run in separate flocks. In the former case, they show distinct seasonal variations in activity. In the latter case, they show continuous libido and breeding capability, serving females whenever they have an opportunity (Fernandez-Baca et al., 1972); higher plasma testosterone levels have been found in this situation (Losno and Coyotupa, 1979), although no related changes in fertility rate have been reported (Urquieta et al., 1994). Aggressive behaviour towards other males has been observed, culminating in a direct confrontation with biting, and also chest ramming, which can lead to serious injuries, especially if the canine teeth are well developed (Tibary, 2003).
Ejaculation in camelids appears to occur throughout the entire duration of copulation (Tibary and Anouassi, 1997b; Tibary and Vaughan, 2006). Sperm is present in the ejaculate of alpacas within 5 min of the initiation of copulation (Fernandez-Baca, 1970; Kubicek, 1974; Lichtenwalner et al., 1996a). In the llama, urethral pulses increase in frequency 4 min after the start of copulation and occur in clusters every minute. Each cluster lasts 20 s and is composed of four to five rapid urethral pulses followed by a tremor of the whole body. Each cluster is preceded by two repositions and 38 pelvic thrusts. The urethral pulses accompanying the whole body tremor are considered to be a single ejaculation (Lichtenwalner et al., 1996a, 1997). Thus, ejaculation in the llama starts approximately 4 min after the beginning of copulation and occurs every minute (18 to 19 ejaculations/22 min). These observations (multiple ejaculation and tremors during ejaculation) have been confirmed by the pattern of ejaculation observed during semen collection using an artificial vagina (Lichtenwalner et al., 1996a,b, 1997). Semen is deposited deep in the uterine horns and most likely at the papilla of the utero-tubal junction (Bravo et al., 2002; Tibary and Vaughan, 2006). Intrauterine deposition of semen helps to compensate for a low sperm concentration and plays a major role in induction of ovulation.
Rutting behaviour in Old World Camelids (OWC)
The onset of the breeding season is accompanied by an increased aggressiveness of the male dromedary towards other animals in the herd (especially other males) and sometimes even towards people. Confined males show increased pacing and anxiety, and attempts to break out of the corral or pen are common. During the breeding season, male dromedaries spend most of their time guarding the herd and surveying for any strange male or female in heat. Because of this continuous stress, a net reduction of food intake and increased digestive transit (stress diarrhoea) are observed, and males tend to lose weight (up to 35%) during the breeding season, sometimes to the point of emaciation (Tibary and Anouassi, 1997b). Aggressive behaviour during the breeding season has also been described in the Bactrian camel (Chen et al., 1980). In a free-roaming herd, dominant males chase each other and engage in fighting, which can lead to serious biting injuries.
Sexual behaviour in the dromedary camel is characterized by frequent exteriorization of the soft palate (also called dulaa or dulla) (Plate 50) and marking (Tibary and Anouassi, 1997b). The protrusion of the dulla occurs at an interval of 5 to 30 min and is accompanied by a loud gurgling/roaring sound. Protrusion of the soft palate becomes more frequent with increased stimulation (presence of another male or females). Some dromedaries do not exhibit complete exteriorization of the soft palate, but instead only a mere flapping; these are usually older animals or males that have had their soft palate removed surgically during their racing careers. Bactrian camels do not exteriorize the soft palate to the same extent as dromedaries during their sexual behaviour, but both Bactrian camels and dromedaries display more saliva production and frothing than usual (Plate 51).
Marking takes two major forms: (i) urine spraying; and (ii) smudging of the poll gland secretions. Plate 52 shows a male dromedary rubbing poll gland secretions on to the ground. Both types of marking behaviour have also been described in the Bactrian camel (Chen et al., 1980; Tibary and Anouassi, 1997b).
Male dromedaries and Bactrian camels frequently produce a metallic sound by grinding the molars via lateral movements of the lower jaw. This sound can be produced any time, but usually replaces the gurgling and ejection of the soft palate during copulation.
As already noted for camelids in general, copulation is completed with the female sitting in the sternal position. The duration of copulation in dromedaries is variable (Table 16.5) (Abdel Rahim and El-Nazier, 1992; Agarwal et al., 1995). Among factors affecting the length of copulation are breed, age, sire, season and frequency of mating (Tibary and Anouassi, 1997b; Tibary et al., 2005). The duration of copulation tends to be shorter at the beginning of the breeding season and in younger males. The copulation time decreases as weather becomes warmer and the end of the breeding season approaches. Bactrian camels exhibit similar copulation behaviour. According to one study, copulation time is limited to 1–6 min in 86% of the matings, but can be as long as 10 min (Chen et al., 1980).
The dromedary displays multiple distinct periods of pelvic thrusting, gluteal muscle contractions and semen discharge during copulation. Contractions of the ischiocavernous, bulbospongious and urethralis muscles surrounding the pelvic urethra may be correlated with ejaculation. Ejaculation starts within a couple of minutes of intromission and continues throughout the copulation period.
Breeding Soundness Examination
Studies on the pathology of the male camelid reproductive tract are scarce (Tibary and Anouassi, 1997d, 2002; Tibary et al., 2001). A comprehensive study on abnormalities in alpacas examined 3015 breeding males and 792 male reproductive tracts at post-mortem (Sumar, 1983). The incidence of pathological conditions in breeding alpacas was 18.2% (testicular hypoplasia 10%, cryptorchidism 5.7% and ectopic testes 2.5%). In slaughterhouse material, the incidence of abnormalities was 30.2% (hypoplasia 10.8%, cryptorchidism 3%, ectopic testes 1.9%, testicular cysts 14.5%) (Sumar, 1983).
Male breeding soundness examination (BSE) is an important part of the evaluation of herd infertility and decision making in the selection or purchase of a herd sire (Tibary and Anouassi, 1997c). Most often, the evaluation of males for infertility is attempted only if a gross abnormality is seen or after a long period of unsuccessful matings occurs, which limits the ability of the clinician to reach a diagnosis in time to prevent economic loss. Examination of the male should be conducted methodically to avoid oversight of any problems that may affect reproductive performance. A standard for BSE is yet to be determined for camelids. Male evaluation should include: identification of the animal, health and reproductive history, a detailed description of the reason(s) for examination, general health examination, special examination of the genital system and an evaluation of mating ability. A complete blood count and serum biochemistry panel should be performed on all males recently introduced to the farm. New males generally represent one of the most common biosecurity breaches in a camelid operation, and it is highly recommended to test for contagious diseases upon purchase. Importantly, the BSE should also include an evaluation of semen characteristics. Accordingly, an account of both semen collection and seminal characteristics is included in this section.
History and physical examination
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