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Animal Reproduction Science 62 2000 173–193 www.elsevier.comrlocateranireprosci
Reproductive aspects and storage of semen in Camelidae
P.W. Bravo
a,
, J.A. Skidmore
b
, X.X. Zhao
c
a
Centro Experimental La Raya, UniÕersidad Nacional San Antonio Abad, Cusco, Peru
b
The Camel Reproduction Centre, Dubai, United Arab Emirates
c
Department of Veterinary Medicine, Gansu Agricultural UniÕersity, Lanzhou, Gansu, People’s Republic of China
Abstract
The characteristics of male and female reproductive tracts and reproductive physiology in camelids are described. An account is given on methods of collection, characteristics and storage
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of semen, and fertility after artificial insemination AI with fresh, liquid-stored and frozen–thawed lamoid and camel semen. q 2000 Published by Elsevier Science B.V.
Keywords: Camel; Dromedary; Bactrian; Llama; Alpaca; Vicuna
1. Introduction
There are two genera within the Camelidae family, Camelus and Lama. The genus Ž
. Camelus consists of Camelus dromedarius, dromedary camel
one hump and C.
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bactrianus, Bactrian camel two humps . Both species are also known as Old World camelids. The genus Lama constitutes of four species: two domesticated, Lama glama,
llama; L. pacos, alpaca; and two wild species, L. guanicoe, guanaco, and L. Õicugna, vicuna. They are collectively known as South American or New World camelids, and
for the purpose of this review, as lamoids. All camelids live on harsh conditions, camels in desert areas, and lamoids on high altitude terrains. All of them have 37 pairs of
chromosomes. Both camels and lamoids can interbred within their genera and the offspring is fertile.
Corresponding author. Present address: Dept. Animal Science, Brighan Young University, Provo, UT 84602, USA.
0378-4320r00r - see front matter q 2000 Published by Elsevier Science B.V. Ž
. PII: S 0 3 7 8 - 4 3 2 0 0 0 0 0 1 5 8 - 5
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Progress on artificial insemination AI , semen preservation and related techniques in camelids has been slow in comparison to other livestock species. As there is relatively
limited information in the literature on the anatomy and physiology of the male and female camelid, first, a short account on these aspects is given.
2. The male reproductive tract
The testes of Camelidae are ovoid in shape and are found in the scrotum in a perineal position, as in the dog and pig. The testes of camels are descended at birth and very
small, but an increase in size occurs at the onset of puberty, with the maximum weight attained at 10–14 years of age. In lamoids, the testes may not be in the scrotum at birth,
but descended by 6 months of age. In mature alpaca and llama, the testes weigh 18 and 24 g, respectively, which represents approximately 0.02–0.03 of the total body weight.
Testicular size and weight for llamas, alpacas and vicunas are given in Table 1.
The camel testes vary in length from 7 to 10 cm in dromedary and 12 to 14 cm in Ž
Bactrian and weigh 80–100 g each, the left tending to be bigger than the right Tayeb, .
1951–1952; Zhao, 1995 . It should be noted that there are seasonal changes in the size of the testes, which become enlarged and protrude when male camels are sexually active
in the rutting season. The diameter of the seminiferous tubules in the alpaca is between 174 and 237 mm
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Casas et al., 1993–1996 . In the camel, the seminiferous tubules have smaller diameter when the male is not in rut. The season does not have an effect on the size of
spermatozoa, although it can effect their number. The estimated production of camel spermatozoa is 8.1 = 10
6
sperm cellsrday at the end of spring, and it drops to 4.2 = 10
6
day
y1
at the end of summer. There are no differences in the size of Camelidae
Table 1 Ž
. Ž .
Mean testicular size length=transverse axis and weight g of llamas, alpacas and vicunas of different ages Ž
. ns158 alpacas, 54 llamas, 6 vicunas
a b
c
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Age months Llama
Alpaca Vicuna
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Size cm Weight
Size Weight
Size
d
6 2.4=1.4
na na
na na
12 3.4=2.3
5.1 2.3=1.5
2.9 na
18 3.5=2.6
14.0 2.8=1.9
6.6 na
24 3.9=2.3
17.4 3.3=2.2
9.9 na
30 4.4=2.5
17.8 3.6=2.3
13.9 na
36 4.5=2.7
18.2 3.6=2.4
13.6 2.5=1.4
Adults 5.4=3.3
na 3.7=2.4
17.2 3.3=1.9
a
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Bravo et al. 1992 .
b
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Bravo 1978 , unpublished data.
c
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Urquieta et al. 1991 .
d
Not available.
spermatozoa, with the total length being 50 mm, of the head 5.3 mm, and the tail 37 mm Ž
. Palomino, 1962; Merlian et al., 1979 . The cycle of the seminiferous epithelium of the
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male llama series of changes with well-defined cellular associations has been defined as eight stages with the relative frequencies of cell populations being 9.8, 12.5,
17.7, 14.1, 5.8, 8.1, 13.0 and 18.9, for stages 1 through 8, respectively Ž
. Dehlon and von Lawzewitch, 1987 .
The epididymis is located on the anterior edge of the testis and extends from the interior extremity to just above the upper edge. Macroscopically, it can be divided into
head, body and tail regions. Histologically, the epididymis has six segments differenti- ated by roman numerals. Segment I is short where ductuli efferentia join the epididymis.
Segments II and III show maximal epithelial height and mitotic activity, respectively,
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and some lactate dehydrogenase LDH activity. Epithelial cells in segment IV contain periodic acid-Schiff activity, amylase and neuramidase-resistant secretory granules.
Segment V shows a strong acid phosphatase and LDH activities. Segment VI has moderate acid phosphatase and high LDH activities, as well as maximum sperm storage
Ž
. Dehlon and von Lawzewitsch, 1994 .
The vas deferens, enclosed in the spermatic cord, measures 35–40 cm in lamoids and 45–50 cm in camels. It has two portions, the proper vas deferens and a fusiform
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dilation, the ampulla. A distinct ampulla is not observable in camels Zhao, 1995 . In lamoids, the ampulla is approximately 4 mm in diameter and is located on the dorsal
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aspect of the bladder Osorio and San Martin, 1966 . Histological studies of the ampulla reveal a dilation of the submucosa with the presence of glandular acini. Observations in
adult alpacas do not reveal large numbers of spermatozoa in the ampulla; hence, it is not a place for storage of spermatozoa as occurs in bulls and rams. This may be the reason
why semen collection by electroejaculation is not reliable.
The penis is fibroelastic with its sigmoid-shaped flexure in front of the scrotum, not behind it as in the bull. The length is 35–40 cm in lamoids and 37–60 cm in camels and
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the diameter decreases from its root 22 cm towards the glans penis 4 cm . The glans penis is 8.5 cm long in camels and ends in a cartilaginous process, which supposedly
directs the penis through the cervix of the female during copulation. It is curved along its vertical plane, giving it a hook shape with a definite neck between the glans of the
body of the penis. These observations are important when designing an artificial vagina Ž
. AV . The urethral opening is located at the tip of a second and smaller urethral process.
The detachment of the glans penis from the prepuce in lamoids seems to be related to the secretion of testosterone. The initiation of penis–prepuce detachment in llamas
appears at 13–15 months and continues from the tip caudally. By 21–22 months of age, the penis is completely detached and the testosterone concentrations are almost at adult
values. In alpacas, 12.2 of males shows an initiation of detachment by 12 months of age and by 24 and 34 months of age, the penis is free from any attachment to the
prepuce in 59.5 and 94.4 of males, respectively.
The prepuce of the camel is voluminous, flattened from side to side and triangular in shape when viewed laterally. In all Camelidae, it is directed caudally and because of
this, the male urinates towards the rear, but when erection of the penis occurs, the cranial prepucial muscles pull the prepuce, and also the penis, forward from their
backward position.
The accessory sex glands are the prostate and the bulbourethral glands, as camelids do not have vesicular glands. The prostate gland has two components, a compact and
diffuse part, the two forming an H-shape which lies dorsal to the pelvic urethra. The capsule of the prostate is thick and supplied with smooth muscles fibres. The bul-
bourethral glands are two compact, almond-shaped structures and are located on either side of the terminal portion of the pelvic urethra. They may be palpated digitally via the
rectum. The capsule surrounding these glands contains striated muscle.
3. The female reproductive tract
