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Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca
Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca
CHAPTER
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Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca JULIO SUMAR and GREGG P. ADAMS
P
resent-day alpacas and llamas developed from a common feral ancestry in South America during the last millennium. Many aspects of their reproductive pattern are similar but extrapolation from one species to another must be done with caution. Although differences in the reproductive biology have not been documented, few critical studies have been conducted to compare the various species of camelids. Breeding experiences and research with llamas and alpacas under different latitudes and lower altitudes such as those being carried out in Australia, Canada, and the United States may soon contribute to a better understanding of the biology of reproduction in llamas and alpacas.
confirmation of ovulation and is a rapid method of “progesterone testing.” The oviducts are long and tortuous and end in an open bursa that normally covers the ovary. The tip of the uterine horns in both domestic species is blunt and
Table 115-1 Dimensions of the Reproductive Organs of Female Llamas and Alpacas VALUE (cm): MEAN ± SD Organ Dimension
GROSS AND ULTRASONOGRAPHIC ANATOMY OF THE FEMALE The gross appearance of the female reproductive organs in the alpaca is illustrated in Figures 115-1 and 115-2. The dimensions of alpaca and llama reproductive tracts are compared in Table 115-1.1–3 The ultrasound appearance of the ovary is illustrated in Figure 115-3.4 The ovum itself is too small to be detected by present-day ultrasound instruments, but antral follicles as small as 1 to 2 mm in diameter can be detected. Several fluid-filled follicles (e.g., from four to eight), with or without a corpus luteum, may be detected in the ovaries at any given time. On ultrasound examination, the appearance of the llama or alpaca ovary is more similar to that of the cow than of the mare. The ovary and ovarian structures are, however, smaller than in cows (e.g., ovulatory-sized follicle, 10 mm versus 16 mm in diameter, respectively; mature corpus luteum, 13 mm versus 28 mm, respectively). As in the cow but not the mare, ovarian follicles are arranged in a peripheral cortex, and ovulation can take place at any spot on the surface of the ovary. The corpus luteum and large follicles protrude distinctly from the surface of the ovary in llamas and are readily palpable. On ultrasonography, corpora lutea are seen to have a very characteristic spherical shape and are hypoechogenic (dark gray) relative to the surrounding tissues. A horizontal echogenic (light gray) area traversing the center of the corpus luteum also is a distinctive ultrasonographic feature. The capability to ultrasonographically recognize and monitor the development of the corpus luteum is fortuitous because it allows
Length of labia Vagina (hymen to cervix) Length Diameter Cervix Length Diameter Number of rings Uterine body Length Diameter Uterine horns Length Diameter Oviduct length Right ovary Length Depth Width Left ovary Length Depth Width
Alpaca
Llama
2.5
5.0
13.4 ± 2.0 3.4 ± 0.7
15–21 5
2 — 2–3
2–5 2–4 2–3
3.0 ± 0.7 —
3–5 3–5
7.9 ± 1.3 — 20.4 ± 4.2
8.5–15 2.5–4 10.5–18.3
1.6 ± 0.3 1.1 ± 0.2 1.1 ± 0.2
1.3–2.5 1.4–2.0 0.6–1.0
1.6 ± 0.3 1.1 ± 0.2 1.1 ± 0.2
1.5–2.5 1.5–2.5 0.5–1.0
SD, standard deviation. Data from Sato A, Montoya L: Aparato reproductor de la alpaca (Lama pacos). Anatomía macroscópica. IVITA/CICCS, Universidad Nacional Mayor de San Marcos. Revista de Camélidos Sudamericanos 1990;7:23; Bravo PW, Sumar J: Some anatomical parameters of the reproductive tract in alpacas [in Spanish]. Resúmenes de inves, Universidad Nacional Mayor de San Marcos, Lima, Peru; Fowler ME: Medicine and surgery of South American camelids: llama, alpaca, vicuña, guanaco. Ames, IA: Iowa University Press, 1989; and Sumar J: Studies on reproductive pathology in alpacas. Master’s thesis, Department of Obstetrics and Gynaecology, Veterinary Medicine Faculty, Swedish University of Agrarian Sciences, Uppsala, Sweden, 90 pp.
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A
B
D
C
E Fig. 115-1 Gross appearance of alpaca ovaries. A, Cross section showing a corpus luteum (CL) and numerous follicles (F). B, Recently ovulated follicle with an ovulatory papilla (arrow). C, Mature 12-mm follicle. D, Cross section of a corpus hemorrhagicum. E, Corpus luteum and several follicles in the ovaries of a pregnant alpaca (at 2 months of gestation).
Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca
A
857
B Fig. 115-2 Reproductive organs of the alpaca and llama. A, Craniolateral view of the suspended reproductive tract of an alpaca at slaughter showing the left and right uterine horns (lh, rh) suspended by the broad ligament (bl), the left and right ovaries (lo, ro), and the left oviduct (black arrow). B, Dorsal view of the excised tract of a llama. The uterine horns are relatively short, not tapered, and come to a blunt uterotubal junction, unlike in cows or ewes, in which the uterine horns are long and taper toward the uterotubal junction.
Fig. 115-3 Ultrasound images of the llama ovary, uterus, and cervix. Morphologic features are characteristic of the luteal phase:, a follicle and a corpus luteum in the ovary, curled uterine horn, and distinct cervical folds. The scale at the top is in 1-cm increments, and the images are in a sagittal plane with the cranial direction to the left.4
rounded, unlike in other ruminants, in which it tapers slowly toward the uterotubal junction. Accordingly, the oviduct of alpacas and llamas opens into the uterine horns through a small, raised papilla, which acts as a welldefined sphincter. Even under great pressure it is not possible to flush liquids from the uterus into the oviduct, but flushing in the opposite direction is possible. As in other domestic species, the uterus of the alpaca and llama is bicornuate, but the left uterine horn is slightly longer than the right (7.9 ± 1.3 cm versus 7.4 ± 0.9 cm), even in the nullipara. In situ, the uterine horns curl ventrally and caudally, and the degree of curl is maximal during the luteal phase (progesterone dominance) and minimal during the follicular phase (estrogen dominance)4 (Fig. 115-4). The degree of uterine horn curl is much less than in other ruminants (e.g., sheep, goats, cattle), and in the excised tract, the uterine horns shrink and may not appear curled at all, but rather appear Y-shaped. The echotexture (grain
of the ultrasound image) of the uterus changes from homogeneous light gray (smooth and uniform) during the luteal phase and early pregnancy to heterogeneous and increasingly dark during the follicular phase (see Fig. 115-4). Estrogen causes the reproductive tissues to imbibe water and, since fluid is nonechogenic, the uterus becomes relatively hypoechogenic during the follicular phase. A similar pattern has been reported in cows.5 In nonpregnant llamas, the body of the uterus is short (2 to 3 cm) and not clearly differentiated from the base of either horn on ultrasonography. Uterine tone, based on digital palpation, is maximal during the follicular phase and minimal during the luteal phase and early pregnancy, as in cattle. The uterus is remarkably turgid during the follicular phase, and longitudinal grooves can be palpated along its upper surface. Thus, both the homogeneous dark echotexture and extreme turgidity of the uterus indicate a profound accumulation of interstitial fluid during follicular dominance. The tubular genitalia are suspended
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Fig. 115-4 Characteristic differences in the reproductive organs of alpacas and llamas during the follicular phase (receptive) versus the luteal phase (nonreceptive).4
from the lateral pelvic and abdominal walls by the broad ligament; the ligament attaches along the ventral aspect of the uterus such that the uterine body and horns are readily palpable per rectum. The cervix has two or three irregular annular or spiral folds. On ultrasonography, the cervical folds appear as transverse echogenic bands and are especially prominent during the luteal phase and pregnancy (see Fig. 115-4). Presumably, edema of the cervical folds during the follicular phase is responsible for the dark echotexture and indistinct appearance on the sonogram characteristic of this phase. The vagina is surprisingly long and commonly exceeds 20 cm.
ANATOMY OF THE MALE In the adult alpaca, the testes are found in a nonpendulous scrotum in the perineal region 5 to 9 cm ventral to the anus.1,6 The testes are small and elliptical and positioned so that the long axis is oriented vertically or in an oblique dorsocaudal orientation. Normally, both testes are of the same size and of a firm consistency, with free movement inside the scrotum. The head, body, and tail of the epididymis are small and firmly connected to the
testes. The average weight of one fully developed alpaca testis is approximately 17 g (range, 13 to 28 g), measuring between 4 and 5 cm in length and 2.5 to 3.0 cm in depth.7 Considerable variation, however, has been found in testicle size and liveweight in alpacas. In one study, male llamas that reached the age of 2 years (83 kg of body weight) had testes weighing about 12 g, with dimensions of 3.5 × 2.2 cm and a volume of 13 cc. At the age of 5 years, llama testes weighed about 24 g, with dimensions of 5.0 cm × 2.7 cm and a volume of 22 cc.9 In another study,10 body weight and testicular index increased linearly from birth to 24 months of age, with a subsequent slower increase to adulthood. A positive relationship was found between age and testicular index (R2 = 0.88). The deferent duct (ductus deferens) is very thin (2 mm) at its beginning and thickens (3 mm) when it reaches the abdominal cavity and ends near the bladder, forming what in other species is the ampullae.14 The prostate consists of a clearly defined body at the neck of the bladder, and a disseminate part along the pelvic urethra. The prostate body measures approximately 3 cm × 2 cm and is easily palpable per rectum in the adult. The bulbourethral glands are oval and are located on either side of the urethra at the pelvic outlet. Camelids have no vesicular glands.
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Fig. 115-5 Penis of alpacas show-
A
B
C
ing progressive stages of separation of the free end of the penis from its preputial adhesions. A, Complete adhesion with only the tip of the cartilaginous process showing; B, the beginning of separation; C, persistent adhesion of the tip of the penis, and D, a penis completely free of its preputial adhesions.
D
The penis is fibroelastic, with a small (approximately 1 cm across) cartilaginous process that has a hooklike curve at its tip (Fig. 115-5). The length of the nonerect penis in the alpaca is 26 cm, and the sigmoid flexure is prescrotal.6 The prepuce is small, located approximately 15 cm caudal to the umbilicus, and has a triangular opening that is oriented caudally.1 During urination, camelids direct the stream of urine backward between the hind legs. The protractor preputial muscle pulls the prepuce forward before mating, changing the direction of the preputial opening and thus allowing for the penis to be directed forward.
PUBERTY Young female alpacas of 12 to 13 months of age display behavioral estrus similar to that in adult alpacas.11 A majority of females display sexual receptivity at 12 months of age even though ovarian activity begins at
10 months of age, with the presence of follicles of 5 mm or more in diameter. In a study carried out in southern Peru using 280 yearling alpaca females,12 a highly significant relationship (P < 0.001) was found between body weight at mating and subsequent birth rates. For each kilogram increase in body weight up to 33 kg, a 5% increase in natality was observed; for increases in excess of 33 kg, the percentage of nonpregnant females was relatively independent of body weight. In traditional Peruvian production systems, only about 50% of yearling alpacas reach a body weight of 33 kg at mating time (January through March). Therefore, breeding age is postponed to 2 years of age and often to 3 years of age in llamas. It also has been shown that with better nutrition after weaning (7 to 8 months of age), nearly 100% of yearling alpacas can reach 33 kg body weight.13 In males, the penis is completely adherent to the prepuce at birth. Under the influence of testosterone, the adhesions disappear gradually as the male matures.6,7
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At 1 year of age the males show sexual interest in the females, but only about 8% of alpaca males have complete liberation of penis-prepuce adhesions and are capable of copulating. At 2 years of age, approximately 70% of the males are free of adhesions, and 100% are free at 3 years of age (see Fig. 115-5). Puberty, based on penisprepuce detachment, is attained at an average of 21 months of age (range, 9 to 31 months) in llamas, at a body weight of 70 kg (range, 48 to 92 kg).10 Also, testosterone concentration starts to increase exponentially at 21 months of age (to 300 pg/mL), reaching a plateau at 30 months of age (650 pg/ml).9,10 From 2 to 11 months, the testes grow slowly (infantile stage), with a sequential increase of noncanalized sex cords and undifferentiated Leydig cells.14 At an age of about 12 months, the sex cords start to develop a distinct lumen containing Sertoli cells and spermatogonia. The first spermatozoa appear at about 18 months of age, with half of the animals having spermatozoa in the caput epididymidis. From 18 months, the number of Leydig cells increases considerably, and by 20 to 24 months, the diameter of the tubules is greatly increased, with presence of considerable numbers of spermatozoa in the caput epididymidis. Beginning at 3 years of age, normal alpacas have spermatozoa in the epididymis. Spermatogenesis is initiated in some alpacas as early as 16 months and in others as late as 26 months.59 The general practice in Peru is to start using the males for breeding at 3 years of age.
SEASONALITY Studies with alpacas and llamas in their natural habitat in the highlands of Peru showed that sexual activity is seasonal and lasts from December to March (summer months). These are the warmest months of the year, with sufficient rain and abundant green forage.15 In farms on which males and females are together all year, the birthing and breeding times lie within this time range. This marked seasonality of reproduction also is characteristic of the wild species—the vicuña and guanaco.16 Observations in different zoological parks of the world, however, indicate that llamas are year-round breeders.17 In North America, where llamas are kept under good nutritional conditions year-round and copulation is allowed only on an individual basis, they are considered nonseasonal breeders. An analysis of llama birthing records from the Rocky Mountains area of the United States revealed that births occurred during all months of the year, but with a preponderance (73%) between June and December.18 In another study, ovulation, fertilization, and embryo survival rates were not affected by the season of the year.19 Males show much less seasonal variation in libido and testicular function. The male alpaca is capable of producing fertile ejaculates year-round, but as in other domestic species, semen quality and libido are affected by season and availability of feed. Under North American conditions of management, no seasonal effect on testosterone values of adult male llamas has been found.10 In a study of male alpacas and llamas in Peru, plasma testosterone concentrations were markedly elevated during spring and summer (the breeding season),
Table 115-2 Seasonal Variation in Peripheral Testosterone Level in Male Alpacas and Llamas TESTOSTERONE CONCENTRATION (pg/ml): MEAN ± SEM Season: Month Spring: March Summer: June Autumn: September Winter: December
Alpacas
Llamas
1142 ± 108 992 ± 388 877 ± 91 2445 ± 694
208 ± 52 37 ± 14.9 291 ± 74 362 ± 73
SEM, standard error of the mean. Data from Lichtenwalner AB, Woods GL, Weber JA: Male llama choice between receptive and nonreceptive females. Appl Anim Behav Sci 1998;59:349–356.
whereas lower levels occurred in autumn and winter20 (Table 115-2).
PATTERN OF OVARIAN EVENTS Because copulation is a necessary prelude to ovulation, alpacas and llamas have been classified as reflex ovulators or induced ovulators, as opposed to spontaneous ovulators.21,22 Female alpacas and llamas do not have estrous cycles like those in other species of large domestic animal; estrus and ovulation are not manifested in a repetitive cycle. Highlights of ovarian function are presented here, but a more detailed account is found in Chapter 118. Based on laparoscopic examination of the ovaries of alpacas (n = 20)23 and llamas (n = 12),24 it was found that growth, maintenance, and regression of a follicle each required an average of 4 days (total, 12 days; range, 9 to 17 days). In a study of 74 llamas kept in their natural habitat in South America and examined daily by transrectal ultrasonography,25 successive dominant follicles emerged at intervals of 19.8 ± 0.7 days in unmated and vasectomy-mated llamas and 14.8 ± 0.6 days in pregnant llamas. The minimum time to ovulation was estimated to be 26 hours after natural mating and 24 hours after treatment with intramuscular human chorionic gonadotropin (hCG) at a dose of 500 to 700 IU.21 Using an ultrasonographic technique in llamas, ovulation was detected, on average, 2 days (range, 1 to 3 days) after a single mating.4,25 Single service by an intact or vasectomized male resulted in an ovulation rate of 77% to 82%, and an increase in the number of services by intact males to three within a period of 24 hours did not significantly affect ovulation rate.15 In females allowed a single mating, 50% ovulated between 26 and 30 hours, 24% ovulated between 30 and 72 hours, and 26% failed to ovulate after mating.26 Forty percent of the animals that failed to ovulate were yearlings, and 15% were adults. Some evidence indicates that females can ovulate without coital stimulation or exogenous hormones, especially when initially isolated from and then reintroduced
Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca to a male. The rate of spontaneous ovulation has been reported to be approximately 5% in alpacas.6,15 Spontaneous ovulation was detected in 3 of 20 (15%) llamas by palpation in one study,27 and in 3 of 34 (9%) llamas by ultrasonography in two other studies.4,25 Laterality of ovulation (from either the left or the right ovary), as indicated by the presence of a corpus luteum of pregnancy, has been reported in several studies.6,24,26,28,29 On examinations of the genital organs of 928 pregnant alpacas, no differences were found in the ovulatory rate between ovaries. A corpus luteum was detected in the right ovary in 51% of the alpacas, in the left in 47%, and in both ovaries in 2%.28 In the llama (n = 110), a corpus luteum was detected in the right ovary in 54% of females, in the left ovary in 44%, and in both ovaries in 1%.29 Luteal function after sterile and fertile matings has been studied in llamas by several investigators.6,25,27,28,30 In nonpregnant alpacas, the corpus luteum underwent rapid development after ovulation, reached maximum size and secretory activity at 8 to 9 days after mating, and declined sharply in both size and secretory activity by 12 days after mating.31 Similar characteristics were observed in nonpregnant llamas (i.e., mated to vasectomized males) evaluated by ultrasonography.32 Although prolonged luteal phases have been anecdotally reported in association with embryonic loss, spontaneous pseudopregnancy (prolonged luteal phase unassociated with embryonic loss) has been wrongly inferred in llamas.21 A prolonged luteal phase was not observed in any sterile-mated (nonpregnant) alpacas or llamas.25,27,31,32 In pregnant animals, the corpus luteum reaches maximal diameter at 22 days after mating and is maintained throughout gestation.32,33
SEXUAL RECEPTIVITY AND MATING BEHAVIOR In the absence of copulatory stimulation, female alpacas display periods of sexual receptivity of up to 36 days, with short periods of nonreceptivity that may last 48 hours.21 Considerable variability in display of overt receptivity is apparent between individual animals, regardless of parity. The variability in sexual receptivity may be attributable primarily to the degree of follicle maturity at any given stage of the follicular phase; however, no documentation is available in this regard. The receptive female will assume the prone position (ventral recumbency) after a short period of pursuit by the male, or she may approach a male that is copulating with another female and adopt the prone position21 (Fig. 115-6). Some receptive females may occasionally display mounting behavior with other females of the herd, although such behavior is much less common than in cattle. If the female is nonreceptive, rejection is shown by running away and spitting at the male. Males will attempt to mount receptive or nonreceptive females; their initial approach is indiscriminate. In a study of sexual behavior in llamas, the male attempted to mount eight of nine females a total of 60 times during a 12-hour period.20 Each of the eight females was mounted an average of four times, for an average of 5 minutes per mount; mounting was attempted irrespective of the receptivity of the female. Normally, only receptive females will adopt the
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Fig. 115-6 A pair of copulating alpacas in a prone position, surrounded by six females also in the prone position, typical of a display of sexual receptivity.
prone position, but in some instances, aggressive males can force nonreceptive females to adopt the prone position. During the very short courting phase and during mating, the male makes blowing, grunting, nasal sounds. Copulation takes place in a recumbent position, with the male mounted above and just behind the female. The female assumes a very passive attitude during copulation and, in some instances when copulation is prolonged, will appear to tire and may assume lateral recumbency. Compared with other domestic species, coitus is remarkably prolonged in alpacas and llamas (10 to 50 minutes).6 After a certain amount of time has elapsed, the continuous association of males and females somehow inhibits the sexual activity of the males, a situation that may prevent mating of females returning to estrus after a sterile mating or early embryonic death.
MATING SYSTEMS Observation of the sexual activity in the open field, when males and females are joined, at the beginning of the sexual season, showed that mating activity was particularly intense during the first week of the breeding season.34 Greater than 70% of 262 females were recorded as having been mated at least once during this short period. But sexual activity decreased thereafter, reaching a frequency of zero in some instances. After different males were introduced and the original males were removed, however, sexual activity was reactivated and reached a level comparable to that of the first week.35 Based on these observations, a breeding system named the alternating or rotary system was developed.36 This system works well in the large herds commonly found in southern Peru. Males are used at a stocking rate of 6% for the entire breeding period of 60 days. Half of the males are used for 1 week and are then rotated the following week with the other half. By alternating the males in this manner, libido and mating activity remain high, and the opportunity for the females to be mated once or more may be maximized. Use of the rotary system in a large alpaca cooperative in Peru (adults and yearlings, n = 1399) resulted in a birth rate increase from 57% to 81%.36
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A
B Fig. 115-7 Unusual right-sided pregnancy in alpacas (approximately 8 to 9 months) with the corpus luteum (arrow) in the left (left image) or right (right image) ovary.
PREGNANCY The duration of gestation in the alpacas of the Huacaya and Suri breeds has been reported as 341 and 345 days, respectively.21 For llamas in the United States, a mean of 344 days (range, 331 to 347) was reported.18 In one study of 79 nulliparous and 61 multiparous llamas in southern Peru in which only two matings were allowed (at an interval of 6 to 8 hours apart), the length of the gestational period (mean ± SD) was 346 ± 8 days (range, 327–357).37 Neither parity of the dam nor sex of the cria was found to influence gestation length. Despite the fact that ovulation occurs from both ovaries with equal frequency, nearly all alpaca and llama fetuses occupy the left uterine horn (as indicated by position of the conceptus and site of umbilical attachment), with rare exceptions (Fig. 115-7). This finding indicates that embryos originating from the right side migrate to the left horn for attachment. The reason for the right-toleft migration, which apparently is unique to Camelidae, is not known. One explanation for this phenomenon implicated a differential luteolytic effect of the left versus the right uterine horn.38 It was concluded that the right horn effects luteolysis through both systemic and local pathways. An interesting difference was found between the uterine vascular system in the llama and the alpaca and that of animals of other farm species.40 This was the presence of a major branch of the right uterine artery that crossed the cranial intercornual area to supply much of the left uterine horn. Thus, the vascular anatomy indicated that much venous blood from the left horn drained to the right side; this finding is compatible with the hypothesis that the left horn can exert luteolytic control over the corpus luteum in the right ovary through a local venoarterial pathway. Whatever the cause of migration of the embryo to the left uterine horn, this may be a unique mechanism by which camelids reduce twins to a single fetus. Multiple ovulations occur in 3% to 10% of alpacas after natural mating and in 9% to 20% after treatment
with gonadotropins, but twins born alive are very rare.41,42 Twin pregnancies are not uncommon in the early stages of gestation but are very seldom observed at late stages or at parturition. Very few cases have been recorded in Peru in alpacas or llamas; a higher rate reported in the United States42 may be a reflection of better nutrition. The role of the corpus luteum during pregnancy in the alpaca and llama has been studied,46 and results indicated that the corpus luteum is necessary for the maintenance of pregnancy throughout gestation in both llamas and alpacas. On the basis of the source of progesterone required to maintain pregnancy, these species may be classified as corpus luteum–dependent, similar to the cow, goat, and sow. The placenta in the alpaca, as in other camelids, is diffuse and epitheliochorial in type. The chorionic epithelium is thrown into unbranched villi or folds, which are closely apposed to corresponding undulations in the endometrial epithelium. Hence, the fetal-maternal interface consists of an intricate interdigitation of microvilli. In late gestation, both chorionic and uterine epithelia are deeply indented by placental capillaries, so that the intercapillary distance may be as little as 2 μm. The distance appears to be less that that found in the epitheliochorial placenta of any other species of domestic ungulates in late gestation and may be one of the several adaptations to pregnancy at high altitudes.43 A unique extrafetal membrane has been described in newborn alpacas, llamas, vicuñas, and guanacos.44,45 The extra membrane encases the entire fetal body and is attached at the mucocutaneous junctions and coronary bands; it appears to be a product of the basal layer of the epidermis.
EMBRYONIC AND FETAL MORTALITY Diverse studies have established that prenatal loss attains considerable levels in all farm animal species and that the bulk of this loss occurs during the early embryonic stages.
Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca In an early study31 more than 80% of the ova recovered 3 days after mating were in the process of dividing, and only 50% of the fertilized ova survived for more than 30 days of gestation. In a later study,47 however, reproductive wastage in a group of alpacas of differing ages and parity was 83% (ova, embryo, and fetus loss). Very few fetal losses were found from 90 days after mating to parturition, and most were late-term abortions. Factors responsible for this high attrition rate are unknown, but nutritional constraints, hormonal imbalance, improper day of mating and mating system, and chromosomal aberrations may be principal causes. These studies were conducted in alpacas living in their natural habitat, affected by a harsh natural environment, deteriorating feed supply caused by overgrazing, and the presence of infectious and parasitic diseases. Specific infections of the reproductive organs, however, have not been identified as a cause of embryonic losses in llamas.7 The overall rate and causes of embryo and fetus loss await more critical evaluation.
PARTURITION AND ITS CONTROL Among 130 alpacas observed giving birth at La Raya Research Station in Cusco, Peru, unassisted labor lasted a mean of 203 ± 129 minutes for primiparous females (n = 34) and 193 ± 122 minutes for multiparous females (n = 96).39 The time course for the three different stages of labor is indicated in Table 115-3. In llamas (n = 95), a mean of 176 minutes has been reported for the three different stages of labor.49 Birth in alpacas and llamas appears to be achieved more easily than in the cow or mare. Camelids in general do not lick their offspring at birth, nor do they engage in placentophagia. More than 90% of births in alpacas and llamas occur between 7 AM and 1 PM. This adaptation gives the cria the best chance to get warm and dry before nightfall, because even in the summer freezing temperatures are common at altitudes higher than 4000 m.6 In studies done in Australia,50 the time of parturition in alpacas has been shown to be under photoperiodic control. Also, alpacas appear to be able to delay birthing for hours or even a day to avoid giving birth during the night or during inclement weather.51 It has been postulated that the fetus
Table 115-3 Duration of Labor Stages in Primiparous versus Multiparous Alpacas DURATION (MEAN ± SD MINUTES) Parity
First Stage
Second Stage
Third Stage
Multiparous (n = 96) Primiparous (n = 34)
87.5 ± 67.2
24.7 ± 16.0
80.7 ± 39.0
101.5 ± 77.6
24.5 ± 12.8
77.0 ± 38.6
Data from Condorena N, Sumar J, Alarcón V: Per yodo de gestacion en llamas (Lama pacos). Turrialba XXXX;42:112–113.
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may determine the day of birth and the mother determines the hour.52 Induction of parturition may be used in farm species to concentrate the birthing season to a confined period. The birthing season in the highlands of Peru lasts about 3.5 months as a result of a prolonged period of mating. In a group of females exposed to males for 60 days, the birthing period lasted 75 days (Sumar, unpublished data). In an early study done in Peru,53 pregnant alpacas within 45 days of parturition were treated with prostaglandin F2α (PGF2α) 0.12 mg, PGF2α 0.25 mg, dexamethasone 10 mg, dexamethasone 10 mg plus estradiol 10 mg, or saline (in control animals). Results showed that both doses of PGF2α significantly shortened the interval to parturition. No undesirable effects were observed during parturition or lactation; however, some excess risk for mortality was found for crias born with a body weight less than 5 kg (normal = 7 kg). The results clearly show the effectiveness of PGF2α for elective induction of parturition. In a more recent study, a prostaglandin analogue, fluprostenol, effectively induced parturition, whereas dexamethasone was associated with fetal death and oxytocin had no effect.54 In another report,55 another prostaglandin analogue, cloprostenol, effectively aborted llamas at up to 7 months of gestation without adverse effects on subsequent fertility (250 μg given intramuscularly, to time at 24 hours interval). Of interest, the interval from treatment to parturition or abortion was 21 hours 29 minutes (range, 19 to 29 hours) in alpacas given fluprostenol, whereas in llamas given cloprostenol the interval was 3 days. It is unknown whether differences are due to species, prostaglandin analogue or dose, or the stage of gestation at the time of treatment.
POSTPARTUM PERIOD Up to the fourth day after parturition, the female alpaca is submissive and will allow herself to be mounted by the male.47 Luteal regression, follicular growth, and uterine involution are not complete, however, and the female will not ovulate; moreover, she is at risk of uterine infection from such early matings. By 10 days post partum, the diameter of the largest follicle is about 8 to 10 mm, the corpus luteum has regressed considerably, and the uterus has involuted substantially (weighing only one fifth of its weight 24 hours after birth). Mating of females within 15 to 20 days after birthing has been recommended to obtain good pregnancy rates, with one offspring per female per year.56 In a study of llamas, pregnancy rates from breeding at 20 or 30 days were threefold higher (61%) than at 10 days post partum (21%).10
References 1. Sato A, Montoya L: Aparato reproductor de la alpaca (Lama pacos). Anatomía macroscópica. IVITA/CICCS, Universidad Nacional Mayor de San Marcos. Revista de Camélidos Sudamericanos 1990;7:23. 2. Bravo PW, Sumar J: Some anatomical parameters of the reproductive tract in alpacas [in Spanish]. Resúmenes de
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21. 22.
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inves, Universidad Nacional Mayor de San Marcos, Lima, Peru. Fowler ME: Medicine and surgery of South American camelids: llama, alpaca, vicuña, guanaco. Ames, IA: Iowa University Press, 1989. Adams GP, Griffin PG, Ginther OJ: In situ morphologic dynamic of ovaries, uterus and cervix in llamas. Biol Reprod 1989;41:551–558. Sumar J: Defectos congenitos y hereditarios en la alpaca. Teratología. Lima, Peru: Grafica Bellido,1989. Sumar J: Reproductive physiology in South American camelids. In Land RB, Robinson DW (eds): Genetics of reproduction in sheep. UK: Butterworths, 1985, pp 81– 95. Sumar J: Studies on reproductive pathology in alpacas. Master’s thesis, Department of Obstetrics and Gynaecology, Veterinary Medicine Faculty, Swedish University of Agrarian Sciences, Uppsala, Sweden, 90 pp. Bravo PW: The postpartum llama: fertility after parturition. Biol Reprod 1994;51:1084–1087. Sumar J, Alarcón V, Huanca T: Pubertad en la llama macho. Proceedings of the XI Panamerican Congress of Veterinary Sciences, Lima, Peru, 1988. Bravo PW, Stabenfeldt GH, Fowler ME, et al: Testes development and testosterone concentration in the llama (Lama glama). Procedings of the12th International Congress on Animal Reproduction, The Hague, The Netherlands, 1992, vol 4, pp 1698–1700. Novoa C, Fernández-Baca S, Sumar J, Leyva V: Pubertad en la alpaca. Rev Inv Pec (IVITA) Universidad Nacional Mayor de San Marcos 1972;1:29–35. Leyva V, Sumar J: Evaluación del peso corporal al empadre sobre la capacidad reproductiva de hembras alpaca de un año de edad. Proceedings of the 4th International Convention on South American Camelids, Corporación Nacional Forestal e Instituto de la Patagonia, Punta Arenas, Chile, Abstract 1, 1981. Bustinza V, Medina G: Crecimiento de alpacas. Memorias del V Cong Int de Sistemas Agropecuarios Andinos, Puno, Peru, Abstract 408, 1986. Montalvo C, Cevallos E, Copaira M: Madurez sexual de la alpaca macho. Estudio histologico del testículo. II Conv Int Sobre Camélidos Sudamericanos, Puno, Peru, 1975. Fernández-Baca S: Manipulation of reproductive functions in male and female New World camelids. Anim Reprod Sci 1993;33:307–327. Franklin WL: Contrasting socioecologies of South America’s wild camelids: the vicuña and the guanaco. In Eisenbery JF, Kleinman DG (eds): Advances in the study of mammalian behaviour. Special publication of the American Society of Mammalogists 1983;7:573–629. Schmidt CR: Breeding season and notes on some other aspects of reproduction in captive camelids. International Zoology Yearbook 1973;13:387–390. Johnson LW: Llama reproduction. In Johnson LW (ed): Llama medicine workshop for veterinarians. Appendix 10b. Colorado State University, Fort Collins, CO, 1988. Fernandez-Baca S, Novoa C, Sumar J: Actividad reproductiva en la alpaca mantenida en separacion del macho. Mem Asoc Latinoam Prod Anim 1972, vol 7, pp 7–18. Sumar J, Franco J, Alarcon V: Niveles de Testosterona circulante en la alpaca (Lama pacos) y llama (Lama glama). Proceedings of the 2nd Jornadas International de Biopatología Andina, Cusco, Peru, 1999. San Martín M, Copaira M, Zúñiga J, et al: Aspects of reproduction in the alpaca. J Reprod Fertil 1968;16:395. Milligan SR: Induced ovulation in mamals. Oxf Rev Reprod Biol 1982;4:1–40.
23. Bravo PW, Sumar J: Laparoscopic examination of the ovarian activity in alpacas. Anim Reprod Sci 1989;21:271. 24. Bravo PW: Studies on ovarian dynamics and response to copulation in the South American camelids Lama glama and Lama pacos. PhD thesis, University of California–Davis, 1990, p 91. 25. Adams GP, Sumar J, Ginther OJ: Effects of lactational and reproductive status on ovarian follicular waves in llamas (Lama glama). J Reprod Fertil 1990;90:535–545. 26. Sumar J, Bravo PW, Foote WC: Sexual receptivity and time of ovulation in alpacas. Small Rumin Res 1993;11:143–150. 27. England BG, Foote WC, Matthews DH, et al: Ovulation and corpus luteum function in the llama (Lama glama). J Endocrinol 1969;45:505–513. 28. Fernandez-Baca S, Sumar J, Novoa C, Leyva V: Relación entre la ubicación del cuerpo luteo y la localizacion del embrión en la alpaca. Rev Invest Pec (IVITA) Universidad Nacional Mayor de San Marcos 1973;2:131–135. 29. Sumar J, Leyva V: Relación entre la ubicación del CL y la localización del embrión en la llama (Lama lama). Anales III Conv Int Sobre Camélidos Sudamericanos, Viedma, Argentina, 1979. 30. Bravo PW, Fowler ME, Stabenfeldt GH, Lasley B: Endocrine responses in the llama to copulation. Theriogenology 1990;334:39–47. 31. Fernández-Baca S: Luteal function and the nature of reproductive failures in alpacas. PhD thesis, Cornell University, Ithaca, NY, 1970, pp 84–100. 32. Adams GP, Sumar J, Ginther OJ: Form and function of the corpus luteum in llamas. Anim Reprod Sci 1991; 24:127–138. 33. Sumar J, Fredriksson G, Alarcon V, et al: Levels of 15-keto13,14-dihydro-PGF2α, progesterone and oestradiol-17β, after induced ovulations in llamas and alpacas. Acta Vet Scand 1988;29:339–346. 34. Fernandez-Baca S, Novoa C: Conducta sexual de la alpaca en empadre a campo. 1968;3:7–20. 35. Fernández-Baca S: Comportamiento sexual de la alpaca macho frente a la renovacion de las hembras. Rev Inv Pec (IVITA) Universidad Nacional Mayor de San Marcos 1972;1:116–128. 36. Novoa C, Sumar J, Franco E: Empadre complementario de alpacas hembras vacías. Proceedings of the 1st International Convention on South American Camelids. Universidad Nacional Técnica del Altiplano, Puno, Peru, Abstract, 1970, pp 144–147. 37. Condorena N, Sumar J, Alarcón V: Per yodo de gestacion en llamas (Lama pacos). Turrialba XXXX••;42:112–113. 38. Fernandez-Baca S, Hansel W, Saatman R, et al: Differential luteolytic effect on right and left uterine horns in the alpaca. Biol Reprod 1979;20:586–595. 39. Sumar J: Algunos aspectos obstétricos de la alpaca. Boletín Técnico No. 2. IVITA, Universidad Nacional Mayor de San Marcos, Convenio CIID-Canada, 1985, 16 pp. 40. Del Campo MR, Del Campo CH, Ginther OJ: Vascular provisions for a local utero-ovarian cross-over pathway in New World camelids. Theriogenology 1996;46:983–991. 41. Sumar J: Gestación gemelar en la alpaca. Rev Inv Pec (IVITA) Universidad Nacional Mayor de San Marcos 1980;5:58–60. 42. Fowler ME: Twinning in llamas. Llamas Int Cam J 1990;35–38. 43. Steven DH, Burton GJ, Sumar J, Nathanielsz PW: Ultrastructural observations on the placenta of the alpaca (Lama pacos). Placenta 1980;1:21–32. 44. Sumar J: Reproduction in llamas and alpacas. Anim Reprod Sci 1996;42:405–415. 45. Merkt H, Boer M, Rath D, Schoon HA: The presence of an additional fetal membrane and its function in
Breeding Soundness Examination of the Male Llama and Alpaca
46.
47.
48.
49.
50.
51.
the newborn guanaco (Lama guanicoe). Theriogenology 1988;30:437–439. Sumar J: Removal of the ovaries or ablation of the corpus luteum and its effect on the maintenance of gestation in the alpaca and llama. Acta Vet Scand Suppl 1983;83:133–141. Bravo PW, Sumar J, Riera SG, Foote WC: Reproductive wastage in female alpaca. In Improving reproductive performance of small ruminants. Utah State University, Logan, UT, 1987, pp 155–159. Sumar J: Algunos aspectos obstétricos de la alpaca. Boletín Técnico No. 2. Universidad Nacional Mayor de San Marcos, Convenio CIID-Canada. Lima, Peru, 1985. Del Castillo M, Aedo R: El parto en la llama (Lama glama). Bach. thesis, Universidad Nacional S Antonio Abad, Cusco, Peru, 1988. p 75. Knight TW, Death AF, Wyeth TK: Photoperiodic control of the time of parturition in alpacas (Lama pacos). Anim Reprod Sci 1995;39:259–265. Sumar J, Smith GW, Mayhua E, Nathanielsz PW: Adrenocortical function in the fetal and new born alpaca. Comp Biochem Physiol 1978;59A:79–84.
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52. Liggins GC: The fetus and birth. In Austin CR, Short RV (eds): Embryonic and fetal development, 2nd ed. Vol 2; Reproduction in mammals. Cambridge, UK: Cambridge University Press, 1983, pp 114–141. 53. Osorio de Valdivia E, Sumar J, Casas J, Ponce J: Inducción y sincronizacion del parto en la alpaca. AnnVII Reunión Asoc Latinoam Prod Anim (ALPA), Panamá, 1979. 54. Bravo WP, Bazab PJ, Troedsson MHT, et al: Induction of parturition in alpacas and subsequent survival of neonates. J Am Vet Med Assoc 1996;209:1760–1762. 55. Smith BB, Timm KI, Reed PJ, Christensen, M: Use of cloprostenol as an abortifacient in the llama (Lama glama). Theriogenology 2000;54:497–505. 56. Sumar J, Novoa C, Fernandez-Baca S: Fisiologia reproductiva postparto en la alpaca. Rev Inv Pec (IVITA), Universidad Nacional S Maecos 1972;1:21–27. 57. Lichtenwalner AB, Woods GL, Weber JA: Male llama choice between receptive and nonreceptive females. Appl Anim Behav Sci 1998;59:349–356.
116
Breeding Soundness Examination of the Male Llama and Alpaca P. WALTER BRAVO
B
reeding soundness examination (BSE) is common in several livestock species and is an excellent tool that can be used to discard males that do not fit selection criteria. In llamas and alpacas, this procedure is still under development; nonetheless, there is tangible evidence that semen evaluation may be done without much elaboration or the use of sophisticated instrumentation. This section does not deal with different traits that are used to select a sire, commonly known among llama and alpaca breeders as a “padre.” Other phenotypic criteria are beyond the scope of this section and the reader is counseled to look for further literature. Rather, this section is
devoted completely to the examination of the external genitalia and their physiology, including semen evaluation and assessing circulating concentrations of testosterone. Some general criteria for identification are also considered because most BSEs will be used for future sires.
IDENTIFICATION Most males considered for BSE should have an accurate and lasting identification. Ear tags, collars, and recently, microchips are used to identify animals. Different brands of microchips, ear tags, and collars are available on the
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Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca JULIO SUMAR and GREGG P. ADAMS
P
resent-day alpacas and llamas developed from a common feral ancestry in South America during the last millennium. Many aspects of their reproductive pattern are similar but extrapolation from one species to another must be done with caution. Although differences in the reproductive biology have not been documented, few critical studies have been conducted to compare the various species of camelids. Breeding experiences and research with llamas and alpacas under different latitudes and lower altitudes such as those being carried out in Australia, Canada, and the United States may soon contribute to a better understanding of the biology of reproduction in llamas and alpacas.
confirmation of ovulation and is a rapid method of “progesterone testing.” The oviducts are long and tortuous and end in an open bursa that normally covers the ovary. The tip of the uterine horns in both domestic species is blunt and
Table 115-1 Dimensions of the Reproductive Organs of Female Llamas and Alpacas VALUE (cm): MEAN ± SD Organ Dimension
GROSS AND ULTRASONOGRAPHIC ANATOMY OF THE FEMALE The gross appearance of the female reproductive organs in the alpaca is illustrated in Figures 115-1 and 115-2. The dimensions of alpaca and llama reproductive tracts are compared in Table 115-1.1–3 The ultrasound appearance of the ovary is illustrated in Figure 115-3.4 The ovum itself is too small to be detected by present-day ultrasound instruments, but antral follicles as small as 1 to 2 mm in diameter can be detected. Several fluid-filled follicles (e.g., from four to eight), with or without a corpus luteum, may be detected in the ovaries at any given time. On ultrasound examination, the appearance of the llama or alpaca ovary is more similar to that of the cow than of the mare. The ovary and ovarian structures are, however, smaller than in cows (e.g., ovulatory-sized follicle, 10 mm versus 16 mm in diameter, respectively; mature corpus luteum, 13 mm versus 28 mm, respectively). As in the cow but not the mare, ovarian follicles are arranged in a peripheral cortex, and ovulation can take place at any spot on the surface of the ovary. The corpus luteum and large follicles protrude distinctly from the surface of the ovary in llamas and are readily palpable. On ultrasonography, corpora lutea are seen to have a very characteristic spherical shape and are hypoechogenic (dark gray) relative to the surrounding tissues. A horizontal echogenic (light gray) area traversing the center of the corpus luteum also is a distinctive ultrasonographic feature. The capability to ultrasonographically recognize and monitor the development of the corpus luteum is fortuitous because it allows
Length of labia Vagina (hymen to cervix) Length Diameter Cervix Length Diameter Number of rings Uterine body Length Diameter Uterine horns Length Diameter Oviduct length Right ovary Length Depth Width Left ovary Length Depth Width
Alpaca
Llama
2.5
5.0
13.4 ± 2.0 3.4 ± 0.7
15–21 5
2 — 2–3
2–5 2–4 2–3
3.0 ± 0.7 —
3–5 3–5
7.9 ± 1.3 — 20.4 ± 4.2
8.5–15 2.5–4 10.5–18.3
1.6 ± 0.3 1.1 ± 0.2 1.1 ± 0.2
1.3–2.5 1.4–2.0 0.6–1.0
1.6 ± 0.3 1.1 ± 0.2 1.1 ± 0.2
1.5–2.5 1.5–2.5 0.5–1.0
SD, standard deviation. Data from Sato A, Montoya L: Aparato reproductor de la alpaca (Lama pacos). Anatomía macroscópica. IVITA/CICCS, Universidad Nacional Mayor de San Marcos. Revista de Camélidos Sudamericanos 1990;7:23; Bravo PW, Sumar J: Some anatomical parameters of the reproductive tract in alpacas [in Spanish]. Resúmenes de inves, Universidad Nacional Mayor de San Marcos, Lima, Peru; Fowler ME: Medicine and surgery of South American camelids: llama, alpaca, vicuña, guanaco. Ames, IA: Iowa University Press, 1989; and Sumar J: Studies on reproductive pathology in alpacas. Master’s thesis, Department of Obstetrics and Gynaecology, Veterinary Medicine Faculty, Swedish University of Agrarian Sciences, Uppsala, Sweden, 90 pp.
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A
B
D
C
E Fig. 115-1 Gross appearance of alpaca ovaries. A, Cross section showing a corpus luteum (CL) and numerous follicles (F). B, Recently ovulated follicle with an ovulatory papilla (arrow). C, Mature 12-mm follicle. D, Cross section of a corpus hemorrhagicum. E, Corpus luteum and several follicles in the ovaries of a pregnant alpaca (at 2 months of gestation).
Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca
A
857
B Fig. 115-2 Reproductive organs of the alpaca and llama. A, Craniolateral view of the suspended reproductive tract of an alpaca at slaughter showing the left and right uterine horns (lh, rh) suspended by the broad ligament (bl), the left and right ovaries (lo, ro), and the left oviduct (black arrow). B, Dorsal view of the excised tract of a llama. The uterine horns are relatively short, not tapered, and come to a blunt uterotubal junction, unlike in cows or ewes, in which the uterine horns are long and taper toward the uterotubal junction.
Fig. 115-3 Ultrasound images of the llama ovary, uterus, and cervix. Morphologic features are characteristic of the luteal phase:, a follicle and a corpus luteum in the ovary, curled uterine horn, and distinct cervical folds. The scale at the top is in 1-cm increments, and the images are in a sagittal plane with the cranial direction to the left.4
rounded, unlike in other ruminants, in which it tapers slowly toward the uterotubal junction. Accordingly, the oviduct of alpacas and llamas opens into the uterine horns through a small, raised papilla, which acts as a welldefined sphincter. Even under great pressure it is not possible to flush liquids from the uterus into the oviduct, but flushing in the opposite direction is possible. As in other domestic species, the uterus of the alpaca and llama is bicornuate, but the left uterine horn is slightly longer than the right (7.9 ± 1.3 cm versus 7.4 ± 0.9 cm), even in the nullipara. In situ, the uterine horns curl ventrally and caudally, and the degree of curl is maximal during the luteal phase (progesterone dominance) and minimal during the follicular phase (estrogen dominance)4 (Fig. 115-4). The degree of uterine horn curl is much less than in other ruminants (e.g., sheep, goats, cattle), and in the excised tract, the uterine horns shrink and may not appear curled at all, but rather appear Y-shaped. The echotexture (grain
of the ultrasound image) of the uterus changes from homogeneous light gray (smooth and uniform) during the luteal phase and early pregnancy to heterogeneous and increasingly dark during the follicular phase (see Fig. 115-4). Estrogen causes the reproductive tissues to imbibe water and, since fluid is nonechogenic, the uterus becomes relatively hypoechogenic during the follicular phase. A similar pattern has been reported in cows.5 In nonpregnant llamas, the body of the uterus is short (2 to 3 cm) and not clearly differentiated from the base of either horn on ultrasonography. Uterine tone, based on digital palpation, is maximal during the follicular phase and minimal during the luteal phase and early pregnancy, as in cattle. The uterus is remarkably turgid during the follicular phase, and longitudinal grooves can be palpated along its upper surface. Thus, both the homogeneous dark echotexture and extreme turgidity of the uterus indicate a profound accumulation of interstitial fluid during follicular dominance. The tubular genitalia are suspended
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Fig. 115-4 Characteristic differences in the reproductive organs of alpacas and llamas during the follicular phase (receptive) versus the luteal phase (nonreceptive).4
from the lateral pelvic and abdominal walls by the broad ligament; the ligament attaches along the ventral aspect of the uterus such that the uterine body and horns are readily palpable per rectum. The cervix has two or three irregular annular or spiral folds. On ultrasonography, the cervical folds appear as transverse echogenic bands and are especially prominent during the luteal phase and pregnancy (see Fig. 115-4). Presumably, edema of the cervical folds during the follicular phase is responsible for the dark echotexture and indistinct appearance on the sonogram characteristic of this phase. The vagina is surprisingly long and commonly exceeds 20 cm.
ANATOMY OF THE MALE In the adult alpaca, the testes are found in a nonpendulous scrotum in the perineal region 5 to 9 cm ventral to the anus.1,6 The testes are small and elliptical and positioned so that the long axis is oriented vertically or in an oblique dorsocaudal orientation. Normally, both testes are of the same size and of a firm consistency, with free movement inside the scrotum. The head, body, and tail of the epididymis are small and firmly connected to the
testes. The average weight of one fully developed alpaca testis is approximately 17 g (range, 13 to 28 g), measuring between 4 and 5 cm in length and 2.5 to 3.0 cm in depth.7 Considerable variation, however, has been found in testicle size and liveweight in alpacas. In one study, male llamas that reached the age of 2 years (83 kg of body weight) had testes weighing about 12 g, with dimensions of 3.5 × 2.2 cm and a volume of 13 cc. At the age of 5 years, llama testes weighed about 24 g, with dimensions of 5.0 cm × 2.7 cm and a volume of 22 cc.9 In another study,10 body weight and testicular index increased linearly from birth to 24 months of age, with a subsequent slower increase to adulthood. A positive relationship was found between age and testicular index (R2 = 0.88). The deferent duct (ductus deferens) is very thin (2 mm) at its beginning and thickens (3 mm) when it reaches the abdominal cavity and ends near the bladder, forming what in other species is the ampullae.14 The prostate consists of a clearly defined body at the neck of the bladder, and a disseminate part along the pelvic urethra. The prostate body measures approximately 3 cm × 2 cm and is easily palpable per rectum in the adult. The bulbourethral glands are oval and are located on either side of the urethra at the pelvic outlet. Camelids have no vesicular glands.
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859
Fig. 115-5 Penis of alpacas show-
A
B
C
ing progressive stages of separation of the free end of the penis from its preputial adhesions. A, Complete adhesion with only the tip of the cartilaginous process showing; B, the beginning of separation; C, persistent adhesion of the tip of the penis, and D, a penis completely free of its preputial adhesions.
D
The penis is fibroelastic, with a small (approximately 1 cm across) cartilaginous process that has a hooklike curve at its tip (Fig. 115-5). The length of the nonerect penis in the alpaca is 26 cm, and the sigmoid flexure is prescrotal.6 The prepuce is small, located approximately 15 cm caudal to the umbilicus, and has a triangular opening that is oriented caudally.1 During urination, camelids direct the stream of urine backward between the hind legs. The protractor preputial muscle pulls the prepuce forward before mating, changing the direction of the preputial opening and thus allowing for the penis to be directed forward.
PUBERTY Young female alpacas of 12 to 13 months of age display behavioral estrus similar to that in adult alpacas.11 A majority of females display sexual receptivity at 12 months of age even though ovarian activity begins at
10 months of age, with the presence of follicles of 5 mm or more in diameter. In a study carried out in southern Peru using 280 yearling alpaca females,12 a highly significant relationship (P < 0.001) was found between body weight at mating and subsequent birth rates. For each kilogram increase in body weight up to 33 kg, a 5% increase in natality was observed; for increases in excess of 33 kg, the percentage of nonpregnant females was relatively independent of body weight. In traditional Peruvian production systems, only about 50% of yearling alpacas reach a body weight of 33 kg at mating time (January through March). Therefore, breeding age is postponed to 2 years of age and often to 3 years of age in llamas. It also has been shown that with better nutrition after weaning (7 to 8 months of age), nearly 100% of yearling alpacas can reach 33 kg body weight.13 In males, the penis is completely adherent to the prepuce at birth. Under the influence of testosterone, the adhesions disappear gradually as the male matures.6,7
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At 1 year of age the males show sexual interest in the females, but only about 8% of alpaca males have complete liberation of penis-prepuce adhesions and are capable of copulating. At 2 years of age, approximately 70% of the males are free of adhesions, and 100% are free at 3 years of age (see Fig. 115-5). Puberty, based on penisprepuce detachment, is attained at an average of 21 months of age (range, 9 to 31 months) in llamas, at a body weight of 70 kg (range, 48 to 92 kg).10 Also, testosterone concentration starts to increase exponentially at 21 months of age (to 300 pg/mL), reaching a plateau at 30 months of age (650 pg/ml).9,10 From 2 to 11 months, the testes grow slowly (infantile stage), with a sequential increase of noncanalized sex cords and undifferentiated Leydig cells.14 At an age of about 12 months, the sex cords start to develop a distinct lumen containing Sertoli cells and spermatogonia. The first spermatozoa appear at about 18 months of age, with half of the animals having spermatozoa in the caput epididymidis. From 18 months, the number of Leydig cells increases considerably, and by 20 to 24 months, the diameter of the tubules is greatly increased, with presence of considerable numbers of spermatozoa in the caput epididymidis. Beginning at 3 years of age, normal alpacas have spermatozoa in the epididymis. Spermatogenesis is initiated in some alpacas as early as 16 months and in others as late as 26 months.59 The general practice in Peru is to start using the males for breeding at 3 years of age.
SEASONALITY Studies with alpacas and llamas in their natural habitat in the highlands of Peru showed that sexual activity is seasonal and lasts from December to March (summer months). These are the warmest months of the year, with sufficient rain and abundant green forage.15 In farms on which males and females are together all year, the birthing and breeding times lie within this time range. This marked seasonality of reproduction also is characteristic of the wild species—the vicuña and guanaco.16 Observations in different zoological parks of the world, however, indicate that llamas are year-round breeders.17 In North America, where llamas are kept under good nutritional conditions year-round and copulation is allowed only on an individual basis, they are considered nonseasonal breeders. An analysis of llama birthing records from the Rocky Mountains area of the United States revealed that births occurred during all months of the year, but with a preponderance (73%) between June and December.18 In another study, ovulation, fertilization, and embryo survival rates were not affected by the season of the year.19 Males show much less seasonal variation in libido and testicular function. The male alpaca is capable of producing fertile ejaculates year-round, but as in other domestic species, semen quality and libido are affected by season and availability of feed. Under North American conditions of management, no seasonal effect on testosterone values of adult male llamas has been found.10 In a study of male alpacas and llamas in Peru, plasma testosterone concentrations were markedly elevated during spring and summer (the breeding season),
Table 115-2 Seasonal Variation in Peripheral Testosterone Level in Male Alpacas and Llamas TESTOSTERONE CONCENTRATION (pg/ml): MEAN ± SEM Season: Month Spring: March Summer: June Autumn: September Winter: December
Alpacas
Llamas
1142 ± 108 992 ± 388 877 ± 91 2445 ± 694
208 ± 52 37 ± 14.9 291 ± 74 362 ± 73
SEM, standard error of the mean. Data from Lichtenwalner AB, Woods GL, Weber JA: Male llama choice between receptive and nonreceptive females. Appl Anim Behav Sci 1998;59:349–356.
whereas lower levels occurred in autumn and winter20 (Table 115-2).
PATTERN OF OVARIAN EVENTS Because copulation is a necessary prelude to ovulation, alpacas and llamas have been classified as reflex ovulators or induced ovulators, as opposed to spontaneous ovulators.21,22 Female alpacas and llamas do not have estrous cycles like those in other species of large domestic animal; estrus and ovulation are not manifested in a repetitive cycle. Highlights of ovarian function are presented here, but a more detailed account is found in Chapter 118. Based on laparoscopic examination of the ovaries of alpacas (n = 20)23 and llamas (n = 12),24 it was found that growth, maintenance, and regression of a follicle each required an average of 4 days (total, 12 days; range, 9 to 17 days). In a study of 74 llamas kept in their natural habitat in South America and examined daily by transrectal ultrasonography,25 successive dominant follicles emerged at intervals of 19.8 ± 0.7 days in unmated and vasectomy-mated llamas and 14.8 ± 0.6 days in pregnant llamas. The minimum time to ovulation was estimated to be 26 hours after natural mating and 24 hours after treatment with intramuscular human chorionic gonadotropin (hCG) at a dose of 500 to 700 IU.21 Using an ultrasonographic technique in llamas, ovulation was detected, on average, 2 days (range, 1 to 3 days) after a single mating.4,25 Single service by an intact or vasectomized male resulted in an ovulation rate of 77% to 82%, and an increase in the number of services by intact males to three within a period of 24 hours did not significantly affect ovulation rate.15 In females allowed a single mating, 50% ovulated between 26 and 30 hours, 24% ovulated between 30 and 72 hours, and 26% failed to ovulate after mating.26 Forty percent of the animals that failed to ovulate were yearlings, and 15% were adults. Some evidence indicates that females can ovulate without coital stimulation or exogenous hormones, especially when initially isolated from and then reintroduced
Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca to a male. The rate of spontaneous ovulation has been reported to be approximately 5% in alpacas.6,15 Spontaneous ovulation was detected in 3 of 20 (15%) llamas by palpation in one study,27 and in 3 of 34 (9%) llamas by ultrasonography in two other studies.4,25 Laterality of ovulation (from either the left or the right ovary), as indicated by the presence of a corpus luteum of pregnancy, has been reported in several studies.6,24,26,28,29 On examinations of the genital organs of 928 pregnant alpacas, no differences were found in the ovulatory rate between ovaries. A corpus luteum was detected in the right ovary in 51% of the alpacas, in the left in 47%, and in both ovaries in 2%.28 In the llama (n = 110), a corpus luteum was detected in the right ovary in 54% of females, in the left ovary in 44%, and in both ovaries in 1%.29 Luteal function after sterile and fertile matings has been studied in llamas by several investigators.6,25,27,28,30 In nonpregnant alpacas, the corpus luteum underwent rapid development after ovulation, reached maximum size and secretory activity at 8 to 9 days after mating, and declined sharply in both size and secretory activity by 12 days after mating.31 Similar characteristics were observed in nonpregnant llamas (i.e., mated to vasectomized males) evaluated by ultrasonography.32 Although prolonged luteal phases have been anecdotally reported in association with embryonic loss, spontaneous pseudopregnancy (prolonged luteal phase unassociated with embryonic loss) has been wrongly inferred in llamas.21 A prolonged luteal phase was not observed in any sterile-mated (nonpregnant) alpacas or llamas.25,27,31,32 In pregnant animals, the corpus luteum reaches maximal diameter at 22 days after mating and is maintained throughout gestation.32,33
SEXUAL RECEPTIVITY AND MATING BEHAVIOR In the absence of copulatory stimulation, female alpacas display periods of sexual receptivity of up to 36 days, with short periods of nonreceptivity that may last 48 hours.21 Considerable variability in display of overt receptivity is apparent between individual animals, regardless of parity. The variability in sexual receptivity may be attributable primarily to the degree of follicle maturity at any given stage of the follicular phase; however, no documentation is available in this regard. The receptive female will assume the prone position (ventral recumbency) after a short period of pursuit by the male, or she may approach a male that is copulating with another female and adopt the prone position21 (Fig. 115-6). Some receptive females may occasionally display mounting behavior with other females of the herd, although such behavior is much less common than in cattle. If the female is nonreceptive, rejection is shown by running away and spitting at the male. Males will attempt to mount receptive or nonreceptive females; their initial approach is indiscriminate. In a study of sexual behavior in llamas, the male attempted to mount eight of nine females a total of 60 times during a 12-hour period.20 Each of the eight females was mounted an average of four times, for an average of 5 minutes per mount; mounting was attempted irrespective of the receptivity of the female. Normally, only receptive females will adopt the
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Fig. 115-6 A pair of copulating alpacas in a prone position, surrounded by six females also in the prone position, typical of a display of sexual receptivity.
prone position, but in some instances, aggressive males can force nonreceptive females to adopt the prone position. During the very short courting phase and during mating, the male makes blowing, grunting, nasal sounds. Copulation takes place in a recumbent position, with the male mounted above and just behind the female. The female assumes a very passive attitude during copulation and, in some instances when copulation is prolonged, will appear to tire and may assume lateral recumbency. Compared with other domestic species, coitus is remarkably prolonged in alpacas and llamas (10 to 50 minutes).6 After a certain amount of time has elapsed, the continuous association of males and females somehow inhibits the sexual activity of the males, a situation that may prevent mating of females returning to estrus after a sterile mating or early embryonic death.
MATING SYSTEMS Observation of the sexual activity in the open field, when males and females are joined, at the beginning of the sexual season, showed that mating activity was particularly intense during the first week of the breeding season.34 Greater than 70% of 262 females were recorded as having been mated at least once during this short period. But sexual activity decreased thereafter, reaching a frequency of zero in some instances. After different males were introduced and the original males were removed, however, sexual activity was reactivated and reached a level comparable to that of the first week.35 Based on these observations, a breeding system named the alternating or rotary system was developed.36 This system works well in the large herds commonly found in southern Peru. Males are used at a stocking rate of 6% for the entire breeding period of 60 days. Half of the males are used for 1 week and are then rotated the following week with the other half. By alternating the males in this manner, libido and mating activity remain high, and the opportunity for the females to be mated once or more may be maximized. Use of the rotary system in a large alpaca cooperative in Peru (adults and yearlings, n = 1399) resulted in a birth rate increase from 57% to 81%.36
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CHAPTER 115
A
B Fig. 115-7 Unusual right-sided pregnancy in alpacas (approximately 8 to 9 months) with the corpus luteum (arrow) in the left (left image) or right (right image) ovary.
PREGNANCY The duration of gestation in the alpacas of the Huacaya and Suri breeds has been reported as 341 and 345 days, respectively.21 For llamas in the United States, a mean of 344 days (range, 331 to 347) was reported.18 In one study of 79 nulliparous and 61 multiparous llamas in southern Peru in which only two matings were allowed (at an interval of 6 to 8 hours apart), the length of the gestational period (mean ± SD) was 346 ± 8 days (range, 327–357).37 Neither parity of the dam nor sex of the cria was found to influence gestation length. Despite the fact that ovulation occurs from both ovaries with equal frequency, nearly all alpaca and llama fetuses occupy the left uterine horn (as indicated by position of the conceptus and site of umbilical attachment), with rare exceptions (Fig. 115-7). This finding indicates that embryos originating from the right side migrate to the left horn for attachment. The reason for the right-toleft migration, which apparently is unique to Camelidae, is not known. One explanation for this phenomenon implicated a differential luteolytic effect of the left versus the right uterine horn.38 It was concluded that the right horn effects luteolysis through both systemic and local pathways. An interesting difference was found between the uterine vascular system in the llama and the alpaca and that of animals of other farm species.40 This was the presence of a major branch of the right uterine artery that crossed the cranial intercornual area to supply much of the left uterine horn. Thus, the vascular anatomy indicated that much venous blood from the left horn drained to the right side; this finding is compatible with the hypothesis that the left horn can exert luteolytic control over the corpus luteum in the right ovary through a local venoarterial pathway. Whatever the cause of migration of the embryo to the left uterine horn, this may be a unique mechanism by which camelids reduce twins to a single fetus. Multiple ovulations occur in 3% to 10% of alpacas after natural mating and in 9% to 20% after treatment
with gonadotropins, but twins born alive are very rare.41,42 Twin pregnancies are not uncommon in the early stages of gestation but are very seldom observed at late stages or at parturition. Very few cases have been recorded in Peru in alpacas or llamas; a higher rate reported in the United States42 may be a reflection of better nutrition. The role of the corpus luteum during pregnancy in the alpaca and llama has been studied,46 and results indicated that the corpus luteum is necessary for the maintenance of pregnancy throughout gestation in both llamas and alpacas. On the basis of the source of progesterone required to maintain pregnancy, these species may be classified as corpus luteum–dependent, similar to the cow, goat, and sow. The placenta in the alpaca, as in other camelids, is diffuse and epitheliochorial in type. The chorionic epithelium is thrown into unbranched villi or folds, which are closely apposed to corresponding undulations in the endometrial epithelium. Hence, the fetal-maternal interface consists of an intricate interdigitation of microvilli. In late gestation, both chorionic and uterine epithelia are deeply indented by placental capillaries, so that the intercapillary distance may be as little as 2 μm. The distance appears to be less that that found in the epitheliochorial placenta of any other species of domestic ungulates in late gestation and may be one of the several adaptations to pregnancy at high altitudes.43 A unique extrafetal membrane has been described in newborn alpacas, llamas, vicuñas, and guanacos.44,45 The extra membrane encases the entire fetal body and is attached at the mucocutaneous junctions and coronary bands; it appears to be a product of the basal layer of the epidermis.
EMBRYONIC AND FETAL MORTALITY Diverse studies have established that prenatal loss attains considerable levels in all farm animal species and that the bulk of this loss occurs during the early embryonic stages.
Reproductive Anatomy and Life Cycle of the Male and Female Llama and Alpaca In an early study31 more than 80% of the ova recovered 3 days after mating were in the process of dividing, and only 50% of the fertilized ova survived for more than 30 days of gestation. In a later study,47 however, reproductive wastage in a group of alpacas of differing ages and parity was 83% (ova, embryo, and fetus loss). Very few fetal losses were found from 90 days after mating to parturition, and most were late-term abortions. Factors responsible for this high attrition rate are unknown, but nutritional constraints, hormonal imbalance, improper day of mating and mating system, and chromosomal aberrations may be principal causes. These studies were conducted in alpacas living in their natural habitat, affected by a harsh natural environment, deteriorating feed supply caused by overgrazing, and the presence of infectious and parasitic diseases. Specific infections of the reproductive organs, however, have not been identified as a cause of embryonic losses in llamas.7 The overall rate and causes of embryo and fetus loss await more critical evaluation.
PARTURITION AND ITS CONTROL Among 130 alpacas observed giving birth at La Raya Research Station in Cusco, Peru, unassisted labor lasted a mean of 203 ± 129 minutes for primiparous females (n = 34) and 193 ± 122 minutes for multiparous females (n = 96).39 The time course for the three different stages of labor is indicated in Table 115-3. In llamas (n = 95), a mean of 176 minutes has been reported for the three different stages of labor.49 Birth in alpacas and llamas appears to be achieved more easily than in the cow or mare. Camelids in general do not lick their offspring at birth, nor do they engage in placentophagia. More than 90% of births in alpacas and llamas occur between 7 AM and 1 PM. This adaptation gives the cria the best chance to get warm and dry before nightfall, because even in the summer freezing temperatures are common at altitudes higher than 4000 m.6 In studies done in Australia,50 the time of parturition in alpacas has been shown to be under photoperiodic control. Also, alpacas appear to be able to delay birthing for hours or even a day to avoid giving birth during the night or during inclement weather.51 It has been postulated that the fetus
Table 115-3 Duration of Labor Stages in Primiparous versus Multiparous Alpacas DURATION (MEAN ± SD MINUTES) Parity
First Stage
Second Stage
Third Stage
Multiparous (n = 96) Primiparous (n = 34)
87.5 ± 67.2
24.7 ± 16.0
80.7 ± 39.0
101.5 ± 77.6
24.5 ± 12.8
77.0 ± 38.6
Data from Condorena N, Sumar J, Alarcón V: Per yodo de gestacion en llamas (Lama pacos). Turrialba XXXX;42:112–113.
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may determine the day of birth and the mother determines the hour.52 Induction of parturition may be used in farm species to concentrate the birthing season to a confined period. The birthing season in the highlands of Peru lasts about 3.5 months as a result of a prolonged period of mating. In a group of females exposed to males for 60 days, the birthing period lasted 75 days (Sumar, unpublished data). In an early study done in Peru,53 pregnant alpacas within 45 days of parturition were treated with prostaglandin F2α (PGF2α) 0.12 mg, PGF2α 0.25 mg, dexamethasone 10 mg, dexamethasone 10 mg plus estradiol 10 mg, or saline (in control animals). Results showed that both doses of PGF2α significantly shortened the interval to parturition. No undesirable effects were observed during parturition or lactation; however, some excess risk for mortality was found for crias born with a body weight less than 5 kg (normal = 7 kg). The results clearly show the effectiveness of PGF2α for elective induction of parturition. In a more recent study, a prostaglandin analogue, fluprostenol, effectively induced parturition, whereas dexamethasone was associated with fetal death and oxytocin had no effect.54 In another report,55 another prostaglandin analogue, cloprostenol, effectively aborted llamas at up to 7 months of gestation without adverse effects on subsequent fertility (250 μg given intramuscularly, to time at 24 hours interval). Of interest, the interval from treatment to parturition or abortion was 21 hours 29 minutes (range, 19 to 29 hours) in alpacas given fluprostenol, whereas in llamas given cloprostenol the interval was 3 days. It is unknown whether differences are due to species, prostaglandin analogue or dose, or the stage of gestation at the time of treatment.
POSTPARTUM PERIOD Up to the fourth day after parturition, the female alpaca is submissive and will allow herself to be mounted by the male.47 Luteal regression, follicular growth, and uterine involution are not complete, however, and the female will not ovulate; moreover, she is at risk of uterine infection from such early matings. By 10 days post partum, the diameter of the largest follicle is about 8 to 10 mm, the corpus luteum has regressed considerably, and the uterus has involuted substantially (weighing only one fifth of its weight 24 hours after birth). Mating of females within 15 to 20 days after birthing has been recommended to obtain good pregnancy rates, with one offspring per female per year.56 In a study of llamas, pregnancy rates from breeding at 20 or 30 days were threefold higher (61%) than at 10 days post partum (21%).10
References 1. Sato A, Montoya L: Aparato reproductor de la alpaca (Lama pacos). Anatomía macroscópica. IVITA/CICCS, Universidad Nacional Mayor de San Marcos. Revista de Camélidos Sudamericanos 1990;7:23. 2. Bravo PW, Sumar J: Some anatomical parameters of the reproductive tract in alpacas [in Spanish]. Resúmenes de
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inves, Universidad Nacional Mayor de San Marcos, Lima, Peru. Fowler ME: Medicine and surgery of South American camelids: llama, alpaca, vicuña, guanaco. Ames, IA: Iowa University Press, 1989. Adams GP, Griffin PG, Ginther OJ: In situ morphologic dynamic of ovaries, uterus and cervix in llamas. Biol Reprod 1989;41:551–558. Sumar J: Defectos congenitos y hereditarios en la alpaca. Teratología. Lima, Peru: Grafica Bellido,1989. Sumar J: Reproductive physiology in South American camelids. In Land RB, Robinson DW (eds): Genetics of reproduction in sheep. UK: Butterworths, 1985, pp 81– 95. Sumar J: Studies on reproductive pathology in alpacas. Master’s thesis, Department of Obstetrics and Gynaecology, Veterinary Medicine Faculty, Swedish University of Agrarian Sciences, Uppsala, Sweden, 90 pp. Bravo PW: The postpartum llama: fertility after parturition. Biol Reprod 1994;51:1084–1087. Sumar J, Alarcón V, Huanca T: Pubertad en la llama macho. Proceedings of the XI Panamerican Congress of Veterinary Sciences, Lima, Peru, 1988. Bravo PW, Stabenfeldt GH, Fowler ME, et al: Testes development and testosterone concentration in the llama (Lama glama). Procedings of the12th International Congress on Animal Reproduction, The Hague, The Netherlands, 1992, vol 4, pp 1698–1700. Novoa C, Fernández-Baca S, Sumar J, Leyva V: Pubertad en la alpaca. Rev Inv Pec (IVITA) Universidad Nacional Mayor de San Marcos 1972;1:29–35. Leyva V, Sumar J: Evaluación del peso corporal al empadre sobre la capacidad reproductiva de hembras alpaca de un año de edad. Proceedings of the 4th International Convention on South American Camelids, Corporación Nacional Forestal e Instituto de la Patagonia, Punta Arenas, Chile, Abstract 1, 1981. Bustinza V, Medina G: Crecimiento de alpacas. Memorias del V Cong Int de Sistemas Agropecuarios Andinos, Puno, Peru, Abstract 408, 1986. Montalvo C, Cevallos E, Copaira M: Madurez sexual de la alpaca macho. Estudio histologico del testículo. II Conv Int Sobre Camélidos Sudamericanos, Puno, Peru, 1975. Fernández-Baca S: Manipulation of reproductive functions in male and female New World camelids. Anim Reprod Sci 1993;33:307–327. Franklin WL: Contrasting socioecologies of South America’s wild camelids: the vicuña and the guanaco. In Eisenbery JF, Kleinman DG (eds): Advances in the study of mammalian behaviour. Special publication of the American Society of Mammalogists 1983;7:573–629. Schmidt CR: Breeding season and notes on some other aspects of reproduction in captive camelids. International Zoology Yearbook 1973;13:387–390. Johnson LW: Llama reproduction. In Johnson LW (ed): Llama medicine workshop for veterinarians. Appendix 10b. Colorado State University, Fort Collins, CO, 1988. Fernandez-Baca S, Novoa C, Sumar J: Actividad reproductiva en la alpaca mantenida en separacion del macho. Mem Asoc Latinoam Prod Anim 1972, vol 7, pp 7–18. Sumar J, Franco J, Alarcon V: Niveles de Testosterona circulante en la alpaca (Lama pacos) y llama (Lama glama). Proceedings of the 2nd Jornadas International de Biopatología Andina, Cusco, Peru, 1999. San Martín M, Copaira M, Zúñiga J, et al: Aspects of reproduction in the alpaca. J Reprod Fertil 1968;16:395. Milligan SR: Induced ovulation in mamals. Oxf Rev Reprod Biol 1982;4:1–40.
23. Bravo PW, Sumar J: Laparoscopic examination of the ovarian activity in alpacas. Anim Reprod Sci 1989;21:271. 24. Bravo PW: Studies on ovarian dynamics and response to copulation in the South American camelids Lama glama and Lama pacos. PhD thesis, University of California–Davis, 1990, p 91. 25. Adams GP, Sumar J, Ginther OJ: Effects of lactational and reproductive status on ovarian follicular waves in llamas (Lama glama). J Reprod Fertil 1990;90:535–545. 26. Sumar J, Bravo PW, Foote WC: Sexual receptivity and time of ovulation in alpacas. Small Rumin Res 1993;11:143–150. 27. England BG, Foote WC, Matthews DH, et al: Ovulation and corpus luteum function in the llama (Lama glama). J Endocrinol 1969;45:505–513. 28. Fernandez-Baca S, Sumar J, Novoa C, Leyva V: Relación entre la ubicación del cuerpo luteo y la localizacion del embrión en la alpaca. Rev Invest Pec (IVITA) Universidad Nacional Mayor de San Marcos 1973;2:131–135. 29. Sumar J, Leyva V: Relación entre la ubicación del CL y la localización del embrión en la llama (Lama lama). Anales III Conv Int Sobre Camélidos Sudamericanos, Viedma, Argentina, 1979. 30. Bravo PW, Fowler ME, Stabenfeldt GH, Lasley B: Endocrine responses in the llama to copulation. Theriogenology 1990;334:39–47. 31. Fernández-Baca S: Luteal function and the nature of reproductive failures in alpacas. PhD thesis, Cornell University, Ithaca, NY, 1970, pp 84–100. 32. Adams GP, Sumar J, Ginther OJ: Form and function of the corpus luteum in llamas. Anim Reprod Sci 1991; 24:127–138. 33. Sumar J, Fredriksson G, Alarcon V, et al: Levels of 15-keto13,14-dihydro-PGF2α, progesterone and oestradiol-17β, after induced ovulations in llamas and alpacas. Acta Vet Scand 1988;29:339–346. 34. Fernandez-Baca S, Novoa C: Conducta sexual de la alpaca en empadre a campo. 1968;3:7–20. 35. Fernández-Baca S: Comportamiento sexual de la alpaca macho frente a la renovacion de las hembras. Rev Inv Pec (IVITA) Universidad Nacional Mayor de San Marcos 1972;1:116–128. 36. Novoa C, Sumar J, Franco E: Empadre complementario de alpacas hembras vacías. Proceedings of the 1st International Convention on South American Camelids. Universidad Nacional Técnica del Altiplano, Puno, Peru, Abstract, 1970, pp 144–147. 37. Condorena N, Sumar J, Alarcón V: Per yodo de gestacion en llamas (Lama pacos). Turrialba XXXX••;42:112–113. 38. Fernandez-Baca S, Hansel W, Saatman R, et al: Differential luteolytic effect on right and left uterine horns in the alpaca. Biol Reprod 1979;20:586–595. 39. Sumar J: Algunos aspectos obstétricos de la alpaca. Boletín Técnico No. 2. IVITA, Universidad Nacional Mayor de San Marcos, Convenio CIID-Canada, 1985, 16 pp. 40. Del Campo MR, Del Campo CH, Ginther OJ: Vascular provisions for a local utero-ovarian cross-over pathway in New World camelids. Theriogenology 1996;46:983–991. 41. Sumar J: Gestación gemelar en la alpaca. Rev Inv Pec (IVITA) Universidad Nacional Mayor de San Marcos 1980;5:58–60. 42. Fowler ME: Twinning in llamas. Llamas Int Cam J 1990;35–38. 43. Steven DH, Burton GJ, Sumar J, Nathanielsz PW: Ultrastructural observations on the placenta of the alpaca (Lama pacos). Placenta 1980;1:21–32. 44. Sumar J: Reproduction in llamas and alpacas. Anim Reprod Sci 1996;42:405–415. 45. Merkt H, Boer M, Rath D, Schoon HA: The presence of an additional fetal membrane and its function in
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the newborn guanaco (Lama guanicoe). Theriogenology 1988;30:437–439. Sumar J: Removal of the ovaries or ablation of the corpus luteum and its effect on the maintenance of gestation in the alpaca and llama. Acta Vet Scand Suppl 1983;83:133–141. Bravo PW, Sumar J, Riera SG, Foote WC: Reproductive wastage in female alpaca. In Improving reproductive performance of small ruminants. Utah State University, Logan, UT, 1987, pp 155–159. Sumar J: Algunos aspectos obstétricos de la alpaca. Boletín Técnico No. 2. Universidad Nacional Mayor de San Marcos, Convenio CIID-Canada. Lima, Peru, 1985. Del Castillo M, Aedo R: El parto en la llama (Lama glama). Bach. thesis, Universidad Nacional S Antonio Abad, Cusco, Peru, 1988. p 75. Knight TW, Death AF, Wyeth TK: Photoperiodic control of the time of parturition in alpacas (Lama pacos). Anim Reprod Sci 1995;39:259–265. Sumar J, Smith GW, Mayhua E, Nathanielsz PW: Adrenocortical function in the fetal and new born alpaca. Comp Biochem Physiol 1978;59A:79–84.
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52. Liggins GC: The fetus and birth. In Austin CR, Short RV (eds): Embryonic and fetal development, 2nd ed. Vol 2; Reproduction in mammals. Cambridge, UK: Cambridge University Press, 1983, pp 114–141. 53. Osorio de Valdivia E, Sumar J, Casas J, Ponce J: Inducción y sincronizacion del parto en la alpaca. AnnVII Reunión Asoc Latinoam Prod Anim (ALPA), Panamá, 1979. 54. Bravo WP, Bazab PJ, Troedsson MHT, et al: Induction of parturition in alpacas and subsequent survival of neonates. J Am Vet Med Assoc 1996;209:1760–1762. 55. Smith BB, Timm KI, Reed PJ, Christensen, M: Use of cloprostenol as an abortifacient in the llama (Lama glama). Theriogenology 2000;54:497–505. 56. Sumar J, Novoa C, Fernandez-Baca S: Fisiologia reproductiva postparto en la alpaca. Rev Inv Pec (IVITA), Universidad Nacional S Maecos 1972;1:21–27. 57. Lichtenwalner AB, Woods GL, Weber JA: Male llama choice between receptive and nonreceptive females. Appl Anim Behav Sci 1998;59:349–356.
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Breeding Soundness Examination of the Male Llama and Alpaca P. WALTER BRAVO
B
reeding soundness examination (BSE) is common in several livestock species and is an excellent tool that can be used to discard males that do not fit selection criteria. In llamas and alpacas, this procedure is still under development; nonetheless, there is tangible evidence that semen evaluation may be done without much elaboration or the use of sophisticated instrumentation. This section does not deal with different traits that are used to select a sire, commonly known among llama and alpaca breeders as a “padre.” Other phenotypic criteria are beyond the scope of this section and the reader is counseled to look for further literature. Rather, this section is
devoted completely to the examination of the external genitalia and their physiology, including semen evaluation and assessing circulating concentrations of testosterone. Some general criteria for identification are also considered because most BSEs will be used for future sires.
IDENTIFICATION Most males considered for BSE should have an accurate and lasting identification. Ear tags, collars, and recently, microchips are used to identify animals. Different brands of microchips, ear tags, and collars are available on the