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Reproduction in llamas and alpacas
ELSEVIER
Animal Reproduction Science 42 (1996) 405-415
Reproduction in llamas and alpacas Julio B. Sumar Universidad Nacional Mayor de San Marcos, Estacion Principal de Aha
de La Raya, Cusco. Peru
Abstract Alpacas and llamas have common ancestry and many similarities in their reproductive systems, but are nevertheless distinct species with anatomical and physiological differences. Their reproductive anatomy has been wel1 documented, but there is a paucity of conclusive, reliable information on their physiology. They are induced ovulators, but little is known about the factors controlling seasonal breeding. Conception rates and embryo mortality are highly variable under natura1 conditions. Despite the paucity of basic information there have been some succes& attempts at embryo transfer and artifïcial insemination in both species, and at interspecific hybridisation. Keywords: Alpaca; Llama; Reproduction
1. Introduction
Most domestic breeds of alpacas and llarnas were developed from common ancestry in South America before the arrival of Europeans. Many aspects of reproduction are similar between alpacas and Ilamas, but there are differences between these two domestic species which can be atxributed to speciation and to physiological variation arising kom several hundred years of selection.
2. Anatomy and physiology 2.1. Anutomy The dimensions of alpaca and llama reproductive tracts have been described elsewhere (Fowler, 1989; Bravo and Sumar, 1983). The ovaries are of a globular irregular shape, similar to those of the sow, particularly when they have multiple follicles. Follicles between 5 and 12 mm are considered normal. The uterus of the alpaca is bicornuate and both oviducts are convoluted, ending in a bursa which surrounds the Elsevier Science B.V. PI1 SO378-4320(96)01538-2
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ovary. The tips of the uterine horns in alpacas and llamas are blunt and rounded, and the oviduct opens into the uterine horn via a small, raised papilla which acts as a wel1 defined sphincter. Even under pressure, it is not possible to flush liquids from the uterus into the oviduct, but antegrade flushing is possible. The cervix has two or three irregularly annular or spiral folds. The uterine body and horns are readily palpable per rectum. The placenta in the alpaca, as in other camelids, is diffuse and epitheliochorial in type (Steven et al., 1980). In late gestation, both chorionic and uterine epithelia are deeply indented by placenta1 capillaries, so that the minimum intercapillary distance across the diffusion pathway may be as little as 2 mm. This distance appears to be less than that found in the epitheliochorial placenta of any other species of domestic ungulate in late gestation and may be one of several adaptations to pregnancy at high altitudes (Steven et al., 1980). A unique extra foetal membrane encasing the entire foetal body is attached at the mucocutaneous junction and coronary bands in newborn alpacas, llamas and vicuñas (J. Sumar, unpublished observations, 1976) and guanacos (Merkt et al., 1988). 2.2. Puberty Female alpacas of 12-13 months have behavioural oestrus similar to adult alpacas (Novoa et al., 1972). The majority of females are sexually receptive at 12 months of age, even though ovarian activity begins at 10 months. There is a relationship between body weight at mating and subsequent birth rate (Leyva and Sumar, 1981). In traditional Peruvian production systems, less than 50% of yearling alpacas reach appropriate liveweight (33 kg) for mating at 1 year of age and breeding is postponed unti12 years in alpacas and at least 3 years in llamas. With better nutrition after weaning (7-8 months of age), almost 100% of yearling alpacas can reach 33 kg body weight (Bustinza and Medina, 1986). 2.3. Reproductive season Alpacas and llamas, and the wild species of camelids such as the vicuña and guanaco, in their natura1 habitat in the highlands of southern Peru breed from December to Match, the warmest months of the year when rainfall is sufficient and green forage abundant (San Ma& et al., 1968; Franklin, 1983). Similarly, in peasant community farms, where males and females are together al1 year, the birth and breeding times fa11 within this range. However, when females are isolated from males and copulation is allowed only once a month both sexes are sexually active during the course of the whole year, and ovulation, fertilisation rates and embryo survival do not vary (Femandez-Baca et al., 1972a). Observations in various zoological parks around the world also indicate that camelids, both domestic and wild, are capable of year-round breeding (Schmidt, 1973), as is the case witb llamas kept in North America, though there is a summer peak in fertility (Johnson, 1988). On the other hand, continuous association of females and males has been shown to inhibit sexual activity of the latter (Femandez-Baca et al., 1972b). Environmental factors responsible for the onset and cessation of sexual activity under natural conditions are not clearly defined.
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of ovarian events
Since copulation is ordinarily a necessary prelude to ovulation, alpacas and llamas have been classified as reflex or induced ovulators (San Martin et al., 1968) 2.4.1. Ovarian follicular activity When not exposed to a male, female alpacas have long periods of sexual receptivity, and short periods of non-receptivity to the male that can last 48 h (San Mat& et al., 1968); these are correlated with rhythmic increases and decreases in serum oestrogen levels, reflecting successive waves of maturation and atresia of ovarian follicles. However, there is considerable individual variability in both the duration of sexual receptivity and regularity of its occurrence, presumably reflecting the fact that in unmated females the follicular phase is not terminated by ovulation at a fixed time, and that there is no luteal phase to regulate the timing of events. There are differing estimates of the periods of growth, maintenance, and regression of follicles of alpacas (Bravo and Sumar, 1989) and llamas (Bravo, 1990; Adams et al., 1990), although there is evidente to suggest that mating and lactation shorten the time between the appearance of successive dominant follicles (Adams et al., 1990). 2.4.2. Oestrus and ovulation Receptive females assume the prone position (ventral recumbency), the position for copulation, after a short period of pursuit by a male, or may approach a male mat is copulating with another female and adopt the prone position (San Martin et al., 1968; England et al., 1971). Some receptive females may occasionally display mounting behaviour with other females of the herd, although such behaviour is much less common than in cattle. A non-receptive female rejects the male (England et al., 1971). Coitus is prolonged in camelids (10-50 min) (Sumar, 1985a). A single service by an intact or vasectomised male is suftkient to induce ovulation in alpacas, with ovulation occurring from 1 to 3 days later (Femandez-Baca, 1970; Adams et al., 1989; Adams et al., 1990; Sumar et al., 1993b). There is an increase in serum luteinising hormone (LH) 15 min after the onset of copulation, followed by a peak at 2 h and a return to basal concentrations by 7 h (Bravo, 1990). Serum oestradiol concentrations remain unchanged for a period of 18 h after copulation, tend to decline at 22 h, and are significantly lower by 48 h after copulation. There is no further release of LH after a second copulatory period within 24 h (Bravo, 1990). Twenty-six to 28% of alpacas do not ovulate in response to copulation and an increase in the number of services does not affect ovulation rate (Femandez-Baca, 1970). Ovulation occurs with approximately equal frequency in both ovaries in alpacas (Sumar, 1985a) and llamas (Sumar and Leyva, 1979). Multiple ovulation occurs in 3-10% of alpacas after natura1 mating and in 9-20% after treatment with gonadotrophins, but twins bom alive are very rare (Sumar, 1985a). Treatment with human chorionic gonadotrophin (hCG, 500-700 IU, i.m.) (San Ma& et al., 1968) 1 mg of LH or 4-8 mg of gonadotrophin-releasing hormone (GnRH) provides an adequate stimulus for ovulation (Sumar, 1985a). Females can occasionally ovulate without coital stimulation or exogenous hormones, particularly after
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isolation from and reintroduction to a male. Estimates of spontaneous ovulation range from 5% in alpacas (Fernandez-Baca, 1970; Sumar, 1985a) to 9-15% in Ilamas (England et al., 1969; Adams et al., 1989; Adams et al., 1990). 2.4.3. Corpus luteum jûnction In non-pregnant alpacas, the corpus luteum undergoes rapid development after ovulation, reaching maximum size and secretory activity 8-9 days after mating, and regresses sharply 12 days post-mating (Femandez-Baca, 1970). The rapid decline in progesterone secretion occurs in connection with repeated surges of PGF,, (Sumar et al., 1988). A similar pattern of progesterone secretion occurs in llamas (England et al., 1969). A prolonged luteal phase has not been observed in any sterile-mated alpacas or Ilamas. A fertile llama mating results in the formation of a corpus luteum which remains functional throughout gestation (Adams et al., 1991). The corpus luteum can be detected by ultrasound on day 3 and reaches maximum size on day 21.4 f 1.2 (where day 0 is day of ovulation). A transient decrease in luteal size and plasma progesterone concentration has been observed between Days 8 and 10 in both llamas and alpacas (Sumar, 1991; Adams et al., 1991). Plasma progesterone concentrations remain elevated until about 2 weeks before parturition (Leon et al., 19901, thereafter slowly declining and finally falling markedly during the final 24 h before parturition. The corpus luteum is necessary for the maintenance of pregnancy throughout gestation in both species (Sumar, 1983a). 2.5. Pregnancy The length of gestation in alpacas of the Huacaya and Suri breeds has been quoted as 341 and 345 days, respectively (San Martin et al., 1968). For llamas in the USA, means of 344 days (range 331-347 days) were reported (Johnson, 1988). Neither parity nor sex of the cria influences gestation length (Sumar, 1985b). Almost al1 alpaca and Ilama fetuses occupy the left uterine hom, even though ovulation occurs from both ovaties with equal frequency (Table 1). This indicates tbat embryos originating in the right side migrate to the left horn for attachment. The reason for the right-to-left migration, which is apparently unique to Camelidae, is unknown. There may be a differential luteolytic effect of the left and right uterine homs (Fernandez-Baca et al., 19791, which may be implicated in the reduction of twin
Table 1 Location of corpora lutea (CL) in relation to that of the embryo in Location of CL
No. of animals
Right ovary Left ovary Both ovaries Total
472 (50.9%) 440 (47.4%) 16 (1.7%) 928
Sources: Sumar and Leyva (19791, Sumar (1985a).
alpacas
Location of embryo Right hom
Left hom
12 (2.5%) 3 (0.7%) 0 15 (1.6%)
46 (97.5%) 437 (99.3%) 16 (100%) 913 (98.4%)
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pregnancies to singles (Sumar, 1991). Twin pregnancies are only occasionally seen in the early stages of gestation. Llama twins may be more common than in alpacas. 2.6. Pregnuncy diagnosis Several methods of pregnancy diagnosis have been described in alpacas and llamas. In the traditional breeding system in southem Peru, pregnancy diagnosis is done by extemal palpation (ballottement) at 8 months of gestation, but this method is not appropriate for good reproductive management (Sumar, 1985a). Vasectomised males used to detect oestrus 20 or more days after a previous service are reliable for detection of non-pregnant females, but not al1 females that reject the male are necessarily pregnant (Femandez-Baca, 1970; Sumar et al., 1993a). Overall, the accuracy of this method for alpacas and llamas is 84% and 95% respectively, within 70-125 days of gestation (Alarcon et al., 1990). Rectal palpation in alpacas is possible as early as 30 days, but is limited by pelvic size and fat deposition in the pelvic inlet, particularly in yearling animals (Alarcon et al., 1990). Seventy percent of yearlings and 90% of adult alpacas can be palpated rectally. In llamas, almost 100% can be palpated. However, the accuracy of this method at 2 months post-mating is 100% in alpacas and llamas (Alarcon et al., 1990). Plasma progesterone changes during the first 30 days of gestation in the alpaca and llama are shown in Table 2. Alpacas or llamas that failed to ovulate, as wel1 as those
Table 2 Blood progesterone levels (nmol IDay
LhllaS
Pregnant
1 5 8 9 10 11 12 13 14 15 16 17 18 19 20 25 30
’) in pregnant and non-pregnant alpacas and llamas dwing the fust 30 days
Alpacas Non-pregnant
Plqnant
Mean
Range
Mean
Me+Itl
Range
MW
0.3 2.4 18.5 16.3 13.7 12.8 16.0 17.3 16.9 12.3 14.4 15.3 12.7 16.6 16.7 13.0 14.0
0.1-0.6 1-5 9-33 10-22 9-22 6-20 11-21 12-21 11-24 8-17 9-21 9-27 8-16 8-24 8-23 10-14 11-17
0.4 1.5 12.0 3.2 0.8
0.5 1.9 16.4 17.8 20.7 25.1 23.2 20.5 22.7 24.6 18.2 22.3 18.0 18.6 17.5 20.4 18.3
0.5-0.6 1-3 8-33 15-20 13-44 13-64 14-47 7-53 9-49 12-62 10-40 9-60 10-35 10-37 9-32 9-49 9-33
0.5 1.4 10.9 14.1 6.9 2.9 0.3
Source: Sumar (1991).
Non-pregnant
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that failed to conceive, showed basal levels of progesterone on day 12 and 30 after mating. In this study, animals were considered pregnant at 1.8 ng ml-’ on day 12 (Sumar et al., 1993a). The occurrence of false positives with high blood progesterone concentrations is probably due to early embryonic 10s~. A striking differente in milk progesterone concentrations between lactating non-pregnant and pregnant alpacas at 12 days after mating could be used as the basis for an early pregnancy test (Sumar, 1991; Sumar et al., 1993a). Ultrasonic techniques for pregnancy diagnosis have been used in alpacas and llamas (Alarcon et al., 1990). In alpacas, the highest accuracy (92%) was recorded at a mean foetal age of 80 days, compared with 90% at 70 days of gestation. In llamas, 100% accuracy was obtained at 75 days of gestation. In both species, the accuracy of the test was reduced to 84% and 65% at 165 days in alpacas and llamas, respectively. Using transrectal ultrasonography, detection of pregnancy has been reported as early as 15 days (Johnson, 19881, but accuracy in most llamas is not adequate until about 28 days of gestation. 2.7. Fertility rates and embryo/foetal
mortality
In al1 farm species studied, the bulk of embryonic loss occurs during the early stages. In an early study of alpacas, more than 80% of the ova recovered 3 days after mating were in the process of dividing, and only 50% of the fertilised ova survived for more than 30 days of gestation (Femandez-Baca, 1970). In a later study, however, reproductive wastage in female alpacas of different ages and reproductive status reached 83.2% (ova, embryo and foetal 10s~) (Bravo et al., 1987). NO embryo-fetal losses were found from 90 days post-mating to term. Factors responsible for this high rate of embryonic mortality are unknown, but nutritional and other environmental constraints may be important since these studies were conducted in alpacas living in their natura1 habitat, a harsh natura1 environment. The causes of embryo/fetal loss require critical evaluation. 2.8. Parturition Parturition in alpacas and llamas is generally quick and easy (Sumar, 1985b; Del Castillo and Aedo, 1988). More than 90% of births in alpacas and llamas occur between 07:OO and 13:00 h. This adaptation gives the cria the best chance to get warm and dry before the cold of night, when even .in the summer, freezing temperatures are common at altitude (Sumar, 1985a). Camelids appear to be able to delay birthing for hours or days to avoid giving birth during the night or on cold days (Sumar et al., 1978). 2.8.1. Control of parturition The arguments for attempting to regulate the onset of parturition are associated principally with managerial or veterinary considerations. Parturition can be induced between days 320 and 351 more successfully and with less side effects with PGF,, than with dexamethasone either alone or in combination with oestradiol (Osorio de Valdivia et al., 1979).
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2.8.2. Postpartum period
Up to the fourth day after parturition the female alpaca wil1 submit to mounting by the male (Sumar et al., 1972). However, luteal regression, follicular growth and uterine involution are not complete, and the female wil1 not ovulate or become pregnant from such early matings. Fertilisation occasionally occurs after mating at 5 days post-partum. By 10 days post-partum the follicles have developed, the corpus luteum has regressed and the uterus is mostly involuted. Mating of females is recommended within 15-20 days after giving birth to obtain good fertility and one offspring per year (Sumar et al., 1972).
3. Male anatomy and physiology 3.1. Anatomy
Male reproductive anatomy has been reviewed elsewhere (Sumar, 1985a; Fowler, 1989). 3.2. Puberty At birth, the penis is completely adherent to the prepuce, but this disappears gradually with growth under the influence of testosterone (Sumar, 1983b; Sumar, 1985a). At 1 year of age, the males show sexual interest in the females, but only about 8% of alpaca males have complete liberation of the penis-prepuce adhesions and are capable of performing copulation (Sumar, 1985a). At 2 years of age, approximately 70% of the males are free of the adhesions, and 100% at 3 years of age. Precocious behaviour and early mating are considered to be desirable traits in genetic selection programmes. Sires are selected on the absente of prepuce-penis adhesions as yearlings. A male alpaca reaches full development at 5 years of age (Sumar, 1983b), but the genera1 practice is to use the males for reproduction at 3 years of age (Sumar, 1985a). Sires are also selected by testis size, on the assumption of a direct relationship with sperm production as seen in other species. 3.3. Spermatogenesis
and semen characteristics
There is only one report on the cycle of the seminiferous epithelium of the llama. This was divided into eight stages, with the relative frequenties different from those described in the camel (Camelus dromedarius) (Delhon and Lawzewitsch, 1987). Ejaculation is a continuous process, with more or less uniform semen quality from the beginning to the end of the copulation (Kubiceck, 1974; Sumar and Garcia, 1986). The collection of semen is complicated by the position of the mating animals. Several methods, such as intravaginal sponges or pessaries, and electroejaculation, have been tried without much success. The use of an artificial vagina mounted inside a dummy, although more natura1 and reliable than the other methods, is not as effective as in rams. The collection of as much as 12.5 ml of ejaculate with a density of 600000 sperm ml-’
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has been reported with the use of an artificial vagina mounted inside a dummy (Sumar and Garcia, 1986). The semen of the alpaca is highly viscous, making the separation of spermatozoa from seminal plasma and the estimation of sperm concentration by conventional methods difficult. Owing to the high viscosity of the seminal plasma, sperm mass motility is slow (Sumar and Garcia, 1986).
4. Mating systems Sexual activity of the alpaca in the open field is particularly intense during the first week of the breeding season, with over 70% of females mating at least once (Femandez-Baca et al., 1972b). Sexual activity decreases thereafter, reaching zero in some instances, but after changing the males, mating activity can be reactivated reaching a leve1 comparable that of the first week. Based on these observations, a breeding system named ‘altemate or rotary’ was developed (Novoa et al., 1970). This system works wel1 in herds larger than 100 females, as is commonly found in southem Peru. Males are used at a 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 altemating the males, libido and mating activity remain high and it maximises the opportunity for the females to be mated at least once. Use of the rotary breeding system in a large alpaca cooperative in Peru resulted in an increase in birth rate from 57 to 81% (Novoa et al., 1970). 4.1. Artificial insemination There have been a number of studies on the feasibility of artificial insemination in alpacas and llamas (Calderon et al., 1968; Sumar and Leyva, 1981; Sumar, 1983b). Inter-species crosses have also been tried between alpaca and vicuña and between Ilama and vicuña. A recto-palpation method, depositing the semen in the homs of the uterus, can be used in alpacas (Calderon et al., 1968). After ovulation had been induced with vasectomized males and with hCG, it was found that the most appropriate time for insemination was 35-45 h following induction of the ovulation. Fertility rates were higher using vasectomised males than hCG to induce ovulation. Studies using vicuña semen and paco-vicuña semen with female alpacas and llamas have met with various levels of success (Leyva et al., 19771, but fertility after natura1 mating is also very low (Bravo et al., 1987).
5. Embryo transfer
Superovulation and embryo collection have been reported in alpacas, but with limited success (Novoa and Sumar, 1968). A study in 1973 reported a successful surgical embryo transfer and live birth of one alpaca and three late abortions (Sumar and Franco, 1974). Non-surgical embryo collection and transfer procedures have been described for llamas (Wiepz and Chapman, 1985). In recent years, there have been many other reports
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of successful embryo transfer in llamas, but the results are not consistent or reconcilable due to differences in experimental conditions. Further studies on superovulation regimes, fertilisation, recovery and transfer of embryos are required.
6. Conclusion
As more basic information is collected about the factors regulating the reproductive processes in alpacas and llamas, it should be possible to improve fertility through better management practices and through the application of reproductive technology. It has been demonstrated that embryo transfer and AI are feasible, but we require more information on mechanisms regulating superovulation, fertilisation and embryo recovery, transfer and survival.
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Femandez-Baca, S., Novoa, C. and Sumar, J., 1972a. Actividad reproductiva en la alpaca mantenida en separacion del macho. Mem. ALPA., 7: 7-18. Femandez-Baca, S., Sumar, J. and Novoa, C., 1972b. Comportamientq de la alpaca macho frente a la renovacion de la hembras. Rev. Inv. Pet. (IVITA), Univ. N.M. San Marcos, 1: 115-128. Femandez-Baca, S., Hansel, W., Saatman, R., Sumar, J. and Novoa, C., 1979. Differential luteolytic effect on right and left uterine homs in the alpaca. Biol. Reprod., 20: 586-595. Fowler, M.E., 1989. Medicine and Surgery of South American Camelids. Llama, Alpaca, Vicuña, Guanaco. Iowa University Press, Ames. Franklin, W.L., 1983. Contrasting socioecologies of South America’s wild camelids: The vicuña and the guanaco. In: J.F. Eisenbery and D.G. Kleinman @ditom), Advances in the Study of Mammahan Behaviour. Am. Sec. Mammalogists, 7: 573-629. (Spet. Pub].) Johnson, L.W., 1988. Llama reproduction. In: L.W. Johnson @dito& Llama Medicine Workshop for Veterinarians. Appendix lob. Colorado State University, Fort Collins. Kubiceck, J., 1974. Samanentnahme beim Alpaca durcheine Hamrohrenfistel (Semen collection in alpaca with an urethral Bstula). Z. Tierx. Zuechtungsbiol., 90: 335-351. Leen, J.B., Smith, B.B., Timm, K.I. and Le Cren, G., 1990. Endocrine changes during pregnancy, parturition and the early post-partum period in the Ilama (lama glama). J. Reprod. Fertil., 88: 503-511. Leyva, V. and Sumar, J., 1981. Evahración del peso corporal al empadre sobte la capacidad reproductiva de hembras alpaca de un año de edad. In: Proc. 4th Int. Conv. on South American Camelids, Corporación Nacional Forestal e Inst. de la Patagonia, Punta Arenas, Chile. (Abstr. 1.) Leyva, V., Franco, E. and Sumar, J., 1977. Inseminacion Attificial en Camelidos Sudamericanos. In: 1 Reunion Assoc. Peruana de Produccion Animal (APPA), Lima. Merkt, H., Boer, M., Rath, D. and Schoon, H.A., 1988. The presence of an additional fetal membrane and its function in the newbom guanaco (Lama guanicoe). Theriogenology, 30: 437-439. Novoa, C. and Sumar. J., 1%8. Coleccion de huevos in vivo y Ensayos de Transferencia de Embriones en Alpacas. 3er Boletin Extraordinario (IVITA), Univ. N.M.S. Marcos. Novoa, C., Sumar, J. and Franco, E., 1970. Empadre complementario de alpacas hembras vac&. In: Proc. 1st. Int. Conv. on South American Camelids, Univ. Nac. Técnica del Altiplano, Puno, Peru. (Abstr. pp. 144-147.) Novoa, C., Femández-Baca, S., Sumar, J. and Leyva, V., 1972. Pubertad en la alpaca. Rev. Inv. Pet. (IVITA) Univ. Nac. M.S.M., l(1): 29-35. Osorio de Valdivia, E.M., Sumar, J., Casas, H. and Ponce, J., 1979. Induccion y sincronizacion del parto en la alpaca. Anales de la Vl1 Reunion de la Asociacion Latinoamericana de Produccion Animal (ALPA), Panama. San Martin, M., Copaira, M., Ztíñiga, J., Rodríguez, R., Bustinza, G. and Acosta, L., 1968. Aspects of reproduction in the alpaca. J. Reprod. Fertil., 16: 395. Schmidt, CR., 1973. Breeding season and notes on some other aspects of reproduction in captive camelids. Int. Zool. Yearbook, 13: 387-390. Steven, D.H., Button, G.J., Sumar, J. and Nathanielsz, P.W., 1980. Uhrastructural observations on the placenta of the alpaca (Lama patos). Placenta, 1: 21-32. Sumar, J., 1983a. Removal of the ovaries or ablation of the corpus luteum and its effect on the maintenance of gestation in the alpaca and llama. Acts Vet. Stand. Suppl., 83: 133-141. Sumar, J., 1983b. Studies on reproductive pathology in alpacas. M.Sc. Thesis, Swedish University of Agrarian Sciences, Department of Obstetrie and Gynaecology Veterinary Medicine Faculty, Uppsala, Sweden, 90 PP. Sumar, J., 1985a. Reproductive physiology in South American camelids. In: R.B. Land and D.W. Robinson (Editors), Genetics of Reproduction in Sheep. Butterwotths, London, pp. 81-95. Sumar, J., 1985b. Algunos aspectos obstétricos de la alpaca. Bol. Téc. No. 2, IVITA, Univ. Nac. M.S. Marcos, Convenio CIID-Canada, 16 pp. Sumar, J., 1991. Contribution of the radioimmunoassay technique to knowledge of the mproductive physiology of South American camelids. In: Isotope and Related Techniques in Animal Production and Health. FAO/IAEA, Vienna, Austria, pp. 353-379. Sumar, J. and Franco, E., 1974. Ensayos de Transferencia de Embriones en Camelidos Suidamericanos. In: Informe Final (IVITAJ, Univ. N.M. San Marcos, Lima, Peru.
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41.5
Sumar, J. and Garcia, M., 1986. Fisiologia de la reproduccion de la alpaca. In: Nuclear and Related Techniques in Animal Pmduction and Health. IAEA, Vienna, pp. 149-177. Sumar, J. and Le.yva, V., 1979. Relación entm la ubicación del Cuerpo luteo y la localización del embrión en la llama (Lama glamo). Anales 111Conv. Int. Sobre Camélidos Sudamericanos, Viedma, Argentina. Sumar, J. and Leyva, V., 1981. Coleccion de Semen mediante Vagina Aftïcial en la Alpaca (Lama patos). In: IV Convencion Intemacional Sobre Camelidos Sudamericanos, 22-27 November, Corporacion Nacional Forestal e Instituto de la Patagonia, Punta Arenas, Cbile. Sumar, J., Novoa, C. and Femandez-Baca, S., 1972. Fisiologia reproductiva post-parto en la alpaca Rev. Inv. Pet. (IVITA), Univ. N.M. San Marcos, 1: 21-27. Sumar, J., Smith, G.W., Mayhua, E. and Nathanielsz, P.W., 1978. Adrenocortical function in the fetal and new bom alpaca. Comp. Biochem. Physiol., 59A: 79-84. Sumar, J., Fredriksson, G., Alarcon, V., Kindahl, H. and Edqvist, L.E., 1988. Levels of 15keto-13,14-dihydro-PGF2a, progesterone and oestradiol-17B, after induced ovulations in llamas and alpaca. Acts Vet. Stand., 29: 339-346. Sumar, J., Alarcón, V. and Echevarrla, L., 1993a. Niveles de progesterona periférica en alpaca llamas y su aplicación en el diagnóstico precoz de gestación y otros usos clínicos. Acts Andina, 2: 161-167. Sumar, J., Bravo, P.W. and Foote, W.C., 1993b. Sexual receptivity and time of ovulation in alpacas. Smal1 Rumin. Res., 11: 143-150. Wiepz, D.W. and Chapman, R.J., 1985. Non-surgical embryo transfer and live birth in a Ilama. In: Johnsson (Editor), Llama Medicine Workshop for Veterinarians.
Animal Reproduction Science 42 (1996) 405-415
Reproduction in llamas and alpacas Julio B. Sumar Universidad Nacional Mayor de San Marcos, Estacion Principal de Aha
de La Raya, Cusco. Peru
Abstract Alpacas and llamas have common ancestry and many similarities in their reproductive systems, but are nevertheless distinct species with anatomical and physiological differences. Their reproductive anatomy has been wel1 documented, but there is a paucity of conclusive, reliable information on their physiology. They are induced ovulators, but little is known about the factors controlling seasonal breeding. Conception rates and embryo mortality are highly variable under natura1 conditions. Despite the paucity of basic information there have been some succes& attempts at embryo transfer and artifïcial insemination in both species, and at interspecific hybridisation. Keywords: Alpaca; Llama; Reproduction
1. Introduction
Most domestic breeds of alpacas and llarnas were developed from common ancestry in South America before the arrival of Europeans. Many aspects of reproduction are similar between alpacas and Ilamas, but there are differences between these two domestic species which can be atxributed to speciation and to physiological variation arising kom several hundred years of selection.
2. Anatomy and physiology 2.1. Anutomy The dimensions of alpaca and llama reproductive tracts have been described elsewhere (Fowler, 1989; Bravo and Sumar, 1983). The ovaries are of a globular irregular shape, similar to those of the sow, particularly when they have multiple follicles. Follicles between 5 and 12 mm are considered normal. The uterus of the alpaca is bicornuate and both oviducts are convoluted, ending in a bursa which surrounds the Elsevier Science B.V. PI1 SO378-4320(96)01538-2
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ovary. The tips of the uterine horns in alpacas and llamas are blunt and rounded, and the oviduct opens into the uterine horn via a small, raised papilla which acts as a wel1 defined sphincter. Even under pressure, it is not possible to flush liquids from the uterus into the oviduct, but antegrade flushing is possible. The cervix has two or three irregularly annular or spiral folds. The uterine body and horns are readily palpable per rectum. The placenta in the alpaca, as in other camelids, is diffuse and epitheliochorial in type (Steven et al., 1980). In late gestation, both chorionic and uterine epithelia are deeply indented by placenta1 capillaries, so that the minimum intercapillary distance across the diffusion pathway may be as little as 2 mm. This distance appears to be less than that found in the epitheliochorial placenta of any other species of domestic ungulate in late gestation and may be one of several adaptations to pregnancy at high altitudes (Steven et al., 1980). A unique extra foetal membrane encasing the entire foetal body is attached at the mucocutaneous junction and coronary bands in newborn alpacas, llamas and vicuñas (J. Sumar, unpublished observations, 1976) and guanacos (Merkt et al., 1988). 2.2. Puberty Female alpacas of 12-13 months have behavioural oestrus similar to adult alpacas (Novoa et al., 1972). The majority of females are sexually receptive at 12 months of age, even though ovarian activity begins at 10 months. There is a relationship between body weight at mating and subsequent birth rate (Leyva and Sumar, 1981). In traditional Peruvian production systems, less than 50% of yearling alpacas reach appropriate liveweight (33 kg) for mating at 1 year of age and breeding is postponed unti12 years in alpacas and at least 3 years in llamas. With better nutrition after weaning (7-8 months of age), almost 100% of yearling alpacas can reach 33 kg body weight (Bustinza and Medina, 1986). 2.3. Reproductive season Alpacas and llamas, and the wild species of camelids such as the vicuña and guanaco, in their natura1 habitat in the highlands of southern Peru breed from December to Match, the warmest months of the year when rainfall is sufficient and green forage abundant (San Ma& et al., 1968; Franklin, 1983). Similarly, in peasant community farms, where males and females are together al1 year, the birth and breeding times fa11 within this range. However, when females are isolated from males and copulation is allowed only once a month both sexes are sexually active during the course of the whole year, and ovulation, fertilisation rates and embryo survival do not vary (Femandez-Baca et al., 1972a). Observations in various zoological parks around the world also indicate that camelids, both domestic and wild, are capable of year-round breeding (Schmidt, 1973), as is the case witb llamas kept in North America, though there is a summer peak in fertility (Johnson, 1988). On the other hand, continuous association of females and males has been shown to inhibit sexual activity of the latter (Femandez-Baca et al., 1972b). Environmental factors responsible for the onset and cessation of sexual activity under natural conditions are not clearly defined.
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of ovarian events
Since copulation is ordinarily a necessary prelude to ovulation, alpacas and llamas have been classified as reflex or induced ovulators (San Martin et al., 1968) 2.4.1. Ovarian follicular activity When not exposed to a male, female alpacas have long periods of sexual receptivity, and short periods of non-receptivity to the male that can last 48 h (San Mat& et al., 1968); these are correlated with rhythmic increases and decreases in serum oestrogen levels, reflecting successive waves of maturation and atresia of ovarian follicles. However, there is considerable individual variability in both the duration of sexual receptivity and regularity of its occurrence, presumably reflecting the fact that in unmated females the follicular phase is not terminated by ovulation at a fixed time, and that there is no luteal phase to regulate the timing of events. There are differing estimates of the periods of growth, maintenance, and regression of follicles of alpacas (Bravo and Sumar, 1989) and llamas (Bravo, 1990; Adams et al., 1990), although there is evidente to suggest that mating and lactation shorten the time between the appearance of successive dominant follicles (Adams et al., 1990). 2.4.2. Oestrus and ovulation Receptive females assume the prone position (ventral recumbency), the position for copulation, after a short period of pursuit by a male, or may approach a male mat is copulating with another female and adopt the prone position (San Martin et al., 1968; England et al., 1971). Some receptive females may occasionally display mounting behaviour with other females of the herd, although such behaviour is much less common than in cattle. A non-receptive female rejects the male (England et al., 1971). Coitus is prolonged in camelids (10-50 min) (Sumar, 1985a). A single service by an intact or vasectomised male is suftkient to induce ovulation in alpacas, with ovulation occurring from 1 to 3 days later (Femandez-Baca, 1970; Adams et al., 1989; Adams et al., 1990; Sumar et al., 1993b). There is an increase in serum luteinising hormone (LH) 15 min after the onset of copulation, followed by a peak at 2 h and a return to basal concentrations by 7 h (Bravo, 1990). Serum oestradiol concentrations remain unchanged for a period of 18 h after copulation, tend to decline at 22 h, and are significantly lower by 48 h after copulation. There is no further release of LH after a second copulatory period within 24 h (Bravo, 1990). Twenty-six to 28% of alpacas do not ovulate in response to copulation and an increase in the number of services does not affect ovulation rate (Femandez-Baca, 1970). Ovulation occurs with approximately equal frequency in both ovaries in alpacas (Sumar, 1985a) and llamas (Sumar and Leyva, 1979). Multiple ovulation occurs in 3-10% of alpacas after natura1 mating and in 9-20% after treatment with gonadotrophins, but twins bom alive are very rare (Sumar, 1985a). Treatment with human chorionic gonadotrophin (hCG, 500-700 IU, i.m.) (San Ma& et al., 1968) 1 mg of LH or 4-8 mg of gonadotrophin-releasing hormone (GnRH) provides an adequate stimulus for ovulation (Sumar, 1985a). Females can occasionally ovulate without coital stimulation or exogenous hormones, particularly after
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isolation from and reintroduction to a male. Estimates of spontaneous ovulation range from 5% in alpacas (Fernandez-Baca, 1970; Sumar, 1985a) to 9-15% in Ilamas (England et al., 1969; Adams et al., 1989; Adams et al., 1990). 2.4.3. Corpus luteum jûnction In non-pregnant alpacas, the corpus luteum undergoes rapid development after ovulation, reaching maximum size and secretory activity 8-9 days after mating, and regresses sharply 12 days post-mating (Femandez-Baca, 1970). The rapid decline in progesterone secretion occurs in connection with repeated surges of PGF,, (Sumar et al., 1988). A similar pattern of progesterone secretion occurs in llamas (England et al., 1969). A prolonged luteal phase has not been observed in any sterile-mated alpacas or Ilamas. A fertile llama mating results in the formation of a corpus luteum which remains functional throughout gestation (Adams et al., 1991). The corpus luteum can be detected by ultrasound on day 3 and reaches maximum size on day 21.4 f 1.2 (where day 0 is day of ovulation). A transient decrease in luteal size and plasma progesterone concentration has been observed between Days 8 and 10 in both llamas and alpacas (Sumar, 1991; Adams et al., 1991). Plasma progesterone concentrations remain elevated until about 2 weeks before parturition (Leon et al., 19901, thereafter slowly declining and finally falling markedly during the final 24 h before parturition. The corpus luteum is necessary for the maintenance of pregnancy throughout gestation in both species (Sumar, 1983a). 2.5. Pregnancy The length of gestation in alpacas of the Huacaya and Suri breeds has been quoted as 341 and 345 days, respectively (San Martin et al., 1968). For llamas in the USA, means of 344 days (range 331-347 days) were reported (Johnson, 1988). Neither parity nor sex of the cria influences gestation length (Sumar, 1985b). Almost al1 alpaca and Ilama fetuses occupy the left uterine hom, even though ovulation occurs from both ovaties with equal frequency (Table 1). This indicates tbat embryos originating in the right side migrate to the left horn for attachment. The reason for the right-to-left migration, which is apparently unique to Camelidae, is unknown. There may be a differential luteolytic effect of the left and right uterine homs (Fernandez-Baca et al., 19791, which may be implicated in the reduction of twin
Table 1 Location of corpora lutea (CL) in relation to that of the embryo in Location of CL
No. of animals
Right ovary Left ovary Both ovaries Total
472 (50.9%) 440 (47.4%) 16 (1.7%) 928
Sources: Sumar and Leyva (19791, Sumar (1985a).
alpacas
Location of embryo Right hom
Left hom
12 (2.5%) 3 (0.7%) 0 15 (1.6%)
46 (97.5%) 437 (99.3%) 16 (100%) 913 (98.4%)
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pregnancies to singles (Sumar, 1991). Twin pregnancies are only occasionally seen in the early stages of gestation. Llama twins may be more common than in alpacas. 2.6. Pregnuncy diagnosis Several methods of pregnancy diagnosis have been described in alpacas and llamas. In the traditional breeding system in southem Peru, pregnancy diagnosis is done by extemal palpation (ballottement) at 8 months of gestation, but this method is not appropriate for good reproductive management (Sumar, 1985a). Vasectomised males used to detect oestrus 20 or more days after a previous service are reliable for detection of non-pregnant females, but not al1 females that reject the male are necessarily pregnant (Femandez-Baca, 1970; Sumar et al., 1993a). Overall, the accuracy of this method for alpacas and llamas is 84% and 95% respectively, within 70-125 days of gestation (Alarcon et al., 1990). Rectal palpation in alpacas is possible as early as 30 days, but is limited by pelvic size and fat deposition in the pelvic inlet, particularly in yearling animals (Alarcon et al., 1990). Seventy percent of yearlings and 90% of adult alpacas can be palpated rectally. In llamas, almost 100% can be palpated. However, the accuracy of this method at 2 months post-mating is 100% in alpacas and llamas (Alarcon et al., 1990). Plasma progesterone changes during the first 30 days of gestation in the alpaca and llama are shown in Table 2. Alpacas or llamas that failed to ovulate, as wel1 as those
Table 2 Blood progesterone levels (nmol IDay
LhllaS
Pregnant
1 5 8 9 10 11 12 13 14 15 16 17 18 19 20 25 30
’) in pregnant and non-pregnant alpacas and llamas dwing the fust 30 days
Alpacas Non-pregnant
Plqnant
Mean
Range
Mean
Me+Itl
Range
MW
0.3 2.4 18.5 16.3 13.7 12.8 16.0 17.3 16.9 12.3 14.4 15.3 12.7 16.6 16.7 13.0 14.0
0.1-0.6 1-5 9-33 10-22 9-22 6-20 11-21 12-21 11-24 8-17 9-21 9-27 8-16 8-24 8-23 10-14 11-17
0.4 1.5 12.0 3.2 0.8
0.5 1.9 16.4 17.8 20.7 25.1 23.2 20.5 22.7 24.6 18.2 22.3 18.0 18.6 17.5 20.4 18.3
0.5-0.6 1-3 8-33 15-20 13-44 13-64 14-47 7-53 9-49 12-62 10-40 9-60 10-35 10-37 9-32 9-49 9-33
0.5 1.4 10.9 14.1 6.9 2.9 0.3
Source: Sumar (1991).
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that failed to conceive, showed basal levels of progesterone on day 12 and 30 after mating. In this study, animals were considered pregnant at 1.8 ng ml-’ on day 12 (Sumar et al., 1993a). The occurrence of false positives with high blood progesterone concentrations is probably due to early embryonic 10s~. A striking differente in milk progesterone concentrations between lactating non-pregnant and pregnant alpacas at 12 days after mating could be used as the basis for an early pregnancy test (Sumar, 1991; Sumar et al., 1993a). Ultrasonic techniques for pregnancy diagnosis have been used in alpacas and llamas (Alarcon et al., 1990). In alpacas, the highest accuracy (92%) was recorded at a mean foetal age of 80 days, compared with 90% at 70 days of gestation. In llamas, 100% accuracy was obtained at 75 days of gestation. In both species, the accuracy of the test was reduced to 84% and 65% at 165 days in alpacas and llamas, respectively. Using transrectal ultrasonography, detection of pregnancy has been reported as early as 15 days (Johnson, 19881, but accuracy in most llamas is not adequate until about 28 days of gestation. 2.7. Fertility rates and embryo/foetal
mortality
In al1 farm species studied, the bulk of embryonic loss occurs during the early stages. In an early study of alpacas, more than 80% of the ova recovered 3 days after mating were in the process of dividing, and only 50% of the fertilised ova survived for more than 30 days of gestation (Femandez-Baca, 1970). In a later study, however, reproductive wastage in female alpacas of different ages and reproductive status reached 83.2% (ova, embryo and foetal 10s~) (Bravo et al., 1987). NO embryo-fetal losses were found from 90 days post-mating to term. Factors responsible for this high rate of embryonic mortality are unknown, but nutritional and other environmental constraints may be important since these studies were conducted in alpacas living in their natura1 habitat, a harsh natura1 environment. The causes of embryo/fetal loss require critical evaluation. 2.8. Parturition Parturition in alpacas and llamas is generally quick and easy (Sumar, 1985b; Del Castillo and Aedo, 1988). More than 90% of births in alpacas and llamas occur between 07:OO and 13:00 h. This adaptation gives the cria the best chance to get warm and dry before the cold of night, when even .in the summer, freezing temperatures are common at altitude (Sumar, 1985a). Camelids appear to be able to delay birthing for hours or days to avoid giving birth during the night or on cold days (Sumar et al., 1978). 2.8.1. Control of parturition The arguments for attempting to regulate the onset of parturition are associated principally with managerial or veterinary considerations. Parturition can be induced between days 320 and 351 more successfully and with less side effects with PGF,, than with dexamethasone either alone or in combination with oestradiol (Osorio de Valdivia et al., 1979).
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2.8.2. Postpartum period
Up to the fourth day after parturition the female alpaca wil1 submit to mounting by the male (Sumar et al., 1972). However, luteal regression, follicular growth and uterine involution are not complete, and the female wil1 not ovulate or become pregnant from such early matings. Fertilisation occasionally occurs after mating at 5 days post-partum. By 10 days post-partum the follicles have developed, the corpus luteum has regressed and the uterus is mostly involuted. Mating of females is recommended within 15-20 days after giving birth to obtain good fertility and one offspring per year (Sumar et al., 1972).
3. Male anatomy and physiology 3.1. Anatomy
Male reproductive anatomy has been reviewed elsewhere (Sumar, 1985a; Fowler, 1989). 3.2. Puberty At birth, the penis is completely adherent to the prepuce, but this disappears gradually with growth under the influence of testosterone (Sumar, 1983b; Sumar, 1985a). At 1 year of age, the males show sexual interest in the females, but only about 8% of alpaca males have complete liberation of the penis-prepuce adhesions and are capable of performing copulation (Sumar, 1985a). At 2 years of age, approximately 70% of the males are free of the adhesions, and 100% at 3 years of age. Precocious behaviour and early mating are considered to be desirable traits in genetic selection programmes. Sires are selected on the absente of prepuce-penis adhesions as yearlings. A male alpaca reaches full development at 5 years of age (Sumar, 1983b), but the genera1 practice is to use the males for reproduction at 3 years of age (Sumar, 1985a). Sires are also selected by testis size, on the assumption of a direct relationship with sperm production as seen in other species. 3.3. Spermatogenesis
and semen characteristics
There is only one report on the cycle of the seminiferous epithelium of the llama. This was divided into eight stages, with the relative frequenties different from those described in the camel (Camelus dromedarius) (Delhon and Lawzewitsch, 1987). Ejaculation is a continuous process, with more or less uniform semen quality from the beginning to the end of the copulation (Kubiceck, 1974; Sumar and Garcia, 1986). The collection of semen is complicated by the position of the mating animals. Several methods, such as intravaginal sponges or pessaries, and electroejaculation, have been tried without much success. The use of an artificial vagina mounted inside a dummy, although more natura1 and reliable than the other methods, is not as effective as in rams. The collection of as much as 12.5 ml of ejaculate with a density of 600000 sperm ml-’
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has been reported with the use of an artificial vagina mounted inside a dummy (Sumar and Garcia, 1986). The semen of the alpaca is highly viscous, making the separation of spermatozoa from seminal plasma and the estimation of sperm concentration by conventional methods difficult. Owing to the high viscosity of the seminal plasma, sperm mass motility is slow (Sumar and Garcia, 1986).
4. Mating systems Sexual activity of the alpaca in the open field is particularly intense during the first week of the breeding season, with over 70% of females mating at least once (Femandez-Baca et al., 1972b). Sexual activity decreases thereafter, reaching zero in some instances, but after changing the males, mating activity can be reactivated reaching a leve1 comparable that of the first week. Based on these observations, a breeding system named ‘altemate or rotary’ was developed (Novoa et al., 1970). This system works wel1 in herds larger than 100 females, as is commonly found in southem Peru. Males are used at a 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 altemating the males, libido and mating activity remain high and it maximises the opportunity for the females to be mated at least once. Use of the rotary breeding system in a large alpaca cooperative in Peru resulted in an increase in birth rate from 57 to 81% (Novoa et al., 1970). 4.1. Artificial insemination There have been a number of studies on the feasibility of artificial insemination in alpacas and llamas (Calderon et al., 1968; Sumar and Leyva, 1981; Sumar, 1983b). Inter-species crosses have also been tried between alpaca and vicuña and between Ilama and vicuña. A recto-palpation method, depositing the semen in the homs of the uterus, can be used in alpacas (Calderon et al., 1968). After ovulation had been induced with vasectomized males and with hCG, it was found that the most appropriate time for insemination was 35-45 h following induction of the ovulation. Fertility rates were higher using vasectomised males than hCG to induce ovulation. Studies using vicuña semen and paco-vicuña semen with female alpacas and llamas have met with various levels of success (Leyva et al., 19771, but fertility after natura1 mating is also very low (Bravo et al., 1987).
5. Embryo transfer
Superovulation and embryo collection have been reported in alpacas, but with limited success (Novoa and Sumar, 1968). A study in 1973 reported a successful surgical embryo transfer and live birth of one alpaca and three late abortions (Sumar and Franco, 1974). Non-surgical embryo collection and transfer procedures have been described for llamas (Wiepz and Chapman, 1985). In recent years, there have been many other reports
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of successful embryo transfer in llamas, but the results are not consistent or reconcilable due to differences in experimental conditions. Further studies on superovulation regimes, fertilisation, recovery and transfer of embryos are required.
6. Conclusion
As more basic information is collected about the factors regulating the reproductive processes in alpacas and llamas, it should be possible to improve fertility through better management practices and through the application of reproductive technology. It has been demonstrated that embryo transfer and AI are feasible, but we require more information on mechanisms regulating superovulation, fertilisation and embryo recovery, transfer and survival.
References Adams, G.P., Griffin, P.G. and Ginther, O.J., 1989. In situ morphologic dynamic of ovaties, uterus and cervix
in llamas. Biol. Reprod., 41: 551-558. Adams, G.P., Sumar, J. and Ginther, O.J., 1990. Effects of lactational and reproductive status on ovarian follicular waves in llamas (Lama glama). J. Reprod. Fertil., 90: 535-545. Adams, G.P., Surnar, J. and Gintber, O.J., 1991. Form and function of the corpus luteum in llamas. Anim. Reprod. Sci., 24: 127-138. Alarcon, V., Sumar, J., Riera, G.S. and Foote, W.C., 1990. Comparison of three methods of ptegnancy diagnosis in alpacas and llamas. Theriogenology, 34: 1119. Bravo, P.W., 1990. Studies on ovarian dynamics and response to copulation in the South American camelids Lama giama and Lama patos. Ph.D. Thesis, Davis University, 91 pp. Bravo, P.W. and Sumar, J., 1983. Some anatomical parameters of the teproductive tract in alpacas. Resúmenes de Inves., Univ. N.M.S. Marcos, Lima. Bravo, P.W. and Sumar, J., 1989. Laparoscopic examination of the ovarian activity in alpacas. Anim. Reprod. Sci., 21: 271. Bravo, P.W., Sumar, J.. Riera, S.G. and Foote, W.C., 1987. Reproductive wastage in female alpaca. In: Improving Reproductive Performance of Smal1 Ruminants. Utah State University, Logan, pp. 155-159. Bustinxa, V. and Medina, G., 1986. Ctecimiento de alpacas. Memorias del V Cong. Int. de Sistemas Agropecuatios Andinos, Puno, Peru. (Abstr. 408.) Calderon, W., Sumar, 1. and Franco, E., 1968. Avances en la Inseminacion ArtificiaJ de las alpacas (Lama patos). In: Revista de la Fa cultad de Medicina Veterinaria, Lima, Peru. Univ. N.M. San Marcos, Vol. 22, p. 19. Del Castillo, M. and Aedo, R., 1988. El parto en la llama (Lama glamu). Bach. Thesis, Univ. Nac. S. Antonio Abad, Cusco, 75 pp. Delhon, G.A. and Lawxewitsch, I.V., 1987. Reproduction in the male llama (Lama gha), a South American camelid. 1. Spermatogenesis and organixation of intertubular space of the mature testis. Acts Anat., 129: 59-66. England, B.G., Foote, W.C., Matthews, D.H., Cardozo, A. and Riera, S., 1969. Ovulation and corpus luteum in the llama (krmn gkuna). J. Endocrinol., 45: 505-513. Bttgland, B.G., Foote, W.C., Cardozo, A.G.. Matthews, D.H. and Riem, S., 1971. Gestrous and mating behaviour in the llama (Lama glamu). Anim. Behav., 19: 722-726. Femandez-Baca, S., 1970. Luteal limction and the nature of reproductive failutes in aipacas. Ph.D Thesis, Comell University, Ithaca, NY, pp. 84-100.
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Reproduction Science 42 (1996) 405-415
Femandez-Baca, S., Novoa, C. and Sumar, J., 1972a. Actividad reproductiva en la alpaca mantenida en separacion del macho. Mem. ALPA., 7: 7-18. Femandez-Baca, S., Sumar, J. and Novoa, C., 1972b. Comportamientq de la alpaca macho frente a la renovacion de la hembras. Rev. Inv. Pet. (IVITA), Univ. N.M. San Marcos, 1: 115-128. Femandez-Baca, S., Hansel, W., Saatman, R., Sumar, J. and Novoa, C., 1979. Differential luteolytic effect on right and left uterine homs in the alpaca. Biol. Reprod., 20: 586-595. Fowler, M.E., 1989. Medicine and Surgery of South American Camelids. Llama, Alpaca, Vicuña, Guanaco. Iowa University Press, Ames. Franklin, W.L., 1983. Contrasting socioecologies of South America’s wild camelids: The vicuña and the guanaco. In: J.F. Eisenbery and D.G. Kleinman @ditom), Advances in the Study of Mammahan Behaviour. Am. Sec. Mammalogists, 7: 573-629. (Spet. Pub].) Johnson, L.W., 1988. Llama reproduction. In: L.W. Johnson @dito& Llama Medicine Workshop for Veterinarians. Appendix lob. Colorado State University, Fort Collins. Kubiceck, J., 1974. Samanentnahme beim Alpaca durcheine Hamrohrenfistel (Semen collection in alpaca with an urethral Bstula). Z. Tierx. Zuechtungsbiol., 90: 335-351. Leen, J.B., Smith, B.B., Timm, K.I. and Le Cren, G., 1990. Endocrine changes during pregnancy, parturition and the early post-partum period in the Ilama (lama glama). J. Reprod. Fertil., 88: 503-511. Leyva, V. and Sumar, J., 1981. Evahración del peso corporal al empadre sobte la capacidad reproductiva de hembras alpaca de un año de edad. In: Proc. 4th Int. Conv. on South American Camelids, Corporación Nacional Forestal e Inst. de la Patagonia, Punta Arenas, Chile. (Abstr. 1.) Leyva, V., Franco, E. and Sumar, J., 1977. Inseminacion Attificial en Camelidos Sudamericanos. In: 1 Reunion Assoc. Peruana de Produccion Animal (APPA), Lima. Merkt, H., Boer, M., Rath, D. and Schoon, H.A., 1988. The presence of an additional fetal membrane and its function in the newbom guanaco (Lama guanicoe). Theriogenology, 30: 437-439. Novoa, C. and Sumar. J., 1%8. Coleccion de huevos in vivo y Ensayos de Transferencia de Embriones en Alpacas. 3er Boletin Extraordinario (IVITA), Univ. N.M.S. Marcos. Novoa, C., Sumar, J. and Franco, E., 1970. Empadre complementario de alpacas hembras vac&. In: Proc. 1st. Int. Conv. on South American Camelids, Univ. Nac. Técnica del Altiplano, Puno, Peru. (Abstr. pp. 144-147.) Novoa, C., Femández-Baca, S., Sumar, J. and Leyva, V., 1972. Pubertad en la alpaca. Rev. Inv. Pet. (IVITA) Univ. Nac. M.S.M., l(1): 29-35. Osorio de Valdivia, E.M., Sumar, J., Casas, H. and Ponce, J., 1979. Induccion y sincronizacion del parto en la alpaca. Anales de la Vl1 Reunion de la Asociacion Latinoamericana de Produccion Animal (ALPA), Panama. San Martin, M., Copaira, M., Ztíñiga, J., Rodríguez, R., Bustinza, G. and Acosta, L., 1968. Aspects of reproduction in the alpaca. J. Reprod. Fertil., 16: 395. Schmidt, CR., 1973. Breeding season and notes on some other aspects of reproduction in captive camelids. Int. Zool. Yearbook, 13: 387-390. Steven, D.H., Button, G.J., Sumar, J. and Nathanielsz, P.W., 1980. Uhrastructural observations on the placenta of the alpaca (Lama patos). Placenta, 1: 21-32. Sumar, J., 1983a. Removal of the ovaries or ablation of the corpus luteum and its effect on the maintenance of gestation in the alpaca and llama. Acts Vet. Stand. Suppl., 83: 133-141. Sumar, J., 1983b. Studies on reproductive pathology in alpacas. M.Sc. Thesis, Swedish University of Agrarian Sciences, Department of Obstetrie and Gynaecology Veterinary Medicine Faculty, Uppsala, Sweden, 90 PP. Sumar, J., 1985a. Reproductive physiology in South American camelids. In: R.B. Land and D.W. Robinson (Editors), Genetics of Reproduction in Sheep. Butterwotths, London, pp. 81-95. Sumar, J., 1985b. Algunos aspectos obstétricos de la alpaca. Bol. Téc. No. 2, IVITA, Univ. Nac. M.S. Marcos, Convenio CIID-Canada, 16 pp. Sumar, J., 1991. Contribution of the radioimmunoassay technique to knowledge of the mproductive physiology of South American camelids. In: Isotope and Related Techniques in Animal Production and Health. FAO/IAEA, Vienna, Austria, pp. 353-379. Sumar, J. and Franco, E., 1974. Ensayos de Transferencia de Embriones en Camelidos Suidamericanos. In: Informe Final (IVITAJ, Univ. N.M. San Marcos, Lima, Peru.
J.B. Sumar/Animal
Reproduction Science 42 (19%)
405-415
41.5
Sumar, J. and Garcia, M., 1986. Fisiologia de la reproduccion de la alpaca. In: Nuclear and Related Techniques in Animal Pmduction and Health. IAEA, Vienna, pp. 149-177. Sumar, J. and Le.yva, V., 1979. Relación entm la ubicación del Cuerpo luteo y la localización del embrión en la llama (Lama glamo). Anales 111Conv. Int. Sobre Camélidos Sudamericanos, Viedma, Argentina. Sumar, J. and Leyva, V., 1981. Coleccion de Semen mediante Vagina Aftïcial en la Alpaca (Lama patos). In: IV Convencion Intemacional Sobre Camelidos Sudamericanos, 22-27 November, Corporacion Nacional Forestal e Instituto de la Patagonia, Punta Arenas, Cbile. Sumar, J., Novoa, C. and Femandez-Baca, S., 1972. Fisiologia reproductiva post-parto en la alpaca Rev. Inv. Pet. (IVITA), Univ. N.M. San Marcos, 1: 21-27. Sumar, J., Smith, G.W., Mayhua, E. and Nathanielsz, P.W., 1978. Adrenocortical function in the fetal and new bom alpaca. Comp. Biochem. Physiol., 59A: 79-84. Sumar, J., Fredriksson, G., Alarcon, V., Kindahl, H. and Edqvist, L.E., 1988. Levels of 15keto-13,14-dihydro-PGF2a, progesterone and oestradiol-17B, after induced ovulations in llamas and alpaca. Acts Vet. Stand., 29: 339-346. Sumar, J., Alarcón, V. and Echevarrla, L., 1993a. Niveles de progesterona periférica en alpaca llamas y su aplicación en el diagnóstico precoz de gestación y otros usos clínicos. Acts Andina, 2: 161-167. Sumar, J., Bravo, P.W. and Foote, W.C., 1993b. Sexual receptivity and time of ovulation in alpacas. Smal1 Rumin. Res., 11: 143-150. Wiepz, D.W. and Chapman, R.J., 1985. Non-surgical embryo transfer and live birth in a Ilama. In: Johnsson (Editor), Llama Medicine Workshop for Veterinarians.