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Animal Reproduction Science 58 2000.



A review on reproduction in South American

Bruce W. Brown )
CSIRO, Animal Production, Locked Bag 1, Deliery Centre, Blacktown, NSW 2148, Australia
Received 11 May 1999; received in revised form 12 October 1999; accepted 12 October 1999

In this paper, aspects of reproductive physiology and endocrinology, as well as sexual
behaviour in South American camelids are reviewed. Because of the many unique features of
reproduction in these animals, the application of advanced breeding techniques that are routinely
used in other domestic species has been slow and, in some cases, are not applicable. Relatively
high embryonic loss and the capacity to carry only one offspring at a time limit production in
females. Furthermore, some 20% of females do not conceive following mating. Research is
needed to elucidate the causes of embryonic loss, particularly in relation to the preferential
location of embryos in the left uterine horn and the apparent differential luteolytic activity of the
two uterine horns. A fuller understanding of the endocrine changes and mechanisms accompanying folliculogenesis, estrus, induction of ovulation and luteal regression may led to treatments that
provide better control of ovulation and enhance the quality and viability of eggs shed. In the male,
the hormonal interactions involved in facilitating libido need to be established and the underlying
causes of declining libido resulting from continued exposure to estrous females, identified. More
importantly, there is a need to develop a routine method to collect semen from animals on farm, or
in studs. Deficiencies in this area have long hampered the evaluation of sires through proper
assessment of their semen quality and in the application of artificial insemination. In addition,
establishment of techniques to freeze semen from these species has obvious advantages for
breeding, including crossbreeding between species to improve products such as fibre and to assist
in preservation of some of the more endangered New World camelids. q 2000 Elsevier Science
B.V. All rights reserved.
Keywords: Alpaca; Llama; Camelids

Tel.: q61-2-9840-2744; fax: q61-2-9840-2940.

E-mail address: B.W. Brown..

0378-4320r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 3 7 8 - 4 3 2 0 9 9 . 0 0 0 8 1 - 0


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

1. Introduction
Over the past 1015 years, there has been an increase in the commercial rearing of
South American camelids in Australia, New Zealand, Europe and the USA for the
companion animal industry, as well as for the production of high quality fibre. This has
drawn attention to the need for efficient reproduction and the development of breeding
techniques to ensure profitable enterprises and maximise opportunities for genetic
selection. However, alpacas and llamas have unique reproductive characteristics, which
are often the cause of their poor breeding performance compared with other conventional domestic species. Camelids of both sexes are necessarily older at time of first
breeding, the gestation period is relatively long compared to that for other small
ruminant species and generally, only singleton offspring are born twins are rare.
Accordingly, genetic gain through conventional breeding is slow.
Assisted reproductive technologies that are now routinely used in other domestic
livestock species, particularly ruminants, have the potential to increase the rate of
genetic improvement in South American camelids. For instance, the export of frozen
semen and embryos internationally has obvious advantages in reducing costs and
eliminating health problems associated with the transport and quarantine of live animals.
However, techniques such as multiple ovulation and embryo transfer MOET., juvenile
in vitro embryo transfer JIVET., semen collection, artificial insemination AI., and
cryopreservation of embryos and the gametes, have not been developed for routine use
in camelids. Therefore, an understanding of these unique reproductive features is
essential for normal breeding management of camelids, as well as developing technologies to improve breeding performance. The purpose of this paper is to review the
scientific advances that have furthered our understanding of reproductive physiology and
endocrinology in small camelids, particularly alpacas and llamas, and to discuss these
findings in the context of methodologies needed to facilitate improved commercial
breeding practices.

2. Evolutionary and environmental background

The fossil record indicates that the ancestor of the family Camelidae originated in the
Great Plains of western North America 911 million years ago and eventually became
extinct there during the Ice Age. About 3 million years ago toward the end of the
Tertiary period, one branch Camelus . of this family migrated across land bridges at the
Bering Straits into Eurasia, to give rise to the present day camels of Africa and Central
Asia. The other branch reached South America much later in the Ice Age Pleistocene
Epoch. and gave rise there to the present day Lama species about 2 million years ago
Wheeler, 1995..
Camelids are ruminants and belong to the mammalian order, Artiodactyla or even-toed
ungulates, also known as cloven-hoofed animals. It is generally accepted that the family

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Camelidae consists of two genera. The Old World Genus or Camelus includes the
Arabian Camelus dromedarius or one-humped. and the Bactrian Camelus bactrianus
or two-humped. camels. The New World Genus Lama comprises the domesticated
Lama pacos or alpaca and Lama glama or llama, as well as two wild species Lama
icugna or vicuna
and Lama guanicoe or guanaco. However, recent molecular analyses
based on mtDNA sequence Stanley et al., 1994. support a divergence of at least 2
million years between vicuna
and guanaco, and therefore suggests that vicuna
is a
separate genus, classified as Vicugna icugna. According to Wheeler 1995., the
domesticated alpaca and llama developed from the wild types vicuna
and guanaco,
respectively. All four species possess 37 pairs of chromosomes Taylor et al., 1968..
It is not known exactly when alpacas and llamas were domesticated but osteological
remains from Andean archaeological sites suggests that it occurred for both species
around 6000 years ago Wheeler, 1995.. Certainly, there is evidence of llama and alpaca
rearing on coastal sites in northern and southern Peru, respectively, 900 to 1400 years
ago and the Incas were already breeding these animals for wool at the time of the
Spanish conquest. The Incas used llamas primarily as pack animals but they also used
their wool and pelts, and their dung for fuel and fertilizer. The surefootedness of the
llama in rough country and its ability to adapt to high altitudes and survive well on
unimproved pastures made this animal a valuable resource to the Indians. Alpacas on the
other hand were mainly raised for their cashmere-like fibre and both species were also
used for meat. It is thought that the extensive crossbreeding between llamas and alpacas
since the Spanish conquest has played an important role in coarsening the wool
compared to that of the preconquest animals. Samples of fine fibre, and extra fine fibre,
obtained from preconquest alpaca breeds found among 1000 year old El Yaral mummies, had mean "SD. fibre diameters of 23.6 "1.9. and 17.9 "1.0. mm, respectively Wheeler, 1995.. In Australia, it is estimated that 80% of alpaca fleeces have
mean fibre diameters between 25 and 30 mm. However, through selection over the last
few years, the Australian Alpaca industry has achieved mean fibre diameters below 20
mm in some animals.
In South America, more than 90% of the alpacas and llamas are found in Peru and
Bolivia in similar numbers 3.06 and 3.30 million, respectively, in 1995.. There are
fewer vicunas
125,400. and guanacos 605,000., the latter species being found mostly
in Argentina Fernandez-Baca, 1995.. Chile and Ecuador contain small numbers of the
four species. The South American camelids at present mostly inhabit high altitude
environments of the Andean highlands though not exclusively so., in treeless pastoral
zones called altiplano. Evidently, the Suri one phenotype of alpaca. is not as well
adapted to altitudes higher than 4200 m above sea level as is the Huacaya phenotype,
since at these altitudes, they show decreased reproductive efficiency and experience
higher new-born mortality compared to the latter breed Fernandez-Baca, 1995.. The
reduced reproductive performance may account for the marked decline in the number of
Suris in Peru over the last 30 years, from about 22% to less than 5% of the total alpaca
population. Annual rainfall in these high altitude areas varies between 250 and 500 mm,
and occurs mostly from December to April Sumar, 1985.. In addition to the two
well-defined phenotypes of alpacas mentioned above the Huacaya is the type mostly
imported into Australia., there are two breeds of llamas known as the Kara and the


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

Chaku. The current number of alpacas in Australia is estimated at 20,000, which

produce around 40 tons of fleece annually Davison, 1998..
Camelids differ from other Artiodactyls by the possession of nail-covered sole pads
on the feet rather than hoofs. This feature places them in the suborder, Tylopoda. The
feet of the alpaca are quite sensitive and, traditionally, they prefer soft moist ground
with tender grasses and pools in which they like to wallow. Other differences include the
absence of horns or antlers, a split upper lip and long curved necks. Unlike horses and
cattle, there is a lack of tensor skin between the thigh and the body so that the legs of
camelids appear to be very long. Camelids also have no gall bladder and are unique
among mammals in that they have elliptical blood corpuscles Schalm, 1967..

3. Puberty
Young males may show sexual interest in females at 1 year of age but are incapable
of mating because the penis adheres to the prepuce from birth and is not completely
liberated until puberty is reached. This anatomical change is essentially an androgen-induced phenomenon influenced by the plane of nutrition Fernandez-Baca,
1993; Sumar,

1996., as is the case with other ruminants Brown, 1994.. Thus, the increasing amounts
of testosterone produced from the testes as the animal matures not only facilitate
development of secondary sexual characteristics, but allows the animal to grow and put
on body condition. At 1 year of age, only 8% of male alpacas have penile separation
from the adhesions while at 2 years of age when the body weight reaches about 50 kg,
70% of the males are capable of intromission Sumar, 1985.. At 3 years, all males are
without penile adhesions. Though male alpacas do not reach full maturity until 5 years
of age, it is common practice to use them for mating from 3 years of age. Pollard et al.
1995. found no evidence that sexually inexperienced males were behaviourally less
efficient as sires than experienced males. However, they found individual variation in
the level of libido between sires, as assessed from the number of females mated. It has
been reported that during periods of intense sexual activity, particularly at the beginning
of the breeding season, alpacas can mate up to 18 times per day Sumar, 1985..
Obviously, early separation of the penis from the prepuce is a desirable genetic trait in
yearlings Sumar, 1985. and therefore should be an important selection consideration,
together with large testis size Sumar, 1996. which is assumed to be directly related to
sperm production, as in other ruminants Brown, 1994..
In small camelids, there appear to be no detailed studies on morphological, functional
or endocrine changes in the ovary, in association with onset of puberty. The majority of
female alpacas are sexually receptive at 1214 months of age, even though ovarian
activity commences earlier at 10 months with the growth of ovarian follicles 5 mm in
diameter or greater Novoa, 1970; Sumar, 1985.. Though onset of puberty is affected by
environmental conditions, it is also greatly influenced by nutritional status; apparently
the attainment of 60% of adult body weight, or about 33 kg, is required for onset of
puberty Sumar, 1985; Smith et al., 1994.. Additionally, there seems to be a relationship
between body weight at mating and subsequent birth rate. For each kg gain in body

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


weight, there was found to be a 5% increase in parturition rate, but above 33 kg

pregnancy rate was independent of body weight Leyva and Sumar, 1981.. Under
conditions of good nutrition, a body weight of 33 kg is achievable for most yearlings
Sumar, 1985.. However, in the poorer pastoral environments of Peru, female alpacas do
not mature as fast and generally are not bred until they are 2 years of age. It is also
common practice to breed female llamas from 2 years of age and while female vicunas

show sexual receptivity at 1 year of age, the fertility of yearlings in the wild is reported
to be low Koford, 1957..

4. Reproductive season
There are conflicting reports on the breeding season of alpacas and llamas; accounts
seem to vary depending on the environment and management system under which they
are kept. In their natural habitat in the highlands of South America, breeding for all four
species of camelids appears to be seasonal and is confined to the warmer, rainy months
from November to April when there is ample forage Koford, 1957; San-Martin et al.,
1968; Franklin, 1983; Sumar, 1985.. On farms in Peru where management practice
allows male and female alpacas to run together all year, lambing occurs from December
to March, indicating a peak in breeding during the previous January to April. Where the
sexes are maintained in separate herds, breeding is timed to take place during January to
March, so that parturition occurs at the most favourable time of year in January to April

The continued presence of males with females can have an inhibitory effect on sexual
activity of the males and, indeed, can cause their libido to disappear altogether Sumar,
1985, 1996.. Remarkably, however, sexual activity in these males is almost immediately
resumed if they are introduced to a new herd of females Fernandez-Baca
et al., 1972b..

When males and females are kept separately and allowed to copulate at infrequent
occasions e.g., once a month., both sexes are sexually active for the whole year Sumar,
1985. and the females may give birth at any time of the year San-Martin et al., 1968..
Time of year at breeding appears to have little or no effect on ovulation rate, fertilisation
rate or embryo survival Fernandez-Baca
et al., 1972a., though Pollard et al. 1995.

observed that female alpacas in New Zealand seemed less receptive and mating time
was shortened in the spring. Camelids of both the domestic and wild types kept in
captivity in different parts of the world are also capable of year-round breeding Brown,
1936; Zuckermann, 1952r1953; Schmidt, 1973; Sumar, 1985. though llamas in North
America still seem to have a summer peak in fertility Johnston, 1988.. During the
breeding season and in the absence of males, females remain in heat for periods
extending for up to 36 days, with only occasional periods of anestrus lasting no longer
than 48 h San-Martin et al., 1968.. Factors controlling onset of sexual activity under
conditions of natural breeding, or the inhibitory effect on male libido resulting from
continued exposure to females, are not known. However, aside from managerial and
nutritional effects, environmental factors such as temperature, humidity and light, as
well as visual or olfactory cues, are likely to influence the central nervous system
centres controlling reproductive behaviour.


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

5. Reproductive anatomy and physiology

The anatomy of the reproductive organs in male and female South American
camelids has been reviewed extensively Smith, 1985; Sumar, 1985; Adams et al., 1989;
Fowler, 1989; Smith et al., 1994. and only needs to be briefly considered here.
5.1. Males
5.1.1. Reproductie organs
The two testicles are held in a non-pendulous scrotum situated below the anus. The
scrotum, which is similar in nature to the sub-anal protuberance found in swine, rodents
and carnivores Smith, 1985., maintains the testicles and the contained spermatozoa. at
a temperature slightly lower than body core temperature. The average weight of the fully
developed testicle is about 15 g, but there is considerable variation between animals in
the size of the testicles and in the relationship between testis size and body weight
Sumar, 1985.. Normally, in the adult, both testes are of the same size and firm but not
hard and move freely within the scrotum. The epididymis is small and conspicuous; the
deferent duct is thin at its beginning but thickens when it reaches the abdominal cavity.
The total length of the deferent duct is about 40 cm. It ends near the bladder but not in a
characteristic ampulla deferens as in other species Sumar, 1985.. The prostate is
H-shaped and lies at the neck of the bladder, and the bulbourethral glands, which are
oval in shape, are located on both sides of the urethra at the pelvic outlet. There are no
seminal vesicles in South American camelids Smith, 1985; Sumar, 1985..
The penis is fibroelastic in type and is not dependent upon vascularisation or
frictional stimulation for copulation. At its end, the firm cartilaginous projection is
formed in a curved hook that bends clockwise and has a small urethral process of
approximately 1 cm in length Sumar, 1985.. The cartilaginous tip may be an adaptation
to facilitate penetration of the penis through the cervix Fowler, 1989. during copulation.
As mentioned earlier, the penis of immature alpacas adheres to the prepuce until
puberty. In the adult, the erect penis, which protrudes through the prepuce, is about
3540 cm long and the sigmoid flexure is post-scrotal Sumar, 1985.. The prepuce is
relatively small, and in unaroused males it is normally directed backwards causing the
male to urinate between his legs.
5.1.2. Collection of semen
The lack of suitable techniques for the collection of semen, due mostly to the peculiar
posture adopted by the animals during mating, as well as the duration of copulation
1050 min., has inhibited studies on seminal characteristics and the use of AI in small
camelids. Several methods to collect ejaculates have been tried without much success of
development as a routine procedure. These include the use of artificial vaginal sleeves
Mogrovejo, 1952., intravaginal pessaries or sacs San-Martin et al., 1968., electroejaculation Fernandez-Baca,
1993., and the use of an artificial vagina AV. mounted

inside a dummy Sumar and Garcia, 1986; Lichtenwalner et al., 1996; Bravo et al.,
1997.. Not surprisingly, the first two methods produced variable ejaculate volumes

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


ranging from 0.4 to 6.6 ml Sumar, 1985., which undoubtedly was due to the methods
themselves interfering with normal copulation including penile penetration of the cervix
and causing premature withdrawal from the condom. Electro-ejaculation requires sedation of the animals and the exact voltage, pulse frequency and duration of electrical
stimulation have not been properly established Fowler, 1989.. This method results in
frequent contamination of the semen with urine and huge variation in sperm concentrations that fluctuated from 1000 to 255,000 sperm mly1 Sumar, 1985; Fernandez-Baca,

A more promising method of semen collection utilizes an AV with a built-in
simulated cervix, which is either mounted inside a dummy Sumar, 1996; Sumar and
Leyva, 1981; Bravo et al., 1997. or fitted over the hindquarters of recumbent females
Lichtenwalner et al., 1996.. The disadvantage with this approach is that the males have
to be trained to use this device and the method is not as effective as AV collection of
semen in rams. The initial use of this procedure in alpacas provided ejaculates of up to
12.5 ml, with sperm concentrations up to 600 = 10 3 sperm mly1 Sumar and Garcia,
1986.. However, recent studies in alpacas using this method reported much smaller
semen volumes varying from 0.4 to 4.3 ml Garnica et al., 1993. and 0.8 to 3.1 ml
Bravo et al., 1997. which were collected after copulation times ranging from 14 to 36
min. Such collections contained sperm concentrations varying from 82250 = 10 3
sperm mly1 . In llamas, the mean volume of semen per collection, after 26 collections,
was 3.0 ml with some as large as 10.6 ml., the average copulation time was 31.7 min
and the concentration of spermatozoa was 1 = 10 6 sperm mly1 Lichtenwalner et al.,
1996.. In contrast, the sperm concentrations in ejaculates from rams and bulls are many
fold greater, ranging from 2000 to 6000 = 10 6 sperm mly1 and 15002500 = 10 6
sperm mly1 , respectively Salamon, 1976.. Moreover, in sheep, the minimum number of
spermatozoa required for acceptable conception rates in flocks is estimated to be around
120125 = 10 6 for fresh semen delivered via the cervix Salamon, 1962. or about
20 = 10 6 for intra-uterine insemination with frozenrthawed semen Maxwell et al.,
1984.. In small camelids, the spermatozoa concentration of inseminates required for
successful fertilization and establishment of pregnancy is not known. In a study on AI in
alpacas Bravo et al., 1997. which resulted in an overall pregnancy rate of 69.2% see
later section on AI., neither the volume of the undiluted semen used, nor the sperm
concentration in the inseminate doses, was reported. If the volumes of ejaculates
collected by AV and their spermatozoan concentrations cited above is representative of
ejaculates after natural mating, then clearly small camelids require much less spermatozoa for fertilization than do other domestic ruminants. Thus, intra-cornual deposition of
semen during copulation may be an adaptation to overcome the relatively low sperm
concentrations in ejaculates in these species.
Semen from llamas collected by electro-ejaculation has been diluted in a Tris
glycerolegg yolk extender at a ratio of 1:8 and successfully frozen in pellets Graham
et al., 1978..
5.1.3. Seminal characteristics and spermatogenesis
The semen of alpacas and llamas is highly viscous and forms a coagulum soon after
copulation Lichtenwalner et al., 1996; Bravo et al., 1997., which presents difficulties in


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separating sperm cells from seminal plasma by conventional methods to assess sperm
concentrations. Moreover, the high viscosity results in oscillatory movement of the
spermatozoa Sumar and Garcia, 1986; Garnica et al., 1993; Bravo et al., 1997. and not
the progressive sperm motility as occurs in ejaculates from other domestic ruminants.
Since, in small camelids, semen is deposited intra-cornual for up to 2 days before
ovulation, the entrapment of spermatozoa in the coagulum in these species may act as a
type of sperm reservoir, fulfilling a similar physiological function to the so-called sperm
cervical reservoir in other domestic ruminants Mattner, 1966.. Furthermore, the high
viscosity of the semen may be important in maintaining the viability of sperm within the
uterus Mattner, 1969..
The time required for liquefaction of alpaca semen averaged 23 h range 848 h. and
the proportion of seminal plasma in the semen is 88.5% Garnica et al., 1993.. Over the
course of the comparatively long copulatory period average time 2025 min., experimental evidence suggests that ejaculation is continuous, without fractions and with a
reasonably uniform semen quality from beginning to end Sumar, 1985; Lichtenwalner
et al., 1996.. The semen of alpacas is described as milky white in colour and has a mean
pH of 7.2 Garnica et al., 1993; Bravo et al., 1997., whilst that of the llama has a mean
pH of 8.1 Lichtenwalner et al., 1996.. The concentrations of chloride, calcium,
inorganic phosphate, phospholipids, total nitrogen, total protein and albumin were found
to be in close agreement with those of other species Garnica et al., 1993.. In alpaca
semen, the proportions of live, and of morphologically normal, spermatozoa range from
58% to 83% and 71% to 84%, respectively Bravo et al., 1997., and are lower than these
parameters in ram semen Brown et al., 1990.. The morphological abnormalities in
alpaca semen included abnormalities of the tail such as bent and double tails accounting
for 915%., tailless heads and double heads 313%. and the presence of cytoplasmic
droplets on 17% of the spermatozoa. In llamas, the seminal abnormalities were even
higher, with a third of the reported 60% abnormal spermatozoa in the collections having
abnormalities associated with the head Lichtenwalner et al., 1996.. Other abnormalities
included bent or coiled tails mean 6.6%., the presence of cytoplasmic droplets 11%.
and abnormal acrosomes 13%..
Histological studies of the alpaca testis Montalvo et al., 1979. have shown that a
lumen appears in the seminiferous tubules at 12 months of age and the first observable
spermatozoa and Leydig cells occur soon after, at 15 to 18 months of age. It is estimated
that the mean "SD. diameter of the seminiferous tubules in adult llamas is 223.07 "
19.8 mm Delhon and von Lawzewitsch, 1987.. Adopting the criteria used by Ortavant
1959. for the ram, these latter workers described 8-cell associations or stages. in the
llama to define a complete cycle of the seminiferous epithelium, as well as 12
spermiogenic steps. The features included the shape and distribution of the germ cell
nuclei, the location of the spermatids, the presence of mitotic figures and the release of
spermatozoa from the tubular wall. In accord with many other mammals, each cross-section of the seminiferous tubule in this species showed one stage of the cycle, except
where a transitional zone between successive stages occurred. Type A spermatogonia
were present at all stages of the cycle. Type B spermatogonia occurred at later stages 6
and 7. and also in stage 8, together with preleptotene spermatocytes, which appeared
just before the complete release of spermatozoa into the lumen.

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The interstitial tissue of the llama testis comprises blood vessels, lymphatic vessels,
connective elements and Leydig cells. The capillaries which are not abundant. and
lymphatic vessels are sometimes found in close association with surrounding interstitial
cells. The presence of lymphatic vessels and connective tissue resembles the structure
found in the ram and bull interstitium, but the volume of the interstitial cells is larger
than in those species.
5.2. Females
5.2.1. Reproductie organs
Ovarian, oviducal and uterine connections are similar to those in other domestic
species. The ovaries are of a globular irregular shape and have been likened to those of
the sow, and contain numerous follicles on the surface. In alpacas, ovarian follicles of
between 5 and 12 mm in diameter are considered normal and any larger follicles are
considered to be pathological Sumar, 1985.. In llamas, follicles range in diameter from
small 3 mm structures arranged around the periphery of the ovary, to follicles of
pre-ovulatory size 716 mm, mean 10.6 mm in diameter. that protruded from the
surface of the ovary Adams et al., 1989.. Folliculogenesis is complete around 10
months of age but the young females generally are not receptive to males until about
1214 months of age see section on Puberty above..
The uterus of alpacas and llamas is bicornual with the two uterine horns separated by
a septum. The tips of the uterine horns are blunt and rounded, with the sides of the
uterus attached to the abdominal and pelvic walls by broad ligaments. The uterine
mucosa consists of a columnar epithelial layer and dense fibrous tissue of the submucosa
which contains small uterine glands Fowler, 1989.. The cervix has two to three spiral
folds that turn to give the appearance of there being two or three rings Smith et al.,
1994.. Its epithelial layer consists of cuboidal cells and there are no glands in the
cervical submucosa. The isthmus of the oviduct acts as a sphincter to prevent any
retrograde movement of fluids from the uterus into the oviduct, though solutions can be
readily flushed through this structure in the opposite direction Sumar, 1985.. The
vagina in the alpaca varies in length from 13 to 15 cm and in diameter from 3.5 to 5 cm
Sumar, 1985; Fowler, 1989..
5.2.2. Estrus, oulation and luteal function
Unlike most domestic species, female camelids are not polyestrus i.e., exhibit
regular distinct periods of heat or sexual receptivity after which ovulation occurs
spontaneously. but rather are induced ovulators San-Martin et al., 1968, England et al.,
1969.. Non-pregnant females llamas and alpacas display prolonged periods of behavioural estrus assessed from twice daily checks., extending for up to 36 days after
first introduction of the males San-Martin et al., 1968; England et al., 1971. and even
up to 90 days in some animals England et al., 1971.. These periods of receptivity are
interrupted by very brief episodes of anestrus lasting no longer than about 48 h
San-Martin et al., 1968.. The intensity of estrus the time taken for a female to assume
the prone mating position, where the most intense estrus is equated to the shortest time.
reduces in response to increasing duration of previous exposure to males, and to


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advancement of season England et al., 1971.. Small camelids have the capacity to breed
all year round see earlier section on Reproductive season..
Ovulation in camelids is induced by penile penetration of the vagina and cervix, and
not from mere mounting of the females by males Fernandez-Baca et al., 1970c.. Also, it
is not related to duration of copulation, which can take from 1050 min. Ovulation is
reported to occasionally occur spontaneously at the height of the breeding season in
about 5% of llamas England et al., 1969, 1971. and alpacas Fernandez-Baca et al.,
1970c; Bravo and Sumar, 1989.. However, there is some doubt as to whether all of these
females were totally deprived of visual, olfactory and auditory cues associated with the
presence of nearby males Fernandez-Baca,
1993.. Ovulation can also be induced in

alpacas and llamas by treatment with gonadotrophic hormones see later section on
Assisted reproductive technologies..
Estimates of time of ovulation after copulation range from 26 to 42 h San-Martin et
al., 1968; England et al., 1969; Novoa, 1970. but more frequent assessment with
ultrasound examinations revealed that 96% of llamas ovulated on the second day after
mating Adams et al., 1989, 1990.. Some females can mate again up to 24 h after the
first joining. Generally, only one egg is shed at each ovulation; multiple ovulations are
reported to occur in 10% of females after natural mating. That the occurrence of
ovulation following copulation is influenced by the size of ovarian follicles may explain
why up to 20% of females fail to ovulate after single or multiple services by intact or
vasectomized males. Bravo et al. 1991. found in alpacas and llamas that ovulation did
not occur in any of the females with ovarian follicles - 7.0 mm in diameter at the time
of copulation. Ovulation did occur when the follicles were G 7.0 mm in diameter. When
regressing follicles were present at the time of mating, luteinization of these structures,
and not ovulation, occurred Bravo et al., 1991.. In these instances, the luteinized
follicles survived for about 5 days and delayed the development of a new dominant
follicle for 5 to 7 days Bravo et al., 1991.. Thus, in adult camelids, it seems that while
the incidence of behavioural estrus is independent of follicular development, the
induction of ovulation that results in normal luteal function is not.
Luteal growth and regression in non-pregnant females have been described for both
llamas and alpacas by several workers England et al., 1969, 1971; Fernandez-Baca et
al., 1970a; Adam et al., 1989, Adams et al., 1991; Bravo et al., 1991.. Apparent
differences in duration of luteal function seem to relate to variation in the interval
between copulation and ovulation, and which of these events is used as the starting
point. There is also some suggestion that corpora lutea on the right ovary undergo more
rapid regression than those on the left ovary and this may relate to the predominantly
local luteolytic action of the right uterine horn see section below on Reproductive
endocrine changes in non-pregnant camelids.. Accordingly, the following is a summary
of luteal development and subsequent regression in alpacas and llamas, where Day 0 is
the day of ovulation. A corpus luteum CL. is detectable by laparotomy or ultrasonography. on Day 3 and it attains maximum size by Days 810. Significant reduction in CL
diameter and plasma progesterone concentrations is evident in llamas around Day 10,
and by Day 12 in alpacas. Complete regression of the CL occurs by Day 18 in both
species. During the time of luteal function, there is a suppressive effect on follicular
growth and the females generally are non-receptive to the males until follicular growth

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recommences Bravo et al., 1991.. For changes in progesterone concentration see below
Reproductive endocrine changes in non-pregnant camelids.
5.2.3. Growth and regression of oarian follicles
Several studies using a variety of methodologies such as laparoscopy, ultrasonography and assay of hormones in plasma and urine Adams et al., 1989, 1990; Bravo and
Sumar, 1989; Bravo et al., 1990a. have revealed overlapping, wave-like patterns of
follicular growth in the ovaries of alpacas and llamas. The ovary bearing the dominant
follicle generally alternates between successive waves of follicular growth in the
majority of cases England et al., 1969; Fernandez-Baca et al., 1970c; Bravo and Sumar,
1989.. For convenience, the pattern of change in follicular growth has been described in
three stages growth, maturation including the period of dominance. and regression
or atresia. It has been estimated that in llamas the interval for the development of
consecutive follicles that reach 8.0 mm in diameter i.e., a size capable of ovulating. is
1112 days Bravo et al., 1990a..
Follicular development in the contralateral ovary begins either late in the maturation
phase or during early atresia of follicles in the opposite ovary. Evidently, follicles must
reach a diameter of about 4.06.0 mm before the female is receptive to the male Bravo
and Sumar, 1989; Bravo et al., 1991.. Generally, two or three follicles are recruited to
develop during the initial phase of growth but only one and sometimes two in about
10% of the animals. ultimately reaches ovulatory size, assessed to be ) 7.0 mm in
diameter Adams et al., 1989; Bravo et al., 1990a.. The selected follicle appears to exert
its dominance i.e., suppresses additional follicular development. over all other follicles
in both ovaries for as long as it maintains its mature size, which is estimated to be about
5 days Bravo et al., 1990a.. Possibly, this suppression of follicular development is due
to inhibition of neural centres involved in gonadotrophin secretion, by locally produced
ovarian androgen andror inhibin. Such a mechanism has been proposed to explain this
phenomena in other species Louvet et al., 1975; Scaramuzzi et al., 1977; Moore et al.,
1978; Tsonis et al., 1983.. If mating does not take place, the dominant follicle regresses
within 35 days and a new wave of follicles commence their rapid growth phase in as
short a time as one day of incipient atresia in the previous dominant follicle. A new
follicle can become dominant within 23 days Bravo, 1994; Bravo et al., 1990a..
5.2.4. Reproductie endocrine changes in non-pregnant camelids
Camelids are unique in that there appear to be no periods of behavioural estrus that
are associated with distinct episodes or surges in estradiol activity, as occurs in
spontaneously ovulating animals such as sheep and cattle, or in some induced ovulators
such as the rabbit. It could be argued that in camelids the rapid replacement rate of
dominant follicles that prevail for relatively long periods of time is likely to ensure
almost uninterrupted levels of estrogen that facilitates continuous receptivity to males.
However, in a study on unmated adult llamas over a 30- to 50-day period Bravo et al.,
1990a., plasma estradiol concentrations were not found to be uniformly high but rather
the hormone was secreted in pulses lasting 45 days and which peaked at concentrations
of 1012 pg mly1 . These pulses were concomitant with the patterns of growth and
regression of large follicles and they appeared to be separated by periods as short as 12


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

days, ranging up to 10 days, when concentrations of the hormone were at the minimal
detectable limits of the assay 6 pg mly1 .. From the few studies on endocrine changes
occurring at copulation Sumar et al., 1988; Bravo et al., 1990b., it is clear that the
concentration of estradiol at this time is already elevated to levels 1020 pg mly1 .
equivalent to the peak values produced in association with large follicle development.
Thus, it is possible that the episodic release of estradiol is sufficient to maintain a
continued sensitization of the neural centres controlling sexual behaviour, provided that
the periods between successive peaks are not extensive perhaps 12 days.. Hence, the
brief periods of anestrus that occur in non-pregnant females may be explained by
occasional asynchrony between successive waves of follicular growth, such that the
initiation of a new follicle growth wave, and its associated estradiol production, is
delayed long enough for desensitization of the neural centres to occur. This is likely to
be the situation, for instance, following the regression of a luteinized follicle.
No temporal relationship was found between gonadotrophin secretion and follicular
development and, not surprisingly, the peaks of estradiol associated with peaks in
follicular growth do not elicit a preovulatory surge of luteinizing hormone LH. Bravo
et al., 1990a.. Following copulation, the elevated level of estradiol remains essentially
unchanged for the next 18 h at least and does not decrease markedly until about 22 to 48
h Bravo et al., 1990b.. The pattern of LH release in llamas and alpacas is similar to that
occurring in other induced ovulators and is initiated in response to copulatory stimulation. Plasma LH concentrations rise markedly within 15 min of initiation of copulation,
followed by a preovulatory LH surge which peaks by 2 h England et al., 1969; Bravo et
al., 1990b, 1991.. The circulating levels of this hormone then decline over a 56-h
period, to reach basal levels by 7 h Bravo et al., 1990b.. Subsequent matings within 24
h of the initial mating. do not appear to stimulate further LH release Bravo et al., 1992..
The influence of follicle size on ovulation referred to above. may be related to their
ability to secrete sufficient estrogen to sensitise the hypothalamo-pituitary system to
produce LH in response to copulation., in amounts adequate to cause ovulation Bravo
et al., 1991.. Indeed, a positive correlation exists between follicle size and estrogen
concentrations Bravo et al., 1990a.. When small ovarian follicles 45 mm. are present
at the time of mating, the amount of LH released is insufficient to induce ovulation and
is quantitatively far less than that produced by females with larger follicles 612 mm.
that do experience ovulation. On the other hand, when regressing follicles are present at
the time of mating, the amount of LH released is similar to that in females with growing
or mature follicles, but luteinization results and not ovulation. Interestingly, the amount
of LH released in llamas is reputedly greater than that in alpacas with comparable sized
follicles Bravo et al., 1991.. Unlike LH, follicle stimulating hormone FSH. concentrations in either species is evidently unaffected by copulation and is unrelated to follicle
size, albeit that the levels mean 0.96 ng mly1 . of this hormone fluctuate throughout
follicle growth cycles Bravo et al., 1990a, 1991..
When ovulation occurs without subsequent conception, the functional CL secretes
measurable progesterone from about Day 4, and this steadily increases in concentration
until about Day 810 after ovulation Adam et al., 1989.. Bravo et al. 1991. reported
that CL appear to develop faster in llamas than in alpacas, based on luteal size and the
rate of increase in progesterone concentrations. Regression of the CL in non-pregnant

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


females begins about Day 1012, in association with pulsatile release of prostaglandin
measured as the main metabolite 15-keto-13, 14-dihydro-PGF2 a . and this suggests that
in llamas and alpacas, prostaglandin is involved in luteal regression Sumar et al., 1988..
At this time, progesterone concentrations decline rapidly to reach basal levels by about
Day 1415 after ovulation Adam et al., 1989.. In the face of declining progesterone
concentrations, follicular growth recommences, resulting in a rise in estradiol secretion
and in the induction of estrus, which has been observed to re-occur as early as Day 12
Fernandez-Baca et al., 1970a.. As in other species such as sheep Brown et al., 1980.,
there is also a high correlation between luteal diameterrweight and progesterone
concentrations in both llamas and alpacas Fernandez-Baca et al., 1970a; Adams et al.,
There is some controversy as to whether pseudopregnancy occurs in camelids, as it
does in other induced ovulators, since there appears to be little scientific evidence to
support the occurrence of this state. The claim that pseudopregnancy occurred in one
third of alpacas during the breeding season following matings with intact males
San-Martin et al., 1968. was based on field observations of females, many of which did
not return to estrus, after their initial estrus, for the whole of the breeding season. In the
absence of any other information or data on these observations, it is distinctly possible
that these females suffered from some local environmental or nutritional problem that
either impaired normal ovarian function, or that was detrimental to pregnancy. In several
other studies in llamas and alpacas in which the incidence of pseudopregnancy was one
of the factors being investigated England et al., 1969; Fernandez-Baca et al., 1970a;
Adams et al., 1991., no evidence for this condition was found. In general, these findings
showed that following ovulation induced by either sterile matings or gonadotrophin
treatment, the resultant CL regressed, and the plasma progesterone concentrations were
low, by about Day 12. Indeed, it has been categorically stated by several workers that
pseudopregnancy is not known to occur in camelids Smith, 1985; Sumar, 1988;
1993.. Nevertheless, Adam et al., 1989. reported that in llamas mated

to an intact male, two of the females had elevated plasma progesterone concentrations
consistent with those in the pregnant animals, even though ultrasound scanning at about
Day 60 confirmed they were not pregnant. As the plasma progesterone levels in these
two females remained high for about 56 and 134 days, it was suggested that these
animals probably had persistent CL Adam et al., 1989..
It is interesting to note that, in alpacas at least, there appears to be a differential
luteolytic effect between the two uterine horns, as demonstrated in a study involving
partial hysterectomy Fernandez-Baca et al., 1979.. When the right uterine horn was
surgically removed in non-pregnant females with a CL on the right ovary, only a slight
delay in luteal regression resulted. However, when the left uterine horn was removed in
females with a CL on the left ovary, or one on each ovary, the CL on the left ovary
persisted and produced progesterone, whilst that on the right ovary regressed at the
expected time of luteolysis Fernandez-Baca et al., 1979.. These observations have led
to the conclusion that the luteolytic activity of the right uterine horn is only local in its
effect, whilst that of the left uterine horn acts both locally and systemically FernandezBaca et al., 1979; see Section 7.2.. It is equally curious that over 95% of successful
pregnancies in alpacas and llamas implant in the left uterine horn, even though 50% of


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

pregnancies are supported by a CL on the right ovary Fernandez-Baca et al., 1979..

Shalash and Nawito 1964. also reported that most pregnancies in dromedary camels
were in the left uterine horn. Thus, it seems that the two uterine horns in these species
have evolved differently in terms of maternal recognition, such that for the establishment
of a successful pregnancy with embryos emanating from the right uterine horn, they
must migrate into the left side of the uterus in order to prevent luteolysis see later
section on Placental development and embryonic loss..
Just as the release of endogenous prostaglandin is coincident with the initiation of
luteal regression, administration of analogues of prostaglandin to pregnant alpacas has
been shown to induce parturition Sumar et al., 1988.. If prostaglandin is the luteolysin
in these species and is produced in the uterine tissues as occurs in other animals, it is
difficult to explain how it can act systemically in view of the fact that this hormone is
largely metabolised in a single passage through the lungs Thorburn et al., 1972.. The
primary prostaglandins have a relatively short half-life in biological systems, ranging
from 3 to 10 min. This is due to either hydrolysis or enzymatic conversion to
prostaglandin metabolites, which lose the biological activity of the parent compound
Challis and Olson, 1988.. It has been demonstrated in sheep that prostaglandin secreted
into the uterine vein can cross into the closely adherent and tortuous ovarian artery via a
counter-current transfer mechanism existing between the two vessels Goding et al.,
1971r1972.. Such a mechanism accounts for the fast action of prostaglandin in exerting
its luteolytic effect on the CL in the ipsilateral ovary. Nevertheless, even if the ovarian
artery and uterine veins are in close apposition to each other in these species, about
which there is no published evidence, such a counter-current transfer mechanism does
not explain how prostaglandin produced in the left uterine horn can cause regression of a
CL in the right ovary. It seems unlikely that the uterus of small camelids have some
other vascular connections that enable interchange of venous blood between the two
sides of the uterus. With such a vascular arrangement, it would be expected that the
hormone secreted in either uterine horn would be equally effective in inducing luteolysis. Possibly, the left uterine horn produces some substance that can act systemically to
stimulate the conversion of arachidonic acid the precursor. to prostaglandins within the
ovary itself, to bring about local luteal regression. Bovine luteal cells contain arachidonic acid and in amounts larger than that in the endometrial tissue Lukaszewska and
Hansel, 1980.. However, it has also been suggested that this substance, and other highly
unsaturated long-chain fatty acids, may have direct luteolytic effects as a result of their
abilities to elevate intracellular calcium Hansel et al., 1991..

6. Mating behaviour
As previously mentioned, non-pregnant females are essentially in continuous estrus,
and when males are introduced to a herd they will attempt to mate with the first
receptive female they encounter. Courtship begins with the male actively pursuing
receptive females and attempting to mount them. According to England et al. 1971.,
courtships lasting longer than about 4 min usually result in no mating or forced mating.
However, the length of courtship may be influenced by the level of libido of individual

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males and, consequently, pursuit of a female by males of high libido may last for up to
10 min before the males give up Fowler, 1989.. On acceptance of a male, the female
takes a prone or seated position, resting on her brisket with her pelvis elevated and
permits the male to straddle her from behind. In this position, the head of the male is
above and slightly behind that of the female, his elbows hold her at the shoulders, and
his forefeet are on the ground Novoa, 1970.. Camelidae are the only ungulates to pair
in the recumbent position. On penetration of the vulva, the male manoeuvres his penis
into the vagina and through the cervix. Rather than the forceful pelvic thrusting
movements characteristic of rams, intromission in male camelids is achieved only after
considerable time is spent searching and probing with the penis, firstly around the
perineal area for the vulva and then in traversing the vagina and cervix. With mild
thrusting movements, semen is deposited directly into the uterine horns Franco et al.,
1981. and this may take from 1050 min, with an average time of 20 to 30 min
England et al., 1971; Sumar, 1985; Fernandez-Baca,
1993.. During copulation, the male

constantly vocalises, making a guttural sound called orgling whilst the female
remains relatively quiet. It has been suggested that the orgling sounds of the male
contribute to the neural response in the hypothalamus of the female to release gonadotrophin releasing hormone GnRH. Bravo, 1994.. Other receptive females may lie
down beside the mating pair and females in heat can also adopt mounting behaviour
San-Martin et al., 1968; Fernandez-Baca
et al., 1970c., though the latter does not

provide sufficient stimulus to induce ovulation Fernandez-Baca

et al., 1970c.. When

males and females are run together, it has been observed that some females can be
mated several times in 1 day for several days, particularly at the height of the breeding
season, while others may only be mated once San-Martin et al., 1968..
Mating practices adopted in alpaca breeding vary from paddock matings where males
are run with females at a rate of 610% San-Martin et al., 1968., to hand, individual
matings. With paddock matings, the males are generally kept separate from the females,
in an adjacent paddock, which has the effect of increasing their libido Moseley, 1995..
The intense sexual activity of both sexes during the first week of breeding can result in
over 70% of females being mated at least once Fernandez-Baca
and Novoa, 1968.. As

the sexual activity of males in breeding herds decreases with time as short as 3 days.
despite the presence of estrous females, the sires should be replaced with fresh males at
frequent intervals weekly. to maintain high levels of libido, coverage of the herd and
overall high fertility. This practice, referred to as the so-called male rotation system,
is now commonly in use in Southern Peru in herds greater than 100 animals. As a result
of this practice, birth rates of 5781% have been reported Novoa et al., 1970.. With
indoor-mating procedures, males can be maintained either at pasture in groups and
brought indoors for mating, or in individual stalls and the receptive females brought
indoors to them.
All four species of New World Camelids can and do interbreed to produce fertile
hybrids Gray, 1954.. The most common, the huarizo, results from male llama = female
alpaca cross and is bred to produce an economically valuable fleece; the reverse cross,
called the misti, is of no economic value. Crosses of male vicuna=
female alpaca
produce pacovicuna,
which have a finer but lighter fleece than the alpaca, though some
of the fineness is lost after the first shearing when the percentage of coarser hair


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increases. It is sometimes difficult to distinguish the hybrid offspring from the purebred
stock on phenotype alone Fernandez-Baca, 1995; Moseley, 1995; Wheeler, 1995..
Because the phenotypes are strictly not pure breeds, crosses between huacaya and
huacaya can produce a certain percentage of suri offspring and crosses between suri and
suri can produce some huacaya progeny Wheeler, 1995..

7. Pregnancy and parturition

The length of gestation in llamas and alpacas ranges from 342 to 350 days
San-Martin et al., 1968; Sumar, 1988; Leon et al., 1990.. Implantation is thought to
take place about 2022 days after breeding Bravo, 1994. and maintenance of the CL of
pregnancy is necessary throughout the entire pregnancy for the production of normal
offspring or cria.. This is based on findings that ovariectomy or ablation of the CL at
any stage of pregnancy leads to abortion Sumar, 1988..
7.1. Confirmation of pregnancy
Rejection of males by previously mated females is the first good indicator of
pregnancy but not the most reliable. Not all females that reject the male are necessarily
pregnant Alarcon
et al., 1990.; they may include animals in which embryonic loss has
recently occurred but luteal regression is not complete. Furthermore, it is possible for a
pregnant female to accept a male if he is particularly aggressive or if she is very
submissive Bourke, 1998.. External signs are not good indicators of pregnancy at any
stage of gestation. Some camelids show little apparent change in body conformation
even with advanced pregnancy and, consequently, the first signs of approaching birth
can often pass unnoticed by observers. Rectal palpation can be used by skilled
veterinarians to detect pregnancies from as early as 35 days but is most reliable after
4550 days Alarcon
et al., 1990.. Intra-rectal ultrasound scanning has been used to
successfully diagnose pregnancy between days 19 and 28 after mating in four llamas
Bourke et al., 1992a.. In a more recent study using this technique Parraguez et al.,
1997., pregnancy was diagnosis as early as 9 days, and 7 days after mating, respectively,
in alpacas and llamas. These latter diagnoses were confirmed by subsequent progesterone analyses and scanning at days 23 and 34, respectively, in the two species. The
early detection of pregnancy with this technique is obviously impressive, but the number
of animals involved so far is relatively small and large scale testing is now required to
assess this technique. Trans-abdominal scanning has been found to be a reliable method
when used later in pregnancy, with an accuracy of 92% at 80 days for alpacas and 100%
at 75 days for llamas Alarcon
et al., 1990.. As pregnancy advanced from these times,
accuracy of diagnosis by this method declined for both species. The monitoring of
plasma progesterone concentration for the first 30 days post mating is a useful method to
detect pregnancy but may also indicate high progesterone secretion by a persistent CL in
non-pregnant females Adam et al., 1989.. Ideally, pregnancy should be confirmed by
two methods and, because of the high embryonic losses, it should be reconfirmed after
the first trimester.

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7.2. Placental deelopment and embryonic loss

The placenta of camelids has been described as epitheliochorial in that it does not
have raised points of attachments cotyledons. like domestic ruminant species. The
chorionic epithelium has numerous half-circled domed projections or folds which serve
as placentomes and are closely opposed to corresponding depressions in the uterine
mucosa Stevens et al., 1980; Fowler, 1989; Smith et al., 1994.. Camelids are unique in
that there is an extra membrane which is derived from the epidermis of the fetus that
covers the entire fetal body and is attached at the mucocutaneous junctions Merkt et al.,
1988; Fowler, 1989.. Its function is not precisely known but it may play a role in
facilitating delivery of the conceptus by lubricating the fetus.
It is estimated that 50% of adult alpacas fail to produce young each year, even though
fertilization rates of 80% or more have been observed 3 days after natural mating. This,
in itself, would account for the low reproductive rate in this species. Moreover, it is
estimated that up to 50% of embryonic loss occurs during the first month of pregnancy
but the precise cause of this loss is not known Fernandez-Baca et al., 1970b.. The
inability of the right uterine horn to carry a pregnancy to term is probably the major
cause. Even though both ovaries appear to contribute equally to the total number of ova
shed estimated from the occurrence of CL., few embryos that are produced and implant
in the right side survive beyond 30 days gestation and none survive after 87 days
Fernandez-Baca et al., 1970b.. In the same study, the number of embryos that
originated in the right side and migrate to the left uterine horn to implant constituted
fewer pregnancies compared with those originating from, and implanting in, the left
uterine horn. However, in a later study in alpacas, it was found that 50.4% of 928
pregnancies that established in the left uterine horn were supported by CL in the right
ovary Fernandez-Baca et al., 1979.. This would imply that many of the embryos
originating in the left side are also lost. That CL in the right ovary apparently regress at
a faster rate than those on the left may suggest a more potent, local action of the
luteolytic agent produced in the right uterine horn, which cannot be prevented by the
presence of an embryo in that horn Fernandez-Baca et al., 1979.. Alternatively, where
migration of embryos from the right to the left uterine horn occurs, the absence of an
embryo in the right side may contribute to the regression of the right CL, though this
must only occur when the migration is delayed beyond the normal time of maternal
recognition. It is not known precisely when this latter event occurs, but it is estimated
that the embryos are held in the oviducts for up to 6 days before they move into the
uterus Adam et al., 1992.. The possibility of differential embryo-maternal recognition
signals between the right and left uterine horns cannot be discounted. Other factors that
are implicated in embryonic loss include poor nutrition, hormone deficiencies and
inbreeding. According to Fowler 1989., diseases have not been identified as abortifacients in alpacas or llamas.
7.3. Endocrine changes during parturition
The few studies on gestational and perinatal endocrine changes in alpacas and llamas
suggest that the sequence of maternal and fetal hormone release in these species is


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

generally in accord with the accepted patterns of endocrine changes that initiate
parturition in other species Thorburn et al., 1972; Challis and Olson, 1988.. Thus,
plasma progesterone concentrations in llamas begin to decline at about 15 days before
birth and drop markedly during the final 24 h to reach basal concentrations of 0.4 ng
mly1 on the day of parturition Leon et al., 1990.. In addition to progesterone, alpacas
have a substantial amount of the progesterone metabolite 20a-dihydroprogesterone in
circulation Fernandez-Baca et al., 1970a., but its significance is unknown. These
changes in progesterone concentrations occur in the face of increasing plasma levels of
total estrogens estroneq estradiol 17b . and estradiol 17b, both of which peak over the
last week of pregnancy and decline to basal levels during the first week post partum.
There is some evidence that fetal adrenal weight increases and that fetal cortisol levels
rise over the last 2 days of pregnancy and during delivery Sumar et al., 1978; Leon et
al., 1990.. In other species, activation of the fetal pituitaryadrenal axis is considered to
be the trigger that stimulates the production of PGF2 a by the placenta and its secretion
into the uterine vein, which in turn causes the regression of the CL Thorburn et al.,
1972.. However, there appear to be no studies in small camelids on changes in
prostaglandin release in association with parturition, or of its production by the placenta.
7.4. Parturition and effects of lactation
A detailed account of the various stages of parturition has been given by Fowler
1989. and will not be discussed here. The majority of females give birth in the standing
position and during daylight hours from 0600 to 1400 h in high altitude areas at least
Sumar et al., 1978; Moseley, 1995.. During labour, the female may lie down occasionally and experience abdominal straining. The amniotic sac may also emerge from the
vulva at this stage and rupture. In an uncomplicated delivery, the fetus should be
delivered within 4560 min after fluid has first appeared at the vulva Fowler, 1989..
However, some have taken 6090 min, and even up to 2 h with first delivery Bourke,
1998.. The placenta is usually expelled within 2 h of birth and the mothers do not eat the
afterbirth, nor lick their young or even free them from the membranes, as do other
domestic ruminants. The birth weights of cria ranges from 7 to 8 kg for alpacas and 10
to 11 kg for llamas. Weaning usually takes place when they are about 79 months of
age. Rejection of offspring is supposedly rare in small camelids and indeed, some
female alpacas and llamas may accept other crias. However, some alpaca breeders in
Australia have experienced rejection of offspring Dr. I.M. Davison, personal communication.. In contrast, the wild types of small camelids are not known to accept any cria
other than their own Fowler, 1989.. Dystocia or difficult birth. is fairly low in
camelids occurring in only about 25% of cases. Most birth difficulties are due to
abnormal presentation or position of the fetus. However, dystocia may also be due to
genital abnormalities, infection, poor nutrition or obesity, shoulder lock or breech birth,
and may generally require veterinary assistance Bourke, 1998..
Milk production will normally increase in the mother over the first few days after
birth and, in common with other ungulate species, the cria must obtain passive immunity
through ingesting colostrum in the milk. However, unlike other domestic ruminants,
growth of preovulatory follicles is not influenced by lactation Adams et al., 1990..

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


Though females can come into heat 14 days after parturition San-Martin et al., 1968,
Sumar, 1996., ovarian function in terms of folliculogenesis and induction of estrus
generally does not resume until about 10 days after birth. Additionally, uterine involution is not complete until about 15 days post partum in the alpaca and, hence, it is
advisable to delay subsequent breeding until 1520 days post partum to ensure good
fertility and one offspring per year.

8. Assisted reproductive technologies

8.1. Induction of oulation and multiple oulation
Ovulation in both alpacas and llamas can be induced with administration of exogenous hormones with LH activity, such as human chorionic gonadotrophin hCG., or
hormones that trigger LH release such as GnRH San-Martin et al., 1968; England et al.,
1969; Fernandez-Baca et al., 1970c; Adam et al., 1989; Bourke et al., 1992a,b, 1995a;
Bravo et al., 1992.. Ovulation occurs about 26 h after hCG injection San-Martin et al.,
1968; Novoa, 1970. and at 28 h after GnRH Bourke et al., 1992b.. The dose rate of
hCG used is dependent upon the route of administration and, evidently, upon the time of
year. Thus, i.v. doses of hCG needed to induce the same ovulatory response proportion
of animals ovulating. in llamas were much smaller in January 2550 IU. than in April
and May 100300 IU, England et al., 1969.. However, i.m. injections of this hormone
require higher dose rates 500750 IU. to achieve ovulation in 90100% of the treated
animals Adam et al., 1989.. The effective dose of GnRH that elicits an ovulatory
response varies enormously over the different studies and is probably due to the nature
of the preparation of the hormone, i.e., an extract of the pure hormone or an analogue.
However, estrogen status and therefore the follicular status of the animal see Section
5.2.2. can also influence pituitary responsiveness to GnRH-induced LH release. Thus,
Bravo et al. 1992. found i.v. doses of 1000 mg of GnRH resulted in ovulation, though
there was a big drop to their next highest dose of 100 mg, which was without effect.
However, Correa et al. 1997. used i.m. doses of 750 mg of GnRH to induce ovulation
in llamas, while only very small doses 8 mg. of a GnRH analogue Buserelin, Receptal,
Hoechst, UK. are necessary to produce the same result Bourke et al., 1992b, 1995a..
As mentioned earlier, ovulation in small camelids is dependent upon sufficient LH
being released in response to copulation and it is not uncommon for alpacas and llamas
to be bred for up to three times within 24 h, in the belief that additional breeding will
stimulate more LH. However, Bravo et al. 1992. found that subsequent matings at 6
and 24 h after initial mating in either species did not provoke any LH response, let alone
additional LH. Similarly, they reported that GnRH, given at 6 or 24 h after an initial
dose of this hormone, or after copulation, had no significant effect on increasing LH. It
has been suggested that the lack of gonadotrophin release in response to subsequent
ovulatory stimulation is due to a refractoriness at the level of the pituitary, which could
involve either a depletion of the LH pool in the pituitary or down-regulation of GnRH
receptors Bravo et al., 1992.. Whatever the cause, these findings demonstrate that
subsidiary LH in relation to that induced by an initial ovulatory stimulus can only be


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

achieved by administration of hormones with LH activity such as hCG, and not with LH
inducing activity, as is the case with GnRH. Indeed, it has been shown that when mating
was accompanied by an injection of hCG 750 IU., ovulation rate increased by 10% and
the time to ovulation decreased by at least 24 h, compared with these parameters after
mating alone Bourke et al., 1992a.. It is now common practice for alpaca breeders to
administer a dose of hCG soon after mating to enhance both ovulation and pregnancy
rate. However, the practice of allowing multiple matings of individual females in
breeding programs should not be discouraged, since deposition of several ejaculates in
females of other species has been shown to increase the overall fertility of flocks and
MOET programs, which by necessity involve induction of super- or multiple-ovulation, are commonly used in other domestic livestock species for many reasons, which
include quick dissemination of genes from superior females, a shortening of the
generation interval to speed up genetic selection and for the cryopreservation of
resulting embryos. However, in these animals, the ability of the female to carry a twin
pregnancy to term is both possible and, in many instances, an economic proposition.
With camelids, twin births are rare three sets of twins were born in Australia in the last
2 years Dr. I.M. Davison, personal communication. and not surprisingly so, since the
right uterine horn is virtually incapable of sustaining a successful pregnancy. Until this
limitation to breeding is fully understood, these animals seem destined to give birth to
only one offspring at a time, a circumstance that can be more easily and economically
achieved through natural mating of individual females. Hence, induction of multiple
ovulations in these animals does not appear to be a practical proposition at this time,
unless there are specific reasons to breed, or cryopreserve embryos, from superior
female stock.
Nevertheless, synchronous stimulation of a number of small ovarian follicles in
camelids, in order to induce preovulatory development and multiple ovulation, is
difficult. This is largely due to 1. the absence of spontaneously occurring luteal phases
because they are induced ovulators. during which superovulation agents are traditionally applied in other domestic species, 2. to the presence of a dominant follicle that
prevails for long periods of time in non-pregnant females. Essentially, two approaches
have been studied in llamas. Firstly, females were treated with 1000 IU of equine
chorionic gonadotrophin eCG. during a luteal phase that was either induced with
gonadotrophin treatment or simulated with exogenous progestagen implants Bourke et
al., 1992b, 1995a.. The second approach involved treatment of females with either eCG
500 IU. or porcine pFSH 220 mg in decreasing doses over 4 days., or in combination
with each other, during estrus and therefore in the absence of a progesterone influence
Correa et al., 1997.. As is the case in domestic ruminants, these superovulation
treatments produced huge variation in individual response, in terms of the number of
stimulated follicles and the number of resultant CL. Also, there was wide variation in
recovery rates of embryos, which tended to be lower in treatment groups with the
greatest ovulation rate, which probably reflects a limitation of the fimbria to capture all
ova shed at the time of ovulation. Thus, it appears that whilst either of the above doses
750 or 1000 IU. of eCG were effective in inducing follicle stimulation range 013 and
117, respectively, Bourke et al., 1992a; Correa et al., 1997., the number that ovulated

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


was greatest with the higher dose 011 cf. 13.. However, treatment with pFSH was
superior to eCG in both the numbers of stimulated follicles range 416. and ovulations,
as assessed by the number of CL present 216. Correa et al., 1997.. Bravo et al.
1995. also found that these dose rates produced some cystic follicles, though the
incidence of this was much greater after treatment with 2000 IU eCG.
8.2. Embryo collection and transfer
Early attempts to transfer embryos in alpacas in South America, which resulted in the
birth of one live cria, were reported by Sumar 1996.. Procedures for the collection and
non-surgical transfer of embryos in llamas have been described in detail Wilson Wiepz
and Chapman, 1985; Bourke et al., 1995b.. In brief, ovulation in donor and recipient
animals is synchronised by a variety of means, including mating, or treatment with
GnRH or hCG. The occurrence of ovulation is monitored using trans-rectal ultrasonography and embryos are collected at about 68 days after ovulation Bourke et al., 1995b..
With light anaesthesia, a Foley catheter is inserted through the vagina and cervix with
the aid of a speculum and positioned in the lumen of the uterus. After inflation of the
cuff, 34 volumes 50 ml. of Dulbeccos phosphate buffered saline containing 1%
heat-inactivated fetal calf serum FCS. are flushed through the catheter and the
collections obtained are searched for embryos. The transfer media is the same as the
flushing media except that it contains 20% FCS. Embryos are drawn into an AI plastic
straw 0.25 or 0.5 ml. fitted to a French Cassou insemination gun, introduced into the
lumen of uterus via the cervix and expelled, either singly or in pairs, into the uterine
horn ipsilateral to the CL.
Bourke et al. 1995b. reported that 50% 5r10. of recipients carried pregnancies to
344 days and one to 304 days after transfer. All pregnancies implanted in the left uterine
horn irrespective of the side of transfer and none of the recipients that received two
embryos had twins. In the study of Wilson Wiepz and Chapman 1985., only one
embryo was recovered from two donors and after transfer to a recipient llama, one
offspring was born at 326 days after transfer.
8.3. In itro technology
Very few studies have been conducted on in vitro culture of eggs from small
camelids Del Campo et al., 1992, 1994.. Essentially, the classical culture systems used
in other domestic animals Walker et al., 1992, 1994; Brown and Radziewic, 1998. were
modified for use in the llama, by using epididymal spermatozoa for in vitro fertilization
IVF. and llama oviducal epithelial cell in co-culture for the 9 day in vitro culture phase.
All culture steps were done in a humidified environment at 38.58C and 5% CO 2 . It was
found that 29.2% of the oocytes were penetrated by spermatozoa but only 57.1% of
these had evidence of male and female pronuclei. The finding that fertilization tended to
be higher in denuded eggs than in those surrounded with cumulus cells may reflect poor
viability of the epididymal sperm used. Though, in this study, only a small number of
the total oocytes formed morulae 5.6%., early or expanded blastocysts 6.0%., or
hatching blastocysts 4.7%., these results are encouraging and show that embryos from


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

small camelids can be produced in vitro. Perhaps modifications to the present culture
system or adapting a defined culture system, together with the use of ejaculated
spermatozoa for IVF, may enhance embryo production rate.
8.4. Artificial insemination
As mentioned previously, the major limitation to AI in small camelids is the lack of
reliable and routine methods for the collection of semen. Earlier attempts with this
procedure in alpacas resulted in very poor pregnancy rates ranging from 2.4% to 38%
and Novoa, 1968; Leyva et al., 1977.. Recent
et al., 1968; Fernandez-Baca

developments with methods for the collection of semen in small camelids see above,
Collection of semen. have led to one study in alpacas, in which pregnancy rates after
laparoscopically guided inter-uterine insemination, and cervical inseminations, were
compared at Day 15 after AI Bravo et al., 1997.. With either approach, undiluted semen
volume and sperm concentration not reported. was used and ovulation was induced
with 750 IU of hCG administered i.m. immediately after insemination. Overall pregnancy rate was 69.2% of ovulating females at Day 15 and there was no significant
difference in pregnancy rate with either site of semen deposition Bravo et al., 1997..
However, nothing is known of the pregnancy rate to term.

9. Conclusions and future research areas

There is no doubt from the foregoing that a huge research effort has gone into the
study of reproduction and behaviour of small camelids over the past 30 years. Because
of the many unique features of their reproductive system and behaviour that need to be
fully understood, the adoption and application of advanced breeding techniques that are
used routinely in other domestic animals has been slow. Alpacas and llamas are
necessarily bred at older ages than most domestic species and therefore knowledge of
the physiological and endocrine changes that facilitate onset of puberty in both sexes is
of economic importance to breeding. Also, the endocrine milieu that facilitates extended
periods of female receptivity to males needs to be re-examined, particularly in relation to
onset of puberty and the potential to breed from yearlings.
The high embryonic loss in small camelids is a major limitation to production in the
female. Research is needed to determine the factors most likely to contribute to this loss,
particularly in relation to the preferential location of embryos in the left uterine horn and
the apparent differential luteolytic activity of the two uterine horns. The pattern of
change in reproductive hormones that accompanies estrus, induction of ovulation and
regression of CL, has received considerable attention and provides a good basis for more
detailed investigations of the factors controlling these physiological events. The role
played by the reproductive hormones in folliculogenesis and the endocrine factors that
facilitate development of a dominant follicle to preovulatory size are poorly understood.
Such research may provide insights into the causes of anovular in many mated females.
It may also lead to treatment schedules that will better synchronize follicular cycles,
ensure adequate development of pre-ovulatory follicles, or enhance multiple ovulations

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


when required. The actual cause of luteolysis and the mechanism by which it occurs is
still largely unknown, especially in light of the fact that the luteolysin may act
systemically. Furthermore, an understanding of the nature of the embryormaternal
recognition signal of pregnancy and the uterine environment needed for successful
implantation would undoubtedly lead to improvements in embryo survival.
In the male, several areas of research are required to improve overall fertility. Firstly,
the hormone interactions involved in facilitating libido need to be established and the
underlying causes of declining libido resulting from continued exposure to estrus
females identified. Secondly, there is a need to develop a method to collect semen that
can be easily and routinely applied to animals on farm, or in studs. The lack of such a
method has long hampered the evaluation of sires through proper assessment of their
semen quality, and in the application of AI. Finally, there is little information available
on the cryopreservation of semen in small camelids. Development of freezing techniques
for these species would enable semen to be more readily used for breeding nationally
and internationally, facilitate cross-breeding between species to improve products such
as fibre and assist in preservation of some of the more endangered New World camelids.

Adam, C.L., Bourke, D.A., Kyle, C.E., Young, P., McEvoy, T.G., 1992. Ovulation and embryo recovery in
the llama. In: Allen, W.R., Higgins, A.J., Mayhew, I.G., Snow, D., Wade, J.F. Eds.., Proc. 1st Int. Camel
Conf.. R&W Pub., Newmarket, pp. 125127.
Adam, C.L., Moir, C.E., Shiach, P., 1989. Plasma progesterone concentrations in pregnant and non-pregnant
llamas Lama glama.. Vet. Rec. 125, 618620.
Adams, G.P., Griffin, P.G., Ginther, O.J., 1989. In situ morphologic dynamics of ovaries, uterus, and cervix in
llamas. Biol. Reprod. 41, 551558.
Adams, G.P., Sumar, J., Ginther, O.J., 1990. Effects of lactational and reproductive status on ovarian follicular
waves in llamas Lama glama.. J. Reprod. Fertil. 90, 535545.
Adams, G.P., Sumar, J., Ginther, O.J., 1991. Form and function of the corpus luteum in llamas. Anim. Reprod.
Sci. 24, 127138.
V., Sumar, J., Riera, G.S., Foote, W.C., 1990. Comparison of three methods of pregnancy diagnosis
in aplacas and llamas. Theriogenology 34, 11191127.
Bourke, D.A., 1998. An introduction to the unique reproductive physiology and breeding activity of SACs.
Proc. Crossing Boundaries, 710.
Bourke, D.A., Adam, C.L., Kyle, C.E., 1992a. Ultrasonography as an aid to controlled breeding in the llama
Lama glama.. Vet. Rec. 130, 424428.
Bourke, D.A., Adam, C.L., Kyle, C.E., McEvoy, T.G., Young, P., 1992b. Ovulation, superovulation and
embryo recovery in llamas. Proc. 12th Int. Congr. Anim. Reprod., The Hague, 2327 August 1, 193195.
Bourke, D.A., Kyle, C.E., McEvoy, T.G., Young, P., Adam, C.L., 1995a. Superovulatory responses to eCG in
llamas Lama glama.. Theriogenology 44, 255268.
Bourke, D.A., Kyle, C.E., McEvoy, T.G., Young, P., Adam, C.L., 1995b. Recipient synchronization and
embryo transfer in South American camelids. Theriogenology 43, 171, Abstr...
Bravo, P.W., 1994. Reproductive endocrinology of llamas and alpacas. Vet. Clin. North Am.: Food Anim.
Pract. 10, 265279.
Bravo, P.W., Flores, U., Garnica, J., Ordonez,
C., 1997. Collection of semen and artificial insemination of
alpacas. Theriogenology 47, 619626.
Bravo, P.W., Fowler, M.E., Stabenfeldt, G.H., Lasley, B.L., 1990a. Ovarian follicular dynamics in the llama.
Biol. Reprod. 43, 579585.


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

Bravo, P.W., Fowler, M.E., Stabenfeldt, G.H., Lasley, B., 1990b. Endocrine responses in the llama to
copulation. Theriogenology 33, 891899.
Bravo, P.W., Stabenfeldt, G.H., Fowler, M.E., Lasley, B.L., 1992. Pituitary response to repeated copulation
andror gonadotropin-releasing hormone administration in llamas and alpacas. Biol. Reprod. 47, 884888.
Bravo, P.W., Stabenfeldt, G.H., Lasley, B.L., Fowler, M.E., 1991. The effect of ovarian follicle size on
pituitary and ovarian responses to copulation in domesticated South American camelids. Biol. Reprod. 45,
Bravo, P.W., Sumar, J., 1989. Laparoscopic examination of the ovarian activity in alpacas. Anim. Reprod. Sci.
21, 271281.
Bravo, P.W., Tsutsui, T., Lasley, B.L., 1995. Dose response to equine chorionic gonadotropin and subsequent
ovulation in llamas. Small Ruminant Res. 18, 157163.
Brown, B.W., 1994. A review of nutritional influences on reproduction in boars, bulls and rams. Reprod. Nutr.
Dev. 34, 89114.
Brown, B.W., Emery, M.J., Mattner, P.E., 1980. Ovarian arterial blood velocity measured with Doppler
ultrasonic transducers in conscious ewes. J. Reprod. Fertil. 58, 295300.
Brown, B.W., Mattner, P.E., Panaretto, B.A., Brown, G.H., Gream, B.D., Honnery, R.L., 1990. Effect of
mouse epidermal growth factor on fertility in rams. Aust. J. Agric. Res. 41, 11471153.
Brown, B.W., Radziewic, T., 1998. Production of sheep embryos in vitro and development of progeny
following single and twin embryo transfers. Theriogenology 49, 15251536.
Brown, C.E., 1936. Rearing wild animals in captivity and gestation periods. J. Mammal. 17, 1013.
W., Sumar, J., Franco, E., 1968. Avances en la inseminacion artificial de las alpacas Lama pacos ..
Rev. Fac. Med. Vet. Univ. Nac. Mayor San Marcos 22, 1935, cited in Bravo et al., 1997..
Challis, J.R.G., Olson, D.M., 1988. Parturition. In: Knobill, E., Neill, J.D. Eds.., The Physiology of
Reproduction. Raven Press, New York, pp. 21772216.
Correa, J.E., Ratto, M.H., Gatica, R. et al., 1997. Superovulation in llamas Lama glama. with pFSH and
equine chorionic gonadotrophin used individually or in combination. Anim. Reprod. Sci. 46, 289296.
Davison, I.M., 1998. Fibre science and technology: lessons from the wool industry. In: Brash, L.D., Davison,
I.M. Eds.., Proc. Alpaca Conf., 7th November. CSIRO Anim. Prod., Prospect, NSW, Australia.
Del Campo, M.R., Del Campo, C.H., Donoso, M.X., Berland, M., Mapletoft, R.J., 1994. In vitro fertilization
and development of llama Lama glama. oocytes using epididymal spermatozoa and oviductal cell
co-culture. Theriogenology 41, 12191229.
Del Campo, M.R., Donoso, M.X., Del Campo, C.H., Rojo, R., Barros, C., Parrish, J.J., Mapletoft, R.J., 1992.
In vitro maturation of llama Lama glama. oocytes. Proc. 12th Int. Congr. Anim. Reprod., The Hague,
2327 August 1, 324326.
Delhon, G.A., von Lawzewitsch, I., 1987. Reproduction in the male llama Lama glama., a South American
camelid. I Spermatogenesis and organization of the intertubular spaces of the mature testis. Acta. Anat.
129, 5966.
England, B.G., Foote, W.C., Cardoza, A.G., Matthews, D.H., Riera, S., 1971. Oestrus and mating behaviour in
the llama Lama glama.. Anim. Behav. 19, 722726.
England, B.G., Foote, W.C., Matthews, D.H., Cardozo, A.G., Riera, S., 1969. Ovulation and corpus luteum
function in the llama Lama glama.. J. Endocrinol. 45, 505513.
S., 1993. Manipulation of reproductive functions in male and female New World camelids.

Anim. Reprod. Sci. 33, 307323.

S., 1995. Genetic erosion of camelidae. Animal genetic resources information. FAO Publ.

14., 97105.
S., Hansell, W., Novoa, C., 1970a. Corpus luteum function in the alpaca. Biol. Reprod. 3,

S., Hansell, W., Novoa, C., 1970b. Embryonic mortality in the alpaca. Biol. Reprod. 3,

S., Hansell, W., Saatman, R., Sumar, J., Novoa, C., 1979. Differential luteolytic effects of

right and left uterine horns in the alpaca. Biol. Reprod. 20, 586595.
S., Madden, D.H.L., Novoa, C., 1970c. Effect of different mating stimuli on induction of

ovulation in the alpaca. J. Reprod. Fertil. 22, 261267.

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


S., Novoa, C., 1968. Primer ensayo de inseminacion artificial de alpacas Lama pacos . con

semen de vicuna Vicugna icugna.. Rev. Fac. Med. Vet. Univ. Nac. Mayor San Marcos 22, 918, cited
in Bravo et al., 1997..
S., Novoa, C., Sumar, J., 1972a. Actividad reproductiva en la alpaca mantenida en separacion

del macho. Mem. Asoc. Latinoam. Prod. Anim. 7, 718, cited in Fernandez-Baca,

S., Sumar, J., Novoa, C., 1972b. Comportamiento sexual de la alpaca mancho frente a la

de las hembras. Rev. Invest. Pecu. IVITA. Univ. San Marcos 1, 115128, cited in

Fowler, M.E., 1989. Medicine and Surgery of South American Camelids. Llama, Alpaca, Vicuna,
Iowa State University Press, Ames.
Franco, E., Sumar, J., Varela, M., 1981. Ejaculacion en la alpaca Lama pacos .. Proc. 4th Conv. Int.
Camelidos Sudam., Punta Arenas, Chile, 2227 Noviembre, cited in Fowler, 1989..
Franklin, W.L., 1983. Contrasting socioecologies of South Americas wild camelids: the vicuna
and the
guanaco. Eisenbery, J.F., Kleinman, D.G. Eds.., Advances in the Study of Mammalian Behaviour. Am.
Soc. Mammal. 7, 573629.
Garnica, J., Achata, R., Bravo, P.W., 1993. Physical and biochemical characteristics of alpaca semen. Anim.
Reprod. Sci. 32, 8590.
Goding, J.R., Cumming, I.A., Chamley, W.A., Brown, J.M., Cain, M.D., Cerini, J.C., Cerini, M.E.D., Findlay,
J.K., OShea, J.D., Pemberton, D.H., 1971r1972. Prostaglandin F2 a , the luteolysin in the mammal?.
Horm. Antagonists Gynecol. Invest. 2, 7397.
Graham, E.F., Schmell, M.K.L., Eversen, B.K., Nelson, D.S., 1978. Semen preservation in nondomestic
mammals. Symp. Zool. Soc. London 43, 153173.
Gray, A.P., 1954. Mammalian Hybrids. Technical Communication, No. 10, Commonwealth Bureau of Animal
Breeding and Genetics, Edinburgh, Bucks, England.
Hansel, W., Alila, H.W., Dowd, J.P., Milvae, R.A., 1991. Differential origin and control mechanisms in small
and large bovine luteal cells. J. Reprod. Fertil., Suppl. 43, 7789.
Johnston, L.W., 1988. Llama reproduction. In: Johnston, L.W. Ed.., Llama Medicine Workshop for
Veterinarians. Colorado State University, Fort Collins, Appendix 10b.
Koford, C.B., 1957. The vicuna
and the puna. Ecol. Monogr. 27, 153219.
Leon, J.B., Smith, B.B., Timm, K.I., LeCren, G., 1990. Endocrine changes during pregnancy, parturition and
the early post-partum period in the llama Lama glama.. J. Reprod. Fertil. 88, 503511.
Leyva, V., Sumar, J., 1981. Evaluacion
del peso corporal al empadre sobre la capacidad reproductiva de
hembras alpaca de un ano
de edad. Proc. 4th Conv. Int. Camelidos Sudam., Punta Arenas, Chile, 2227
Noviembre, cited in Fowler, 1989..
Leyva, V., Sumar, J., Franco, E., 1977. Inseminacion artificial en camelidos sudamericanos. I Reun. Cient.
Annu. Asoc. Peru. Prod. Anim. 21, Abstr.. cited in Sumar, 1985..
Lichtenwalner, A.B., Woods, G.L., Weber, J.A., 1996. Seminal collection, seminal characteristics and pattern
of ejaculation in llamas. Theriogenology 46, 293305.
Louvet, J.P., Harman, S.M., Schreiber, J.R., Ross, G.T., 1975. Evidence for a role of androgens in follicular
maturation. Endocrinology 97, 366372.
Lukaszewska, J., Hansel, W., 1980. Corpus luteum maintenance during early pregnancy in the cow. J. Reprod.
Fertil. 59, 485493.
Mattner, P.E., 1966. Formation and retention of the spermatozoan reservoir in the cervix of the ruminant.
Nature London. 212, 14791480.
Mattner, P.E., 1969. The survival of spermatozoa in bovine cervical mucus and mucus fractions. J. Reprod.
Fertil. 20, 193199.
Maxwell, W.M.C., Wilson, H.R., Butler, L.G., 1984. Fertility of ewes after intrauterine insemination with
frozen semen. Proc. Aust. Soc. Anim. Prod. 15, 448451.
Merkt, H., Boer, M., Rath, D., Schoon, H.A., 1988. The presence of an additional fetal membrane and its
function in the new born Guanaco lama quanacoe.. Theriogenology 30, 437439.
Mogrovejo, S.D. 1952. Estudios del semen de la alpaca. BS Tesis. Fac. Med. Vet. Univ. Nac. Mayor San
Marcos, Lima cited in Sumar, 1985..
Montalvo, C., Cevallos, E., Copaira, M., 1979. Estudio microscopico
del parenquima
testicular de la alpaca


B.W. Brownr Animal Reproduction Science 58 (2000) 169195

durante las estaciones del ano.

19751979. Univ. Nac. Mayor
In: Res. Proyectos de Investigacion,

San Marcos, Lima, p. 37, cited in Fernandez-Baca,


Moore, R.M., Hay, M.F., Dott, H.M., Cran, D.G., 1978. Macroscopic identification and steroidogenic function
of atretic follicles in sheep. J. Endocrinol. 77, 309318.
Moseley, G., 1995. Commercial management of small Camelidae in northern Europe. Vet. Annu. 35,
Novoa, C., 1970. Reproduction in Camelidae. A review. J. Reprod. Fertil. 22, 320.
Novoa, C., Sumar, J., Franco, E., 1970. Empadre complementario de hermbras alpacas vacas.
Bol. Extraordinario 4, 5359, cited in Fowler, 1989..
Ortavant, R., 1959. Le cycle spermatogenetique
chez la belier.
Ann. Zootech. 8, 183244 and 271322.

Parraguez, V.H., Cortez,

S., Gazitua,
F.J., Ferrando, G., MacNiven, V., Raggi, L.A., 1997. Early pregnancy
diagnosis in alpaca Lama pacos . and llama Lama glama. by ultrasound. Anim. Reprod. Sci. 47,
Pollard, J.C., Littlejohn, R.P., Moore, G.H., 1995. Seasonal and other factors affecting the sexual behaviour of
alpacas. Anim. Reprod. Sci. 37, 349356.
Salamon, S., 1962. Studies on the artificial insemination of Merino sheep. The effect of frequent ejaculation on
semen characteristics and freezing capacity. Aust. J. Agric. Res. 13, 11371150.
Salamon, S., 1976. Artificial Insemination of Sheep. Dept. Anim. Husb., Univ. Sydney, Publicity Press,
San-Martin, M., Copaira, M., Zuniga, J., Rodreguez, R., Bustinza, G., Acosta, L., 1968. Aspects of
reproduction in the alpaca. J. Reprod. Fertil. 16, 395399.
Scaramuzzi, R.J., Davidson, W.G., Van Look, P.F.A., 1977. Increasing ovulation rate in sheep by active
immunization against an ovarian steroid androstenedione. Nature London. 269, 817818.
Schalm, O.W., 1967. Normal values in blood of laboratory, fur-bearing and miscellaneous zoo and wild
animals, Veterinary Hematology. 2nd edn. Lea & Febiger, Philadelphia.
Schmidt, C.R., 1973. Breeding season and notes on some other aspects of reproduction in captive camelids.
Int. Zoo. Yearb. 13, 387390.
Shalash, M.R., Nawito, M., 1964. Some reproductive aspects in the female camel. Proc. Vth Congr. Anim.
Reprod. Artif. Insem., Trento 2, 263273.
Smith, C.L., Peter, A.T., Pugh, D.G., 1994. Reproduction in llamas and alpacas: a review. Theriogenology 41,
Smith, T.M., 1985. Reproduction in South American Camelids. Iowa State Univ. Vet. 47, 110115.
Stanley, H.F., Kadwell, M., Wheeler, J.C., 1994. Molecular evolution of the family Camelidae a
mitochondrial DNA study. Proc. R. Soc. London, Ser. B 256, 16.
Stevens, D.H., Burton, G.J., Sumar, J., Nathanielsz, P.W., 1980. Ultrastructural observations on the placenta of
the alpaca, Lama pacos. Placenta 1, 2132.
Sumar, J., 1985. Reproductive physiology in South American Camelids. In: Land, R.B., Robinson, D.W.
Eds.., Genetics of Reproduction in Sheep. Butterworths, London, pp. 8195.
Sumar, J., 1988. 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. 83, 133141.
Sumar, J., Fredriksson, G., Alarcon,
V., Kindahl, H., Edqvist, L.E., 1988. Levels of 15-keto-13,14-dihydroPFG2 a , progesterone and oestradiol-17b after induced ovulations in llamas and alpacas. Acta Vet. Scand.
29, 339346.
Sumar, J., Leyva, V., 1981. Coleccion de semen mediante vagina artificial en la alpaca. Proc. IV Conv. Int.
Camelidos Sudam., Punta Arenas, Chile, 2227 Noviembre, cited in Bravo et al., 1997..
Sumar, J., Smith, G.W., Mayhua, E., Nathanielsz, P.W., 1978. Adrenocortical function in the fetal and
newborn alpaca. Com. Biochem. Physiol. 59A, 7984.
Sumar, J.B., 1996. Reproduction in llamas and alpacas. Anim. Reprod. Sci. 42, 405415.
Sumar, J.B., Garcia, M., 1986. Fisiologia de la reproduccion
de la alpaca. In: Nuclear and Related Techniques
in Animal Production and Health. I.A.E.A., Vienna, pp. 149177, cited in Fernandez-Baca,

Taylor, K.M., Hungerford, D.A., Snyder, R.L., Ulmer, F.A. Jr., 1968. Uniformity of karyotypes in the
Camelidae. Cytogenics 7, 815.
Thorburn, G.D., Nicol, D.H., Bassett, J.M., Shutt, D.A., Cox, R.I., 1972. Parturition in the goat and sheep:

B.W. Brownr Animal Reproduction Science 58 (2000) 169195


changes in corticosteroids, progesterone, oestrogens and prostaglandin F. J. Reprod. Fertil., Suppl. 16,
Tsonis, C.G., Quigg, H., Lee, V.W.K., Leversha, L., Trounson, A.O., Findlay, J.K., 1983. Inhibin in individual
ovine follicles in relation to diameter and atresia. J. Reprod. Fertil. 67, 8390.
Walker, S.K., Heard, T.M., Seamark, R.F., 1992. In vitro culture of sheep embryos without co-culture:
successes and perspectives. Theriogenology 37, 111126.
Walker, S.K., Hill, J.L., Bee, C.A., Warnes, D.M., 1994. Improving the rate of production of sheep embryos
using in vitro maturation and fertilization. Theriogenology 41, 330, Abstr...
Wheeler, J.C., 1995. Evolution and present situation of the South American Camelidae. Biol. J. Linn. Soc. 54,
Wilson Wiepz, D., Chapman, R.J., 1985. Non-surgical embryo transfer and live birth in a llama. Theriogenology 24, 251257.
Zuckermann, S., 1952r1953. The breeding seasons of mammals in captivity. Proc. Zool. Soc. London 122,