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Animal Reproduction Science 124 (2011) 237–243

Contents lists available at ScienceDirect

Animal Reproduction Science

journal homepage: www.elsevier.com/locate/anireprosci

varian function in South American camelids (alpacas, llamas, vicunas, uanacos)�

ane Vaughan ∗

ria Genesis, PO Box 406, Ocean Grove, Victoria 3226, Australia

r t i c l e i n f o

rticle history: vailable online 28 September 2010

a b s t r a c t

Ultrasound technology and hormone assays have provided a better understanding of fol- liculogenesis and ovulation in South American camelids in the last two decades. Females exhibit waves of ovarian follicular growth and are induced ovulators and therefore do not

eywords: amelid lpaca lama icuna vary

exhibit oestrous cycles in the manner of spontaneously ovulating species such as sheep and cattle. There is much variation in inter-wave interval among camelid species (alpaca/llama 10–22 days, vicuna 4–11 days), within species and within individual animals as the range of each phase of follicular growth is wide. Ovulation occurs 24–30 h after mating and luteolysis occurs approximately 10 days later if conception fails to occur.

© 2010 Elsevier B.V. All rights reserved.

ollicle

. Introduction

There are four South American camelids. The alpaca Vicugna pacos) has been domesticated from the vicuna Vicugna vicugna) and the llama (Lama glama) domesti- ated from the guanaco (Lama guanicoe) (Kadwell et al., 001). South American camelids resemble each other in hape, but vary in size, fleece characteristics and geograph- cal distribution (Novoa, 1970). Vicunas are the smallest of he South American camelids, weighing 45–55 kg, and liv- ng at high altitude (above 4000 m) in the central Andes. uanacos (100–120 kg) are mainly found in the southern ndes. Historically, alpacas (55–85 kg) were grown in Peru, olivia, Chile and Argentina for their fleece, and llamas 130–180 kg) were used as beasts of burden and both used or meat, hides and fuel (faeces). Alpacas and llamas are

ow found in South and North America, Europe and Aus- ralasia and alpacas in particular, are being bred for their oft, fine, light-weight wool that comes in a range of colours

� This paper is part of the special issue entitled: Reproductive Cycles of nimals, Guest Edited by Michael G. Diskin and Alexander Evans. ∗ Tel.: +61 3 5254 3365; fax: +61 3 5254 3365.

E-mail address: [email protected].

378-4320/$ – see front matter © 2010 Elsevier B.V. All rights reserved. oi:10.1016/j.anireprosci.2010.08.031

from white, through fawn, to brown, grey and black. Phy- logenetically, South American camelids are closely related to dromedary (one-humped) and Bactrian (two-humped) camels.

The reproductive physiology of camelids differs to that of other domestic livestock. Female camelids exhibit waves of ovarian follicular growth (Adams et al., 1990; Vaughan et al., 2004) and are induced ovulators (San Martin et al., 1968) and therefore do not exhibit oestrous cycles in the manner of spontaneously ovulating species of domestic livestock. Unmated, non-ovulatory females are sexually receptive most of the time, regardless of the stage of ovar- ian follicular development (Sumar, 1983). Males mate in sternal recumbency for approximately 20 min and ejacu- late small volumes of semen many times during this period (Lichtenwalner et al., 1996a,b). Gestation length is approx- imately 11.5 months and twins are rare (San Martin et al., 1968). Generation intervals are relatively long in camelids because males take 1–3 years to reach puberty and females exhibit an extended gestation.

Ovarian function remains relatively poorly understood

in camelids because of lack of research funding inter- nationally. Advances in technology have improved over the past few decades from slaughter-house studies (San Martin et al., 1968), laparotomy (England et al., 1971) and

uction Science 124 (2011) 237–243

Table 1 Ovarian dimensions in camelids.

Alpaca Llama Vicuna Guanaco

Right ovary Length cm 1.6 ± 0.3 1.3–2.5 1.3 1.5 Depth cm 1.1 ± 0.2 1.4–2 0.7 n/aa Width cm 1.1 ± 0.2 0.6–1 1.0 n/a

Left ovary Length cm 1.6 ± 0.3 1.5–2.5 1.2 1.5 Depth cm 1.1 ± 0.2 1.5–2.5 0.7 n/a Width cm 1.1 ± 0.2 0.5–1 1.0 n/a

238 J. Vaughan / Animal Reprod

laparoscopy (Bravo and Sumar, 1989) to the use of transrec- tal ultrasound (Adams et al., 1989; Vaughan et al., 2004) and the availability of hormone assays (Bravo et al., 1990a,b; Aba and Forsberg, 1995); the latter two techniques provid- ing a relatively non-invasive and better understanding of folliculogenesis and ovulation.

2. Ovarian development

During embryological development, the gonads arise from the urogenital ridges in close proximity to paired paramesonephric (Mullerian) ducts that give rise to the internal genitalia. The ovaries do not exhibit structural dif- ferentiation until well after sex determination. Primordial follicles develop some months into gestation and are seen as oocytes surrounded by a single layer of flattened gran- ulosa cells within a basal lamina (Parker and Schimmer, 2006).

The timing of primordial follicle development is unknown in South American camelids but occurs at 8–12 weeks in camels (Marai et al., 1990). Oocytes are arrested in prophase of the first meiosis and do not progress further until shortly before ovulation in the post-pubertal camelid. Primary follicles, characterised by an oocyte surrounded by cuboidal granulosa cells, develop in camels from 20 to 24 weeks of gestation (Marai et al., 1990). Timing of first appearance of primary follicles and number of primary fol- licles present at birth is unknown in camelids. After birth, secondary follicles develop with more than one layer of granulosa cells and a thecal cell layer around the basement membrane with numerous small blood vessels (Rajkovic et al., 2006). Early folliculogenesis to the stage of pre-antral follicles appears to be directed by signals within the ovary and is independent of gonadotrophin stimulation. There is also communication within the ovary amongst oocytes, granulosa and theca cells (Parker and Schimmer, 2006). The onset of folliculogenesis occurs immediately after the first follicles are formed, and continues until the end of the reproductive period (12–18 years in alpacas), even through pregnancy and lactation (Adams et al., 1990). Follicles are also degenerating during foetal development because a lack of follicle stimulating hormone (FSH) does not support further follicular development (Rajkovic et al., 2006).

Regulation of terminal follicular growth beyond the small antral stage is a gonadotrophin-dependent pro- cess occurring after puberty and corresponding to initiation of follicular waves, selection of dominant follicles and terminal maturation of pre-ovulatory folli- cles (Monniaux et al., 1997). Gonadotrophic hormones secreted from the pituitary gland develop a complex feedback/feed-forward system with the ovaries, known as the hypothalamic–pituitary–gonadal axis, allowing fol- licles to proceed beyond the early, pre-antral stages (Rajkovic et al., 2006). Formation of the antrum signals transition from intra-ovarian to extra-ovarian control and once a follicle has entered the growing pool, it is irreversibly committed and cannot return to a quiescent state. Antral

follicles are apparent in camels at 32–36 weeks gestation (Marai et al., 1990).

In mammalian dominant follicles, FSH stimulates gran- ulosa cell proliferation, aromatisation of androgens to

Weight g 1–4 2.4 1.2 n/a

Adapted from Bravo (2002). a Not available.

oestrogens, and luteinising hormone (LH) receptor expres- sion, while LH stimulates androgen production from thecal cells (Rajkovic et al., 2006). Inhibin, secreted by the granu- losa cells of the dominant follicle, feeds back to the pituitary to inhibit FSH secretion. These findings have yet to be clearly elucidated in camelids. Granulosa cells of most early-antral follicles undergo apoptosis and death as they are not rescued by FSH.

3. Adult reproductive anatomy

Camelids have a bicornuate uterus with the tips of the horns blunt and rounded, and a single cervix, whose lumen contains 2–3 rings/spiral folds of mucosa. The uterus is located within the pelvic canal or at the pelvic brim in the non-gravid state (Vaughan and Tibary, 2006). Each uterine horn ends in a long and tortuous oviduct which joins the uterine horn to the ovarian bursa (Sumar, 1983). There is a prominent papilla at the uterotubal junction (Vaughan and Tibary, 2006). The ampulla and ovarian section of the oviduct are the most coiled parts, the isthmus less so. The fimbria are contained within the bursa, near the ovary and the ovarian bursa, is formed by a fold of the mesosalpinx and completely envelops the ovary (Bravo et al., 2000).

Ovaries are round to oval and globular in shape in lla- mas and alpacas (Sumar, 1983) and antral follicles lie over the entire periphery of each ovary (Vaughan and Tibary, 2006). Ovarian size varies amongst the four camelid species (Table 1) and varies within species depending on the struc- tures present on each ovary as follicles >4 mm diameter and corpora lutea project prominently from the surface of the ovary (Adams et al., 1989). All growing follicles in camelids are spherical, probably related to the prominent protru- sion of 85% of the follicle from the surface the ovary (Del Campo and Del Campo, 1995). Oocytes range from 172 to 200 �m in size. Immature oocytes in llamas have a distinct and large germinal vesicle with a dark nucleolus. Mature oocytes display a metaphase plate surrounded by a dark area easily found at 20–40× magnification (Del Campo and Del Campo, 1995).

4. Puberty

Time of first ovulation depends on age at first mating as camelids are induced ovulators. Information on ovarian follicular activity has been attained by measuring uri- nary oestrone sulphate and indicates that follicular growth

uction Science 124 (2011) 237–243 239

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i d a o p 1 s o l N o e m o 1

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Fig. 1. Schematic representation of follicular waves in alpacas and lla- mas. Mating induces ovulation of the dominant follicle and formation of a corpus luteum. Failure to conceive leads to luteolysis of the corpus luteum. RF = recruited follicle, SF = selected follicle, DF = dominant follicle, AF = atretic follicle, O = ovulation, CL = corpus luteum.

J. Vaughan / Animal Reprod

tarts from approximately 5–6 months of age (Bravo, 1997), ut pregnancies from 3 months of age have been recorded Vaughan and Tibary, 2006). The age at which ovarian activ- ty begins and conception occurs is dependent on nutrition nd live weight. Domestic camelids are generally mated hen they have attained two-thirds of their adult weight

Smith et al., 1994), from 12 months of age in alpacas and 8 months of age in llamas.

. Sexual behaviour

Camelids do not have regular oestrus cycles that are typ- cal of spontaneous ovulators and therefore do not display istinct periods of overt oestrus. Non-pregnant females ppear receptive to males on most occasions regardless f stage of follicular development (England et al., 1971) as lasma progesterone levels remain low (Fernandez-Baca, 993). Time taken to adopt sternal recumbency (demon- tration of sexual receptivity) is not a reliable indicator f either plasma oestradiol concentration or ovarian fol- icular diameter (Bravo et al., 1991; Vaughan et al., 2003). either changes in the external genitalia nor vaginal cytol- gy may not be used as an indicator of follicle size (Ferrer t al., 1999). The sexual behaviour patterns of camelids ay also be related to their geographic location, degree

f domestication and social structure of the herd (Novoa, 970).

In an attempt to explain continual receptivity in female amelids, it has been proposed that the overlapping of fol- icular waves maintains blood oestradiol concentrations at

level sufficient to maintain sexual receptivity. If asyn- hrony occurs between successive follicle waves, oestradiol oncentration may drop long enough for sexual receptivity o decline (Brown, 2000) and these females appear indif- erent to the male rather than non-receptive.

Female camelids become non-receptive in the presence f a corpus luteum and elevated plasma progesterone. Non- eceptive female camelids strongly reject the male when laced in a yard together and may run away from the ale or spit, kick and/or scream. Spitting and attempting to

scape are most indicative of reproductive status (Pollard et l., 1994). Sexually inexperienced alpaca females are more ikely to kick and attempt escape but less likely to spit r threaten the male compared with experienced females Pollard et al., 1993).

. Seasonality

Alpacas and llamas are considered non-seasonal breed- rs as ovarian follicular activity occurs throughout the ear and season (photoperiod, rainfall or temperature) oes not affect the number of follicles >6 mm observed on he ovaries (Bravo and Sumar, 1989). However, breeding nd parturition are usually restricted by South Ameri- an farmers to the rainy, warmer months of summer

December–April) when feed is likely to be more abundant nd better quality (Fernandez-Baca, 1993). Vicunas breed n the high altitude rangelands of South America in autumn Aguero et al., 2001).

Modified from Senger (2003).

7. Folliculogenesis

Folliculogenesis, or growth and differentiation of the oocyte and associated cells, is a highly regulated process relying on the integration of signals from multiple organs. Folliculogenesis is yet to be described in guanacos, how- ever, sexually mature alpacas (Vaughan et al., 2004), llamas (Adams et al., 1990) and vicunas (Aguero et al., 2001) which have not been mated to or placed nearby a male exhibit continuous renewing of terminally growing fol- licles defined as follicular waves. The number of antral follicles detected by ultrasonography is inversely propor- tional to the diameter of the largest follicle (Adams et al., 1990; Aguero et al., 2001; Vaughan et al., 2004). Other studies have described growth of successive large anovu- latory follicles in unmated females but did not describe a periodic fluctuation in follicle numbers consistent with the existence of a wave-like pattern of growth (Bravo et al., 1990a,b; Bourke et al., 1992).

A follicle wave involves recruitment and synchronous emergence of a cohort (8–10) of antral follicles approxi- mately 2–3 mm diameter, followed by continued growth of usually one (selected follicle), but sometimes two or three follicles up to 3–5 mm diameter. The follicle destined to become dominant continues growth, while the others in the cohort (subordinate follicles) regress by atresia (Adams et al., 1990; Vaughan et al., 2004) (Fig. 1).

The duration of follicular growth is unknown in camelids but greater than that of a follicle wave observed using ultrasonography. The first stages of follicular growth are difficult to estimate accurately and are not consid- ered in the estimation of the total duration of a follicular wave. After new follicle emergence at the beginning of a follicular wave, follicle growth may be divided into three phases. The growth phase of the follicle in alpacas and lla- mas takes about 5–9 days. The mature phase, when the follicle reaches a pre-ovulatory size of 6–12 mm, is main- tained for 2–8 days. The regression phase takes 3–8 days (Bravo and Sumar, 1989; Adams et al., 1990; Chaves et al.,

2002; Vaughan et al., 2004). These phases are shorter in vicunas (Aguero et al., 2001; Miragaya et al., 2004).

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240 J. Vaughan / Animal Reprod

The interval, in days, between emergence of succes- sive dominant follicles is known as the inter-wave interval. There is much variation in inter-wave interval among camelid species (alpaca/llama 10–22 days, vicuna 4–11 days), within species and within individual animals as the range of each phase of follicular growth is wide (Adams et al., 1990; Bravo et al., 1990a,b; Aguero et al., 2001; Vaughan et al., 2004). Using a ‘mean inter-wave interval’ within a particular camelid species should therefore be avoided as it does not accurately describe what is occurring in an individual animal nor allow prediction of the optimum time of breeding (Vaughan et al., 2004). A longer inter- wave interval has been associated with a larger maximum follicle diameter in alpacas and llamas, suggesting that fol- licles with a longer inter-wave interval remain functional (Adams et al., 1990; Vaughan et al., 2004). There is appar- ently no relationship between inter-wave interval and live weight amongst alpacas (Vaughan et al., 2004).

Follicular growth rates of 0.5–0.8 mm/day (Adams et al., 1989, 1990) and 0.9 mm/day (Chaves et al., 2002) in llamas, 0.4 mm/day in alpacas (Vaughan et al., 2004) and 1.8 mm/day in vicunas (Aguero et al., 2001; Miragaya et al., 2004) have been measured using ovarian ultrasonogra- phy. In unmated alpacas, there is similar follicular growth of the dominant follicle from Days 0 to 10 after new wave emergence regardless of subsequent inter-wave interval (Vaughan et al., 2004).

There is no regularly alternating pattern of dominant follicle emergence between the left and right ovaries in lla- mas and alpacas (San Martin et al., 1968; Fernandez-Baca et al., 1970; Adams et al., 1990; Bourke et al., 1992; Vaughan et al., 2004). Dominant follicles are found equally distributed between the left and right ovary, despite the fact that 98% of all pregnancies are located in the left uterine horn of camelids.

7.1. Hormonal control of folliculogenesis

In mammals, gonadotrophin-releasing hormone (GnRH) is secreted into the hypothalamo-hypophyseal portal system in a pulsatile manner to stimulate the episodic release of gonadotrophins into the systemic circulation. GnRH has yet to be measured in camelids due to the intricacies of sampling the hormone.

Further studies are required for a better understand- ing of follicle recruitment and growth in camelids (Aba, 1995). Periodic surges in FSH and pulsatile release of LH responsible for follicle wave emergence, follicle growth and dominant follicle selection observed in some domestic live- stock have yet to be identified in camelids due to poor sensitivity of hormone assays (Aba et al., 1999). Successful use of porcine and ovine FSH to induce follicular growth in multiple ovulation and embryo transfer programs in alpacas and llamas supports the hypothesis of FSH inducing emergence of follicular waves in camelids.

Fluctuation in plasma oestradiol concentration gener- ally reflects the follicular growth pattern in camelids, but

as mentioned earlier, has little effect on sexual behaviour. There is a significant positive correlation between follicle size and oestrogen concentrations in alpacas and llamas. The emerging follicle synthesises and secretes increasing

cience 124 (2011) 237–243

levels of oestradiol during the growing phase, is maximal just before the plateau of follicle growth is reached and then decreases during atresia if ovulation is not induced (Bravo et al., 1990a,b; Aba et al., 1995; Vaughan, 2001; Chaves et al., 2002). These findings support the two-cell, two-gonadotrophin mechanism for oestradiol biosynthe- sis, which is based on findings from spontaneous ovulators.

The mechanism of dominant follicle selection from among a cohort of follicles in a wave is unknown but appears to operate systemically and is based on differen- tial responsiveness of follicles within a wave to FSH and LH (Adams, 1999). The ability of a developing follicle to release high concentrations of oestrogen and inhibin, which act locally by stimulating growth and cell differentiation of the granulosa and by the indirect effect of feedback inhi- bition of FSH secretion, is central to selection of a given follicle for maturation and ovulation (Ginther, 2000). The concentration of FSH during follicle growth decreases so that it is inadequate for subordinate follicular growth and delays onset of the next follicular wave, but the domi- nant follicle still requires low concentrations of FSH for continued growth. At a later, unknown time, the domi- nant follicle transfers primary gonadotrophic dependence from FSH to LH and has the ability to survive without FSH (Ginther, 2000). Additional follicular development in llamas is suppressed as long as the dominant follicle main- tains its mature size (Bravo et al., 1990a,b) and presumably its functionality as a dominant follicle. As the inhibitory substances, such as inhibin, produced by the mature dom- inant follicle decline prior to atresia, a new surge of FSH occurs but the subordinate follicles from the previous wave are unable to respond to the new stimulus.

The follicular diameter at which dominance and LH- dependence occur in alpacas has not been reported. Bravo et al. (1990a,b) used ultrasonography to conclude that there was only ever one follicle with a diameter greater than 6 mm in llamas. Adams et al. (1990) found the mean max- imum diameter of the largest subordinate follicle to be 5.3 ± 0.3 mm and observed no subordinate follicles greater than 7 mm diameter in llamas.

8. Ovarian activity in unmated females

It is not known how long the development of primor- dial follicle to mature oocyte takes in camelids, but could be several months, as seen in other domestic livestock. Follic- ular waves proceed in the absence of progesterone when females remain unmated as camelids are induced ovula- tors (Bravo et al., 1990a,b). Increasing plasma oestradiol concentration during follicular growth in unmated females does not elicit a pre-ovulatory surge of LH in camelids (Bravo et al., 1990a,b; Vaughan, 2001).

The existing dominant follicle regresses by atresia over a period of 3–8 days, allowing emergence of a new cohort of follicles within 2–3 days following the first decrease in size of the dominant follicle (Bravo et al., 1990a,b). Therefore, as the existing dominant follicle is regressing, another follicle

destined to be the next dominant follicle has begun growth, in such a way that the growth patterns of successive large follicles appear to overlap when represented in pictorial profiles. Growth and regression of successive large follicles

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J. Vaughan / Animal Reprod

ay overlap in camelids by 1–4 days so that as one follicle s regressing, another is about to become dominant (Bravo t al., 1990a,b). At any given time during non-ovulatory ollicular waves, one would expect to find a follicle of at east 6 or 7 mm diameter (Adams et al., 1990; Vaughan et l., 2004).

Follicle waves continue during lactation in non- regnant females. Lactation is associated with a smaller aximum diameter of the dominant follicle and a shorter

nter-wave interval (Adams et al., 1990; Ratto et al., 2003).

. Ovarian activity in mated females: ovulation

The LH surge required for ovulation in camelids is stim- lated by mating rather than by feedback of follicular estrogen, hence the term ‘induced’ or ‘reflex’ ovulation Fernandez-Baca et al., 1970). Males copulate in sternal ecumbency for an average of 15–20 min (range 3–65 min) ut there is no relationship between copulation time and

nduction of ovulation (Fernandez-Baca et al., 1970) nor s there any difference in duration of copulation between lpacas conceiving and those failing to conceive (Knight t al., 1992; Vaughan et al., 2003). Males penetrate the ervix with their penis during copulation and deposit emen into both uterine horns during multiple ejaculations Lichtenwalner et al., 1996a,b; Bravo, 2002). An ovulation- nducing factor in the semen (Adams and Ratto, 2001; anco et al., 2007) and mechanical stimulation of the cervix y the penis during coitus are primarily responsible for he neuro-endocrine reflex of ovulation, presumably begin- ing with a sudden and large release of GnRH (Kauffman nd Rissman, 2006). Visual, auditory, olfactory, physical nd pheromonal cues, including vocalisation by the male known as ‘orgling’) also contribute to transmission of neu- al signals to the brain of the female, as some unmated emales in the presence of a mating pair can ovulate with- ut coitus (Fernandez-Baca et al., 1970).

The first significant rise in plasma LH in alpacas and lla- as occurs 15–40 min after the initiation of mating (Bravo

t al., 1991). Peak LH occurs 2–3 h after mating, and is basal y 4–7 h up to 12 h after joining (Bravo, 1990; Bravo et l., 1991; Aba and Forsberg, 1995; Aba, 1998). LH concen- rations do not differ in amplitude or duration between emales that conceive and those that fail to conceive (Aba, 998).

The LH surge triggers resumption of meiosis in the ocyte, disruption of cumulus cell cohesiveness, rupture f the follicular wall to release the cumulus-oocyte com- lex and a decline in plasma oestradiol levels over a period f approximately 24 h (Bravo et al., 1990a,b; Vaughan, 001). Granulosa cells remaining in the post-ovulatory fol-

icle luteinise and form a corpus luteum, which produces rogesterone necessary for uterine preparation and main- enance of pregnancy (Rajkovic et al., 2006).

The ability to ovulate in response to mating depends artly on the diameter and developmental status of the ominant follicle at the time of mating: follicles <6 mm

iameter follicles in alpacas, llamas and vicunas fail to ovu-

ate; dominant follicles 6–15 mm diameter are capable of vulation (Adams et al., 1989, 1990; Bravo et al., 1991; guero et al., 2001; Chaves et al., 2002; Ratto et al., 2003;

ience 124 (2011) 237–243 241

Vaughan et al., 2003). Ovulatory capability is not necessar- ily related to the fertility of the oocyte contained within the ovulating follicle. It is likely that growing and early static- phase follicles contain oocytes more likely to be fertilised successfully (Ratto et al., 2003; Vaughan et al., 2003).

The LH surge in females in response to copulation may be dependent on follicle size in alpacas and llamas. Females with follicles 4–5 mm diameter released less LH over a 6-h post-mating period and ovulation failed to occur compared with females with follicles >5 mm diameter in one study (Bravo et al., 1991). However, another study did not show any correlation between plasma oestradiol and the amount of LH released after GnRH stimulation in alpacas and llamas (Aba and Forsberg, 1995). Repeated copulatory periods at 6 or 24 h after the initial event do not apparently increase LH significantly, suggesting that the hypothalamus or pituitary gland may undergo a period of refractoriness, possibly due to depletion of pituitary LH or down-regulation of GnRH receptors in the pituitary gland (Bravo et al., 1992).

The ovulation-inducing factor found in the seminal plasma of male alpacas and llamas also plays a role in induc- ing ovulation but effects on post-coital LH secretion in the female are yet to be studied. The ovulation-inducing factor has a dose-dependent effect on ovulation rate and corpus luteum form and function in llamas (Tanco et al., 2007).

The interval between mating and ovulation is approx- imately 30 h (range 24–36 h) in the alpaca and llama (San Martin et al., 1968; Bourke et al., 1995; Adams and Ratto, 2001; Ratto et al., 2006) and is not affected by follicle diam- eter at the time of mating (Adams et al., 1990). There is no effect of lactational status or ability to conceive on the interval from mating to ovulation (Adams et al., 1990).

Ovulation occurs from the surface of the ovary at any point apart from the hilus, with equal frequency from the left and right ovaries even though most pregnancies are located in the left uterine horn (Fernandez-Baca et al., 1970; Adams et al., 1989; Vaughan and Tibary, 2006). The origin of the oocyte from the left or right ovary has no effect on the likelihood of pregnancy (Vaughan et al., 2003). Generally, there is only one dominant follicle but occasionally there are two (5–15%), or very rarely three, dominant follicles (Fernandez-Baca et al., 1970; Bravo et al., 1993).

Two to 5 days post-coitus, a corpus luteum develops at the site of ovulation on the ovary and is associated with ris- ing plasma progesterone concentrations from 4 to 6 days after mating (Aba et al., 1995; Ratto et al., 2006). There is a close temporal relationship between corpus luteum diameter, measured by ultrasonography or rectal palpa- tion, and plasma progesterone while the corpus luteum is growing. The corpus luteum reaches a maximum diame- ter of 8–15 mm with maximum progesterone output 7–9 days after mating in alpacas and llamas (Aba et al., 2000). There is a decrease in plasma progesterone 1–3 days before the morphological decrease in corpus luteum diameter (Adams et al., 1991). The progesterone output of the cor- pus luteum decreases from 9 to 11 days after mating and corpus luteum diameter is halved by 12 days after mat-

ing (Adams et al., 1990; Ratto et al., 2006). The presence of a corpus luteum in llamas and alpacas is usually asso- ciated with a circulating progesterone level greater than 1–2 ng/mL (3.2–6.4 nmol/L) (Sumar et al., 1988; Aba et al.,

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242 J. Vaughan / Animal Reprod

1995). Females that fail to conceive become sexually recep- tive approximately 12–14 days after mating as plasma progesterone levels decline below 6 nmol/L (2 ng/mL).

Recruitment of follicles and a new follicular wave starts soon after ovulation (Adams et al., 1990). The dominant fol- licle in camelids in the first wave after mating is detected via ultrasound approximately 2 days after ovulation (Ratto et al., 2003). The presence of a corpus luteum, and there- fore elevated plasma progesterone, alters follicular wave dynamics in llamas, alpacas and vicunas by shortening the inter-wave interval and reducing maximum follicu- lar diameter attained during each follicular wave (Adams et al., 1990; Vaughan, 2001; Chaves et al., 2002; Aba et al., 2005). Peak values of plasma oestradiol in alpacas and llamas can be up to three times higher during follicular growth in the absence of a corpus luteum in non-pregnant females compared with peak plasma oestradiol concentra- tions measured in pregnant females. These results suggest that progesterone from the corpus luteum exerts a negative influence on follicle activity in animals that have ovulated (Aba et al., 2000) possibly by effects on LH. The effect that progesterone exerts on follicular growth described in camelids is most likely mediated via negative feedback of progesterone on the hypothalamic–pituitary axis. Suppres- sion of hypothalamic GnRH pulses reduces pituitary LH secretion which reduces follicular diameter and inter-wave interval.

9.1. Luteolysis

Regression of the corpus luteum in camelids is under the influence of pulsatile secretion of prostaglandin F2� (PGF2�) secretion from the uterine horns (Aba et al., 2000; Vaughan and Tibary, 2006) with repeated pulses of great- est concentration being secreted from 8 to 9 days after mating to 12 days after mating (Aba et al., 1995, 2000). The role of oxytocin in luteolysis remains unknown. It has been postulated that PGF2� secretion from the left uter- ine horn may induce luteolysis of a corpus luteum in the right ovary via a local veno-arterial pathway (Fernandez- Baca et al., 1979; Del Campo et al., 1996) and may explain why embryos derived from right-sided ovulations migrate to the left uterine horn for successful gestation.

10. Ovarian activity in pregnant females

The corpus luteum is the major source of progesterone throughout pregnancy and its presence is required to main- tain pregnancy (Sumar, 1988). The embryonic signal for maternal recognition of pregnancy remains unknown, but must be transmitted as early as 8–10 days after mating in order to rescue the corpus luteum of pregnancy (Aba et al., 1997). There is a temporary decline in plasma progesterone 8–12 days after mating during the period of maternal recognition of pregnancy, levels reach a peak approxi- mately 20 days after mating, then concentrations vary throughout gestation but remain greater than 6 nmol/L

(2 ng/mL) (Adams et al., 1991; Aba et al., 1995). Proges- terone is higher in pregnant than non-pregnant females 8 days after mating but is not known whether this occurs because there is an embryo present in pregnant females

cience 124 (2011) 237–243

or there is a reduced ability to secrete progesterone in females that fail to conceive (Sumar, 1999). Lactation does not appear to affect progesterone levels during gestation (Adams et al., 1990).

Ovarian follicular activity continues in a wave-like fash- ion during pregnancy in camelids. Progesterone appears to exerts a negative effect on folliculogenesis throughout gestation as there is a decrease in the number of follicles detected, smaller maximum diameter of the dominant fol- licle, reduced inter-wave interval and less prominent day to day growth and regression profiles of dominant follicles up until 6 months of gestation (Adams et al., 1990; Aba, 1995). From 7 months gestation, only 3–4 mm diameter fol- licles are present on the ovaries of alpacas indicating waves become less prominent towards the end of gestation (Bravo and Varela, 1993). The first follicular wave post-partum is usually observed within a week of parturition (Aba et al., 1998).

Conflict of interest statement

The author, Jane Vaughan, does not have a financial or personal relationship with other people or organisa- tions that could inappropriately influence or bias the paper entitled “Ovarian function in South American camelids (alpacas, llamas, vicunas, guanacos)”.

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