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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. Femalesexhibit waves of ovarian follicular growth and are induced ovulators and therefore do not

eywords:amelidlpacalamaicunavary

exhibit oestrous cycles in the manner of spontaneously ovulating species such as sheep andcattle. There is much variation in inter-wave interval among camelid species (alpaca/llama10–22 days, vicuna 4–11 days), within species and within individual animals as the range ofeach phase of follicular growth is wide. Ovulation occurs 24–30 h after mating and luteolysisoccurs 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 alpacaVicugna pacos) has been domesticated from the vicunaVicugna vicugna) and the llama (Lama glama) domesti-ated from the guanaco (Lama guanicoe) (Kadwell et al.,001). South American camelids resemble each other inhape, but vary in size, fleece characteristics and geograph-cal distribution (Novoa, 1970). Vicunas are the smallest ofhe 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 southernndes. Historically, alpacas (55–85 kg) were grown in Peru,olivia, Chile and Argentina for their fleece, and llamas130–180 kg) were used as beasts of burden and both usedor 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 theiroft, fine, light-weight wool that comes in a range of colours

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

E-mail address: vaughan@ava.com.au.

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 relatedto dromedary (one-humped) and Bactrian (two-humped)camels.

The reproductive physiology of camelids differs to thatof other domestic livestock. Female camelids exhibit wavesof ovarian follicular growth (Adams et al., 1990; Vaughanet al., 2004) and are induced ovulators (San Martin et al.,1968) and therefore do not exhibit oestrous cycles in themanner of spontaneously ovulating species of domesticlivestock. Unmated, non-ovulatory females are sexuallyreceptive most of the time, regardless of the stage of ovar-ian follicular development (Sumar, 1983). Males mate insternal 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 camelidsbecause males take 1–3 years to reach puberty and femalesexhibit an extended gestation.

Ovarian function remains relatively poorly understood

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

uction Science 124 (2011) 237–243

Table 1Ovarian dimensions in camelids.

Alpaca Llama Vicuna Guanaco

Right ovaryLength cm 1.6 ± 0.3 1.3–2.5 1.3 1.5Depth cm 1.1 ± 0.2 1.4–2 0.7 n/aa

Width cm 1.1 ± 0.2 0.6–1 1.0 n/aLeft ovary

Length cm 1.6 ± 0.3 1.5–2.5 1.2 1.5Depth cm 1.1 ± 0.2 1.5–2.5 0.7 n/aWidth 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) andthe 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 offolliculogenesis and ovulation.

2. Ovarian development

During embryological development, the gonads arisefrom the urogenital ridges in close proximity to pairedparamesonephric (Mullerian) ducts that give rise to theinternal genitalia. The ovaries do not exhibit structural dif-ferentiation until well after sex determination. Primordialfollicles develop some months into gestation and are seenas 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 isunknown in South American camelids but occurs at 8–12weeks in camels (Marai et al., 1990). Oocytes are arrestedin prophase of the first meiosis and do not progress furtheruntil shortly before ovulation in the post-pubertal camelid.Primary follicles, characterised by an oocyte surroundedby cuboidal granulosa cells, develop in camels from 20 to24 weeks of gestation (Marai et al., 1990). Timing of firstappearance 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 ofgranulosa cells and a thecal cell layer around the basementmembrane with numerous small blood vessels (Rajkovic etal., 2006). Early folliculogenesis to the stage of pre-antralfollicles appears to be directed by signals within the ovaryand is independent of gonadotrophin stimulation. Thereis also communication within the ovary amongst oocytes,granulosa and theca cells (Parker and Schimmer, 2006).The onset of folliculogenesis occurs immediately after thefirst follicles are formed, and continues until the end of thereproductive period (12–18 years in alpacas), even throughpregnancy and lactation (Adams et al., 1990). Follicles arealso degenerating during foetal development because alack of follicle stimulating hormone (FSH) does not supportfurther follicular development (Rajkovic et al., 2006).

Regulation of terminal follicular growth beyond thesmall antral stage is a gonadotrophin-dependent pro-cess occurring after puberty and corresponding toinitiation of follicular waves, selection of dominantfollicles and terminal maturation of pre-ovulatory folli-cles (Monniaux et al., 1997). Gonadotrophic hormonessecreted from the pituitary gland develop a complexfeedback/feed-forward system with the ovaries, knownas the hypothalamic–pituitary–gonadal axis, allowing fol-licles to proceed beyond the early, pre-antral stages(Rajkovic et al., 2006). Formation of the antrum signalstransition from intra-ovarian to extra-ovarian control andonce a follicle has entered the growing pool, it is irreversiblycommitted 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 thecalcells (Rajkovic et al., 2006). Inhibin, secreted by the granu-losa cells of the dominant follicle, feeds back to the pituitaryto inhibit FSH secretion. These findings have yet to beclearly elucidated in camelids. Granulosa cells of mostearly-antral follicles undergo apoptosis and death as theyare not rescued by FSH.

3. Adult reproductive anatomy

Camelids have a bicornuate uterus with the tips of thehorns blunt and rounded, and a single cervix, whose lumencontains 2–3 rings/spiral folds of mucosa. The uterus islocated within the pelvic canal or at the pelvic brim in thenon-gravid state (Vaughan and Tibary, 2006). Each uterinehorn ends in a long and tortuous oviduct which joins theuterine horn to the ovarian bursa (Sumar, 1983). There isa prominent papilla at the uterotubal junction (Vaughanand Tibary, 2006). The ampulla and ovarian section of theoviduct are the most coiled parts, the isthmus less so. Thefimbria are contained within the bursa, near the ovary andthe ovarian bursa, is formed by a fold of the mesosalpinxand 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 overthe 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 andcorpora lutea project prominently from the surface of theovary (Adams et al., 1989). All growing follicles in camelidsare spherical, probably related to the prominent protru-sion of 85% of the follicle from the surface the ovary (DelCampo and Del Campo, 1995). Oocytes range from 172 to200 �m in size. Immature oocytes in llamas have a distinctand large germinal vesicle with a dark nucleolus. Matureoocytes display a metaphase plate surrounded by a darkarea easily found at 20–40× magnification (Del Campo andDel Campo, 1995).

4. Puberty

Time of first ovulation depends on age at first matingas camelids are induced ovulators. Information on ovarianfollicular 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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Fig. 1. Schematic representation of follicular waves in alpacas and lla-mas. Mating induces ovulation of the dominant follicle and formationof a corpus luteum. Failure to conceive leads to luteolysis of the corpusluteum. 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 recordedVaughan and Tibary, 2006). The age at which ovarian activ-ty begins and conception occurs is dependent on nutritionnd live weight. Domestic camelids are generally matedhen they have attained two-thirds of their adult weight

Smith et al., 1994), from 12 months of age in alpacas and8 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 displayistinct periods of overt oestrus. Non-pregnant femalesppear receptive to males on most occasions regardlessf stage of follicular development (England et al., 1971) aslasma progesterone levels remain low (Fernandez-Baca,993). Time taken to adopt sternal recumbency (demon-tration of sexual receptivity) is not a reliable indicatorf 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 (Ferrert al., 1999). The sexual behaviour patterns of camelidsay 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 femaleamelids, 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, oestradioloncentration may drop long enough for sexual receptivityo decline (Brown, 2000) and these females appear indif-erent to the male rather than non-receptive.

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

scape are most indicative of reproductive status (Pollard etl., 1994). Sexually inexperienced alpaca females are moreikely to kick and attempt escape but less likely to spitr threaten the male compared with experienced femalesPollard et al., 1993).

. Seasonality

Alpacas and llamas are considered non-seasonal breed-rs as ovarian follicular activity occurs throughout theear and season (photoperiod, rainfall or temperature)oes not affect the number of follicles >6 mm observed onhe ovaries (Bravo and Sumar, 1989). However, breedingnd 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 abundantnd better quality (Fernandez-Baca, 1993). Vicunas breedn the high altitude rangelands of South America in autumnAguero et al., 2001).

Modified from Senger (2003).

7. Folliculogenesis

Folliculogenesis, or growth and differentiation of theoocyte and associated cells, is a highly regulated processrelying 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 maleexhibit continuous renewing of terminally growing fol-licles defined as follicular waves. The number of antralfollicles 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). Otherstudies have described growth of successive large anovu-latory follicles in unmated females but did not describe aperiodic fluctuation in follicle numbers consistent with theexistence of a wave-like pattern of growth (Bravo et al.,1990a,b; Bourke et al., 1992).

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

The duration of follicular growth is unknown incamelids but greater than that of a follicle wave observedusing ultrasonography. The first stages of follicular growthare difficult to estimate accurately and are not consid-ered in the estimation of the total duration of a follicularwave. After new follicle emergence at the beginning of afollicular wave, follicle growth may be divided into threephases. The growth phase of the follicle in alpacas and lla-mas takes about 5–9 days. The mature phase, when thefollicle 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 invicunas (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 amongcamelid species (alpaca/llama 10–22 days, vicuna 4–11days), within species and within individual animals as therange of each phase of follicular growth is wide (Adams etal., 1990; Bravo et al., 1990a,b; Aguero et al., 2001; Vaughanet al., 2004). Using a ‘mean inter-wave interval’ withina particular camelid species should therefore be avoidedas it does not accurately describe what is occurring in anindividual animal nor allow prediction of the optimumtime of breeding (Vaughan et al., 2004). A longer inter-wave interval has been associated with a larger maximumfollicle 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 liveweight amongst alpacas (Vaughan et al., 2004).

Follicular growth rates of 0.5–0.8 mm/day (Adams etal., 1989, 1990) and 0.9 mm/day (Chaves et al., 2002) inllamas, 0.4 mm/day in alpacas (Vaughan et al., 2004) and1.8 mm/day in vicunas (Aguero et al., 2001; Miragaya etal., 2004) have been measured using ovarian ultrasonogra-phy. In unmated alpacas, there is similar follicular growthof the dominant follicle from Days 0 to 10 after new waveemergence regardless of subsequent inter-wave interval(Vaughan et al., 2004).

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

7.1. Hormonal control of folliculogenesis

In mammals, gonadotrophin-releasing hormone(GnRH) is secreted into the hypothalamo-hypophysealportal system in a pulsatile manner to stimulate theepisodic release of gonadotrophins into the systemiccirculation. GnRH has yet to be measured in camelids dueto 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 LHresponsible for follicle wave emergence, follicle growth anddominant follicle selection observed in some domestic live-stock have yet to be identified in camelids due to poorsensitivity of hormone assays (Aba et al., 1999). Successfuluse of porcine and ovine FSH to induce follicular growthin multiple ovulation and embryo transfer programs inalpacas and llamas supports the hypothesis of FSH inducingemergence 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 folliclesize 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 maximaljust before the plateau of follicle growth is reached andthen 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 fromamong a cohort of follicles in a wave is unknown butappears 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 releasehigh concentrations of oestrogen and inhibin, which actlocally by stimulating growth and cell differentiation ofthe granulosa and by the indirect effect of feedback inhi-bition of FSH secretion, is central to selection of a givenfollicle for maturation and ovulation (Ginther, 2000). Theconcentration of FSH during follicle growth decreases sothat it is inadequate for subordinate follicular growth anddelays onset of the next follicular wave, but the domi-nant follicle still requires low concentrations of FSH forcontinued growth. At a later, unknown time, the domi-nant follicle transfers primary gonadotrophic dependencefrom FSH to LH and has the ability to survive withoutFSH (Ginther, 2000). Additional follicular development inllamas is suppressed as long as the dominant follicle main-tains its mature size (Bravo et al., 1990a,b) and presumablyits functionality as a dominant follicle. As the inhibitorysubstances, such as inhibin, produced by the mature dom-inant follicle decline prior to atresia, a new surge of FSHoccurs but the subordinate follicles from the previous waveare unable to respond to the new stimulus.

The follicular diameter at which dominance and LH-dependence occur in alpacas has not been reported. Bravoet al. (1990a,b) used ultrasonography to conclude that therewas only ever one follicle with a diameter greater than6 mm in llamas. Adams et al. (1990) found the mean max-imum diameter of the largest subordinate follicle to be5.3 ± 0.3 mm and observed no subordinate follicles greaterthan 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 beseveral months, as seen in other domestic livestock. Follic-ular waves proceed in the absence of progesterone whenfemales remain unmated as camelids are induced ovula-tors (Bravo et al., 1990a,b). Increasing plasma oestradiolconcentration during follicular growth in unmated femalesdoes not elicit a pre-ovulatory surge of LH in camelids(Bravo et al., 1990a,b; Vaughan, 2001).

The existing dominant follicle regresses by atresia overa period of 3–8 days, allowing emergence of a new cohort offollicles within 2–3 days following the first decrease in sizeof the dominant follicle (Bravo et al., 1990a,b). Therefore, asthe 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 largefollicles appear to overlap when represented in pictorialprofiles. Growth and regression of successive large follicles

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ay overlap in camelids by 1–4 days so that as one follicles regressing, another is about to become dominant (Bravot al., 1990a,b). At any given time during non-ovulatoryollicular waves, one would expect to find a follicle of ateast 6 or 7 mm diameter (Adams et al., 1990; Vaughan etl., 2004).

Follicle waves continue during lactation in non-regnant females. Lactation is associated with a smalleraximum 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 follicularestrogen, hence the term ‘induced’ or ‘reflex’ ovulationFernandez-Baca et al., 1970). Males copulate in sternalecumbency 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) nors there any difference in duration of copulation betweenlpacas conceiving and those failing to conceive (Knightt al., 1992; Vaughan et al., 2003). Males penetrate theervix with their penis during copulation and depositemen into both uterine horns during multiple ejaculationsLichtenwalner 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 cervixy the penis during coitus are primarily responsible forhe neuro-endocrine reflex of ovulation, presumably begin-ing with a sudden and large release of GnRH (Kauffmannd Rissman, 2006). Visual, auditory, olfactory, physicalnd pheromonal cues, including vocalisation by the maleknown as ‘orgling’) also contribute to transmission of neu-al signals to the brain of the female, as some unmatedemales 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 basaly 4–7 h up to 12 h after joining (Bravo, 1990; Bravo etl., 1991; Aba and Forsberg, 1995; Aba, 1998). LH concen-rations do not differ in amplitude or duration betweenemales that conceive and those that fail to conceive (Aba,998).

The LH surge triggers resumption of meiosis in theocyte, disruption of cumulus cell cohesiveness, rupturef the follicular wall to release the cumulus-oocyte com-lex and a decline in plasma oestradiol levels over a periodf 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 producesrogesterone necessary for uterine preparation and main-enance of pregnancy (Rajkovic et al., 2006).

The ability to ovulate in response to mating dependsartly on the diameter and developmental status of theominant 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 ofvulation (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 theovulating follicle. It is likely that growing and early static-phase follicles contain oocytes more likely to be fertilisedsuccessfully (Ratto et al., 2003; Vaughan et al., 2003).

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

The ovulation-inducing factor found in the seminalplasma of male alpacas and llamas also plays a role in induc-ing ovulation but effects on post-coital LH secretion in thefemale are yet to be studied. The ovulation-inducing factorhas a dose-dependent effect on ovulation rate and corpusluteum 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 (SanMartin 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 isno effect of lactational status or ability to conceive on theinterval from mating to ovulation (Adams et al., 1990).

Ovulation occurs from the surface of the ovary at anypoint apart from the hilus, with equal frequency from theleft and right ovaries even though most pregnancies arelocated in the left uterine horn (Fernandez-Baca et al., 1970;Adams et al., 1989; Vaughan and Tibary, 2006). The originof the oocyte from the left or right ovary has no effect on thelikelihood of pregnancy (Vaughan et al., 2003). Generally,there is only one dominant follicle but occasionally thereare 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 atthe site of ovulation on the ovary and is associated with ris-ing plasma progesterone concentrations from 4 to 6 daysafter mating (Aba et al., 1995; Ratto et al., 2006). Thereis a close temporal relationship between corpus luteumdiameter, measured by ultrasonography or rectal palpa-tion, and plasma progesterone while the corpus luteum isgrowing. The corpus luteum reaches a maximum diame-ter of 8–15 mm with maximum progesterone output 7–9days after mating in alpacas and llamas (Aba et al., 2000).There is a decrease in plasma progesterone 1–3 days beforethe 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 andcorpus luteum diameter is halved by 12 days after mat-

ing (Adams et al., 1990; Ratto et al., 2006). The presenceof a corpus luteum in llamas and alpacas is usually asso-ciated with a circulating progesterone level greater than1–2 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 plasmaprogesterone levels decline below 6 nmol/L (2 ng/mL).

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

9.1. Luteolysis

Regression of the corpus luteum in camelids is underthe 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 aftermating to 12 days after mating (Aba et al., 1995, 2000).The role of oxytocin in luteolysis remains unknown. It hasbeen postulated that PGF2� secretion from the left uter-ine horn may induce luteolysis of a corpus luteum in theright ovary via a local veno-arterial pathway (Fernandez-Baca et al., 1979; Del Campo et al., 1996) and may explainwhy embryos derived from right-sided ovulations migrateto the left uterine horn for successful gestation.

10. Ovarian activity in pregnant females

The corpus luteum is the major source of progesteronethroughout pregnancy and its presence is required to main-tain pregnancy (Sumar, 1988). The embryonic signal formaternal recognition of pregnancy remains unknown, butmust be transmitted as early as 8–10 days after mating inorder to rescue the corpus luteum of pregnancy (Aba et al.,1997). There is a temporary decline in plasma progesterone8–12 days after mating during the period of maternalrecognition of pregnancy, levels reach a peak approxi-mately 20 days after mating, then concentrations varythroughout 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 8days after mating but is not known whether this occursbecause there is an embryo present in pregnant females

cience 124 (2011) 237–243

or there is a reduced ability to secrete progesterone infemales that fail to conceive (Sumar, 1999). Lactation doesnot 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 appearsto exerts a negative effect on folliculogenesis throughoutgestation as there is a decrease in the number of folliclesdetected, smaller maximum diameter of the dominant fol-licle, reduced inter-wave interval and less prominent dayto day growth and regression profiles of dominant folliclesup 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 wavesbecome less prominent towards the end of gestation (Bravoand Varela, 1993). The first follicular wave post-partum isusually observed within a week of parturition (Aba et al.,1998).

Conflict of interest statement

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

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