Animal Reproduction (AR)
Animal Reproduction (AR)
Conference Paper

Natural and controlled ovulation in South American camelids

Gregg P. Adams, Marcelo H. Ratto, Rodrigo A. Carrasco

Downloads: 1
Views: 721


The four species of New World camelids and 2 species of Old World camelids derived from a common ancestor in North America. The reproductive characteristics, particularly those involving ovarian function and ovulation, are remarkably similar among the 6 living species of camelids, so much so that interspecies hybrids of nearly all possible combinations have been documented. Camelids are induced-ovulators, triggered by an ovulation-inducing factor in seminal plasma. The timing and mechanism of endocrine events leading to ovulation are discussed, as well as the discovery, identification and mode of action of the seminal factor responsible. The applied aspects of our present understanding are discussed with specific reference to controlled induction of ovulation, ovarian synchronization, and superovulation. Emphasis has been given to the literature on llamas and alpacas, with some reference to studies done in wild species of South American camelids and Old World camels.


Camelid, ovary, ovulation, superovulation, synchronization.


Aba MA, Forsberg M, Kindhal H, Sumar J, Edqvist L. 1995. Endocrine changes after mating in pregnant and non-pregnant llamas and alpacas. Acta Vet Scand, 36:489-498.

Aba MA, Miragaya MH, Chaves MG, Capdevielle EF, Rutter B, Aguero A. 2005. Effect of exogenous progesterone and eCG treatment on ovarian follicular dynamics in vicuñas (Vicugna vicugna). Anim Reprod Sci, 86:153-161.

Adam CL, Moir CE, Shiach P. 1989. Plasma progesterone concentrations in pregnant and nonpregnant llamas (Lama glama). Vet Rec, 125:618-620.

Adams GP, Griffin PG, Ginther OJ. 1989. In situ morphologic dynamics of ovaries, uterus, and cervix in llamas. Biol Reprod, 41:551-558.

Adams GP, Sumar J, Ginther OJ. 1990. Effects of lactational and reproductive status on ovarian follicular waves in llamas (lama glama). J Reprod Fertil, 90:535-545.

Adams GP, Sumar J, Ginther OJ. 1991. Form and function of the corpus luteum in llamas. Anim Reprod Sci, 24:127-138.

Adams GP. 1994. Control of ovarian follicular waves dynamics in cattle: implications for synchronization and superstimulation. Theriogenology, 41:19-24.

Adams GP, Ratto MH, Huanca W, Singh J. 2005. Ovulation - inducting factor in the seminal plasma of llamas and alpacas. Biol Reprod, 73:452-457

Adams GP, Singh J, Baerwald AR. 2012. Large animal models for the study of ovarian follicular dynamics in women. Theriogenology, 78:1733-1748.

Adams GP, Ratto MH, Silva ME, Carrasco RA. 2016. Ovulation-inducing factor (OIF/NGF) in seminal plasma: a review and update. Reprod Domest Anim, 51(suppl. 2):4-17.

Bogle OA, Ratto MH, Adams GP. 2012. Ovulation-inducing factor induces LH secretion from pituitary cells. Anim Reprod Sci, 133:117-122.

Bravo PW, Fowler ME, Stabenfeldt GH. 1990. Endocrine response in the llama to copulation. Theriogenology, 33:891-899.

Bravo PW, Stabenfeldt GH, Lasley BL, Fowler ME. 1991. The effect of ovarian follicle size on pituitary and ovarian responses to copulation in domesticated South American camelids. Biol Reprod, 45:553-559.

Bravo PW, Stabenfeldt GH, Fowler ME, Lasley BL. 1992. Pituitary response to repeated copulation and/or gonadotropin-releasing hormone administration in llamas and alpacas. Biol Reprod, 47:884-888.

Carrasco R, Singh J, Adams GP. 2016. The dynamics of trkA expression in the bovine ovary are associated with a luteotrophic effect of ovulation-inducing factor/nerve growth factor (OIF/NGF). Reprod Biol Endocrinol, 14:47. doi: 10.1186/s12958-016-0182-9.

Chaves MG, Aba MA, Aguero A, Egey J, Berestin V, Rutter B. 2002. Ovarian follicular wave pattern and the effect of exogenous progesterone on follicular activity in non-mated llamas. Anim Reprod Sci, 69:37-46.

Concanon P, Hodgson B, Lein D. 1980. Reflex LH release in estrous cats following single and multiple copulations. Biol Reprod, 23:111-117.

Del Campo MR, Del Campo CH, Adams GP, Mapletoft RJ. 1995. The application of new reproductive technologies to South American camelids. Theriogenology, 43:21-30.

Dissen GA, Hill DF, Costa ME, Les Dees CW, Lara HE, Ojeda SR. 1996. A role for trkA nerve growth factor receptors in mammalian ovulation. Endocrinology, 137:198-209.

Dissen GA, Parrott JA, Skinner MK, Hill DF, Costa MA, Ojeda SR. 2000. Direct effects of nerve growth factor on thecal cells from antral ovarian follicles. Endocrinology, 141:4736-4750.

England BG, Foot WC, Matthews DH, Cardozo AG, Riera S. 1969. Ovulation and corpus luteum function in the llama (lama glama). J Endocrinol, 45:505-513.

Fatnassi M, Cebrian-Perez JA, Salhi I, Perez-Pe R, Seddik MM, Casao A, Khorchani T, Muiño-Blanco T, Hammadi M. 2017. Identification of β-nerve growth factor in dromedary camel seminal plasma and its role in induction of ovulation in females. Emir J Food Agric, 29:293-299.

Fernandez-Baca S, Hansel W, Novoa C. 1970a. Corpus luteum function in the alpaca. Biol Reprod, 3:252-261.

Fernandez-Baca S, Madden DHL, Novoa C. 1970b. Effect of different mating stimuli on induction of ovulation in the alpaca. J Reprod Fertil, 22:261-267.

Fink G. 1988. Gonadotropin secretion and its control. In: Knobil E, Neill J (Ed.). The Physiology of Reproduction. New York, NY: Raven Press. pp. 1349-1377.

Heintzman PD, Zazula GD, Cahill JA, Reyes AV, MacPhee RDE, Shapiro B. 2015. Genomic data from extinct North American Camelops revise camel evolutionary history. Mol Biol Evol, 32:2433-2440.

Huanca W, Cordero A, Huanca T, Cardenas O, Adams GP, Ratto MH. 2009. Ovarian response and embryo production in llamas treated with eCG alone or with progestin vaginal sponges at the time of follicular wave emergence. Theriogenology, 72:803-808.

Jones EF, Bain JB, Odell WD. 1976. Postcoital luteinizing hormone release in male and female rabbits as determined by radioimmunoassay. Fertil Steril, 27:848-852.

Julio-Pipper M, Lara H, Bravo JA, Romero C. 2006. Effects of nerve growth factor (NGF) o blood vessels area and expression of the angiongenic factors VEGF and TGFbeta 1 in the rat ovary. Reprod Biol Endocrinol, 4:57. doi: 10.1186/1477-7827-4-57.

Julio-Pipper M, Lozada P, Tapia V, Vega M, Miranda M, Vantman D, Ojeda SR, Romero C. 2009. Nerve growth factor induces vascular endotelial growth factor expression in granulosa cells via a TrkA receptor/mitogen-activated protein kinase-extracelullarly regulated kinase 2-dependent pathway. J Clin Endocrinol Metab, 94:3065-3071.

Karsch FJ. 1987. Central actions of ovarian steroids in the feedback regulation of pulsatile secretion of luteinizing hormone. Ann Rev Physiol, 49:365-382.

Kumar S, Sharma,VK, Singh S, Hariprasad GR, Mal G, Srinivasan A, Yadav S. 2013. Proteomic identification of camel seminal plasma: purification of β-nerve growth factor. Anim Reprod Sci, 136:289-295.

Leon JB, Smith BB, Timm KI, Le Cren G. 1990. Endocrine changes during preganancy, parturition and the early post-partum period in the llama (Lama glama). J Reprod Fertil, 88:503-511.

Levanti MB, Germaná A, Abbate F, Montalbano G, Vega JA, Germaná G. 2005. TrkA and p75NTR in the ovary of adult cow and pig. J Anat, 207:93-96.

Miragaya MH, Aba MA, Capdevielle EF, Ferrer MS, Chaves MG, Rutter B, Aguero A. 2004. Follicular activity and hormonal secretory profile in vicuna (Vicugna vicugna). Theriogenology, 61:663-671.

Murray FA, Grifo AP Jr, Parker. CF. 1983. Increased litter size in gilts by intrauterine infusion of seminal and sperm antigens before breeding. J Anim Sci, 56:895-900.

Pan W, Banks WA, Kastin AJ. 1998. Permeability of the blood–brain barrier to neurotrophins. Brain Res, 788:87-94.

Paolicchi F, Urquieta B, Del Valle L, Bustos-Obregon E. 1999. Biological activity of the seminal plasma of alpacas: stimulus for the production of LH by pituitary cells. Anim Reprod Sci, 54:203-210.

Ratto MH, Singh J, Huanca H, Adams GP. 2003. Ovarian follicular wave synchronization and fixed-time natural mating in llamas. Theriogenology, 60:1645-1656.

Ratto MH, Singh J, Huanca H, Adams GP. 2004. In vivo and in vitro maturation of llama oocyte. Theriogenology, 63:2445-2457.

Ratto MH, Huanca W, Singh J, Adams GP. 2005. Local versus systemic effect of ovulation-inducing factor in the seminal plasma of alpacas. Reprod Biol Endocrinol, 3:29. doi: 10.1186/1477-7827-3-29.

Ratto MH, Huanca W, Singh J, Adams GP. 2006. Comparison of the effect of natural mating, LH, and GnRH on interval to ovulation and luteal function in llamas. Anim Reprod Sci, 91:299-306.

Ratto MH, Leduc YA, Valderrama XP, Van Straten KE, Delbaere LT, Pierson RA, Adams GP. 2012. The nerve of ovulation-inducing factor in semen. Proc Natl Acad Sci USA, 109:15042-15047.

Ratto MH, Silva EM, Huanca W, Huanca T, Adams GP. 2013. Induction of superovulation in South American Camelids. Anim Reprod Sci, 136:164-169.

Riveros JL, Schuler G, Bonacic C, Hoffmann B, Chaves MG, Urquieta B. 2010. Ovarian follicular dynamics and hormonal secretory profiles in guanacos (Lama guanicoe). Anim Reprod Sci, 119:63-67.

San Martin M, Copaira M, Zuniga J, Rodriguez R, Bustinza G, Acosta L. 1968. Aspects of reproduction in the alpaca. J Reprod Fertil, 16:395-399.

Scherer CS. 2013. The Camelidae (Mammalia, Artiodactyla) from the quaternary of South America: cladistic and biogeographic hypotheses. J Mamm Evol, 20:45-56.

Silva ME, Smulders JP, Guerra M, Valderrama XP, Letelier C, Adams GP, Ratto MH. 2011. Cetrorelix suppresses the preovulatory LH surge and ovulation induced by ovulation-inducing factor (OIF) present in llama seminal plasma. Reprod Biol Endocrinol, 9:74. doi: 10.1186/1477-7827-9-74.

Silva ME, Colazo MG, Ratto MH. 2012a. GnRH dose reduction decreases pituitary LH release and pituitary response but does not affect corpus luteum (CL) development and function in llamas. Theriogenology, 77:1802-1810.

Silva ME, Recabarren MP, Recabarren SE, Adams GP, Ratto MH. 2012b. Ovarian estradiol modulates the stimulatory effect of ovulation-inducing factor (OIF) on pituitary LH secretion in llamas. Theriogenology, 77:1873-1882.

Silva ME, Ulloa-Leal C, Norambuena C, Fernandez A, Adams GP, Ratto MH. 2014. Ovulation inducing factor (OIF/NGF) from seminal plasma origin enhances Corpus luteum formation in llamas regardles the preovulatory follicle diameter. Anim Reprod Sci, 148:221-227.

Silva ME, Fernandez A, Ulloa-Leal C, Adams GP, Berland MA, Ratto MH. 2015. LH release and ovulatory response after intramuscular, intravenous, and intrauterine administration of β-nerve growth factor of seminal plasma origin in female llamas. Theriogenology, 84:1096-1102.

Silva ME, Ulloa-Leal C, Valderrama XP, Bogle OA, Adams GP, Ratto MH. 2017. Nerve growth factor from seminal plasma origin (spβ-NGF) increases CL vascularization and level of mRNA expression of steroidogenic enzymes during the early stage of corpus luteum development in llamas. Theriogenology, 103:69-75.

Skidmore JA, Billah M, Allen WR. 1996. The ovarian follicular wave pattern and induction of ovulation in the mated and non-mated one-humped camel (Camelus dromedaries). J Reprod Fertil, 106:185-192.

Skidmore J A, Billah M, Binns M, Short R V, Allen W R. 1999. Hybridizing Old and New World camelids: Camelus dromedarius x Lama guanicoe. Proc R Soc Lond B Biol Sci, 266:649-656.

Skidmore JA, Billah M, Short RV, Allen WR. 2001. Assisted reproductive techniques for hybridization of camelids. Reprod Fertil Dev, 13:647-652.

Skidmore JA, Adams GP, Billah M. 2009. Synchronisation of ovarian follicular waves in the dromedary camel (Camelus dromedarius). Anim Reprod Sci 114:249-255.

Skidmore JA. 2011. Reproductive physiology in female old world camelids. Anim Reprod Sci, 124:148-154.

Stanley HF, Kadwell M, Wheeler JC. 1994. Molecular evolution of the family Camelidae: a mitochondrial DNA study. Proc R Soc Lond B Biol Sci, 256(1345):1-6.

Sumar J, Fredriksson G, Alarcon V, Kindahl H, Edqvist LE. 1988. Levels of 15-keto-13, 14-dihydro-PFG2 alpha, progesterone and oestradiol-17 beta after induced ovulations in llamas and alpacas. Acta Vet Scand, 29:339-346.

Sumar J, Bravo PW, Foote WC. 1993. Sexual receptivity and time of ovulation in alpacas. Small Rumin Res, 11:143-150.

Tanco VM, Ratto MH, Lazzarotto M, Adams GP. 2011. Dose-response of female llamas to ovulation-inducing factor from seminal plasma. Biol Reprod, 85:452-456.

Tanco VM, Van Steelandt MD, Ratto MH, GP Adams. 2012. Effect of purified llama ovulation–inducing factor on ovarian function in cattle. Theriogenology, 78:1030-1039.

Turzillo AM, Nett TM. 1999. Regulations of the GnRH receptor gene expression in sheep and cattle. J Reprod Fertil Suppl, 54:75-86.

Ulloa-Leal C, Bogle OA, Adams GP, Ratto MH. 2014. Luteotrophic effect of ovulation-inducing factor/nerve growth factor present in the seminal plasma of llamas. Theriogenology, 81:1101-1107.

Vaughan J, Macmillan KL, D’Occhio MJ. 2004. Ovarian follicular wave characteristics in alpacas. Anim Reprod Sci, 80:353-361.

Vaughan J, Mihm M, Wittek T. 2013. Factors influencing embryo transfer success in alpacas - A retrospective study. Anim Reprod Sci, 136:194-204.

Welker F, Collins MJ, Thomas JA, Wadsley M, Brace S, Cappellini E, Turvey ST, Reguero M, Gelfo JN, Kramarz A, Burger J, Thomas-Oates J, Ashford DA, Ashton PD, Rowsell K, Porter DM, Kessler B, Fischer R, Baessmann C, Kaspar S, Olsen JV, Kiley P, Elliott JA, Kelstrup CD, Mullin V, Hofreiter M, Willerslev E, Hublin JJ, Orlando L, Barnes I, MacPhee RD. 2015. Ancient proteins resolve the evolutionary history of Darwin’s South American ungulates. Nature, 522:81-84.

Wheeler JC. 1995. Evolution and present situation of the South American Camelidae. Biol J Linn Soc, 54:271-295.

5b8fee5d0e88257a2859a5ec animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections