Induced ovulation (animals)

Last updated
Ovulation Aging-1.jpg
Ovulation

Induced ovulation is when a female animal ovulates due to an externally-derived stimulus during, or just prior, to mating, rather than ovulating cyclically or spontaneously. Stimuli causing induced ovulation include the physical act of coitus or mechanical stimulation simulating this, sperm and pheromones.

Contents

Ovulation occurs at the ovary surface and is described as the process in which an oocyte (female germ cell) is released from the follicle. Ovulation is a non-deleterious 'inflammatory response' which is initiated by a luteinizing hormone (LH) surge. [1] The mechanism of ovulation varies between species. In humans the ovulation process occurs around day 14 of the menstrual cycle, this can also be referred to as 'cyclical spontaneous ovulation'. However the monthly menstruation process is typically linked to humans and primates, [2] all other animal species ovulate by various other mechanisms.

Spontaneous ovulation is the ovulatory process in which the maturing ovarian follicles secrete ovarian steroids to generate pulsatile GnRH (the neuropeptide which controls all vertebrate reproductive function) release into the median eminence (the area which connects the hypothalamus to the anterior pituitary gland) to ultimately cause a pre-ovulatory LH surge. Spontaneously ovulating species go through menstrual cycles and are fertile at certain times based on what part of the cycle they are in. Species in which the females are spontaneous ovulators include rats, mice, guinea pigs, sheep, monkeys, and humans. [3]

Induced ovulation is the process in which the pre-ovulatory LH surge and therefore ovulation is induced by some component of coitus e.g. receipt of genital stimulation. Usually, spontaneous steroid-induced LH surges are not observed in induced ovulator species throughout their reproductive cycles, which indicates that GnRH release is absent or reduced due to lack of positive feedback action from steroid hormones. However, by contradiction, some spontaneously ovulating species can occasionally undergo mating-induced preovulatory LH surges. Species in which the females are induced ovulators include cats, rabbits, ferrets, and camels. [3] In 1985, Chen et al., used Bactrian camels to investigate the factor(s) that induce ovulation during breeding season. They monitored the camel ovaries for ovulation by rectal palpation following insemination of semen samples. Chen et al., concluded that in this particular camel species ovulation was induced by the seminal plasma, and not by the spermatozoa. [4]

Evolution

Although the evolution of these two types of ovulation is not well understood, the type of ovulation that would be advantageous in some species can be understood by looking at social groups. Animals that have large, complex social groups benefit from spontaneous ovulation as only the best males get to breed with females. If there are few males suitable for breeding it makes sense to spread out the times at which females are fertile, therefore increasing the proportion in which conception occurs. [5] This does not explain the evolution of ovulation in all species however, for example some species appear to show estrus synchronisation.

Mechanism

In spontaneous ovulators, estrogen secreted by the follicles as they grow and mature affects the release of GnRH, and therefore causes an LH surge.

Ovulation is triggered in induced ovulators by an LH surge from the anterior pituitary that is induced during mating. Animals this has been recorded in include rabbits, voles, ferrets and camels. [3] In some species such as the ferret, the duration of intromission has no effect on the LH surge, whereas in other species such as the cat these are related and higher levels of LH were produced by mating multiple times. In many species, for a LH surge to occur, little intromission is required.

The pathways in which information reaches the brain and causes GnRH release are not understood well; however, midbrain and brainstem noradrenergic neurones appear to be activated in response to intromission during mating. These neurones then go on to stimulate the mediobasal hypothalamic to release GnRH from the median eminence. [3] Most experiments on GnRH and LH release have been focused on spontaneous ovulators, though there have been studies completed on some induced ovulators (e.g., rabbits, ferrets). From this, it appears that norepinephrine facilitates GnRH release in the rabbit and ferret and the locus coereuleus which is the part of the brain involved in conveying genital-somatosensory information to the GnRH neurones. [6] Other substances that have similar effects include neuropeptide Y.

Species

Many species have been found to be induced ovulators and the reasons for this are not always clear. However, one possible reason is that induced ovulation could provide a better reproductive potential for those species that typically have shorter life spans and less encounters resulting in lower mating opportunities throughout their lifetime. [7]

Rodents such as mice and rats are known induced ovulators. In rats the East African mole rat and the Cape-Dune, Natal, Highvield and blind mole rats are known induced ovulators. These species require mating to stimulate the vagina and cervix, resulting in ovulation in the females. The East African mole rat has been found to have small spines on its penis which are also thought to contribute to this stimulation of induced ovulation. [7]

Mice are also thought to be induced ovulators. Studies have found that the lutenising hormone (LH) is crucial to bring about the induced ovulation. Disruption in LH surges in the mice and knockout of the progesterone receptor (progesterone is known to help maintain a pregnancy) results in lowered fertility of the mice. [8]

The koala species are a lesser-known induced ovulator. The koalas require mating in which the presence of ejaculated semen is needed to stimulate the female to produce a LH surge (which would cause ovulation of a follicle). Unlike many other animals, simply being in the presence of a male koala is not enough to induce ovulation itself, nor is vaginal stimulation on its own sufficient to cause induced ovulation to occur. [9]

The presence of koala semen in female koalas is known to be able to cause induced ovulation on its own, however, only in just under 50% of the subjects tested but statistical t tests confirmed this to be significant. [9]

Some genes putatively involved in the induction of ovulation in female koalas have been identified in male seminal plasma (NGF), and in coagulation of seminal fluid (ODC1, SAT1, SAT2, SMOX, SRM, SMS), which may function to prevent sperm leakage from the female reproductive tract in koalas. [10]

Cats are another widely-known induced ovulator. After mating, the LH levels in female cats surge, and the time to ovulation can be predicted to occur between 1–2 days later. [11]

Goats too have been found to be induced ovulators. A 1984 study saw LHRH injections were able to cause ovulation in goats that were of sexual maturity and already in oestrus. These injections had no influence on goats that were not in oestrus and could be because there is reduced sensitivity to LH and FSH receptors in the non-oestrus stages of the cycle so the LHRH may not have been able to induce a great enough response. [12]

Wolverines are other known induced ovulators which require physical mating to cause ovulation. [13]

Horses are induced ovulators and studies using combinations of PGF2alpa analogues, Lipsostiol, d-cloprostenol and hCG were able to artificially induce ovulation in this species though these neural pathways. [14]

Induced ovulation occurs in various carnivoran species, [15] including most felids [16] and several species of mustelids. [17] Many bear species are able to have induced ovulation including the grizzly bear, black bear and polar bear where both the presence of a male and mating itself are requirements for induced ovulation. However, there are some suggestions that mating is not as strict a requirement for ovulation in bears. [18]

Black bears are widely confirmed induced ovulators. It was observed that most females kept separate from males did not ovulate, where as females kept in areas with male bears did. Mating between the bears caused elevated progesterone levels, and this was seen by increased progesterone levels measured in the bears in the months that followed the mating seasons. [19] In black bears, the presence of a male was enough to cause a notable rise in progesterone levels even without mating. This could suggest that pheromonal/chemosensory factors could also contribute to induced ovulation in some species. [19]

Induced ovulation is able to occur in some fish species. In China freshwater fish including a variety of carp types, bream and loach are able to be induced to ovulate by using agonists of dopamine. This induction of ovulation from drugs is able to cause a predictable ovulation period and is very beneficial to farming of these species. [20]

In cattle

The natural cycle of spontaneous ovulation occurs in species such as cows. [21] There is a great demand for ovulation to be induced in cattle, as it allows farmers to synchronize their cattle to ovulate at the same time, helping improve the efficiency of dairy farming. [22] Induced ovulation can be utilized during the warmer seasons to increase plasma progesterone and improve the fertility of the cattle. [23] However, ovulation can only be induced in cows with mature follicles and merely initiates lutenization, it does not reduce the time for ovulation.

There are a number of methods that are used to induce ovulation in cattle such as: artificial insemination, introducing a number of hormones such as chorionic gonadotrophin, hCG and LH. As well as injecting progesterone by intravaginal devices called PRIDs (progesterone-releasing intravaginal devices) [24]

In cats

Domestic cats are often described as induced ovulators. During intromission, the penis probably causes distension of the posterior vagina and induces release of gonadotropin releasing hormone (GnRH) from the hypothalamus via neuroendocrine reflexes. A surge of luteinising hormone (LH) occurs within minutes of mating. With multiple matings, the LH surge is greater and lasts longer than when only one mating occurs. There are reports of ovulation without mating in cats. Spontaneous ovulation not only occurs in cats, but occurs with some frequency. It appears that non-copulatory ovulation may be possible in response to a variety of visual, auditory or olfactory cues. It is more appropriate to consider domestic cats to be both an induced and spontaneous ovulator. [25]

In rabbits

It has been known since 1905 [26] that domestic rabbits are physically induced ovulators, although they may also ovulate spontaneously. Early reports stated that simply having an oestrous doe in close proximity to a buck can induce ovulation, although there were no data presented in these early reports. [27]

In camelids

Dromedary camels (Camelus dromedarius), bactrian camels (Camelus bactrianus), llamas (Lama glama) and alpacas (Lama pacos) are all induced ovulators. [28] [29]

Bactrian camel

Bactrian camels ovulate after insemination into the vagina; it is the seminal plasma, but not the spermatozoa, which induces ovulation. Ovulation occurs in 87% of females after insemination: 66% ovulate within 36 hours and the rest by 48 hours (the same as natural mating). The least amount of semen required to elicit ovulation is about 1.0 ml. [28]

Alpaca

In alpaca, follicles ovulate approximately 26 hours after coital stimulation. Mounting accompanied by intromission is necessary to provide adequate stimulation for LH release and subsequent ovulation. [30] Deposition of semen, which contains ovulation-inducing factor (OIF), [31] has been shown to increase the chance of pregnancy. Prolonged copulation, causing abrasion and inflammation of the uterus, may enhance absorption of OIF.

Related Research Articles

Menstrual cycle A type of ovulation cycle where the endometrium is shed if pregnancy does not occur

The menstrual cycle is the regular natural change that occurs in the female reproductive system that makes pregnancy possible. The cycle is required for the production of oocytes, and for the preparation of the uterus for pregnancy. The menstrual cycle occurs due to the rise and fall of estrogen. This cycle results in the thickening of the lining of the uterus, and the growth of an egg,. The egg is released from an ovary around day fourteen in the cycle; the thickened lining of the uterus provides nutrients to an embryo after implantation. If pregnancy does not occur, the lining is released in what is known as menstruation or a "period".

Ovulation The release of a mature ovum/oocyte from an ovary.

Ovulation is the release of eggs from the ovaries. In women, this event occurs when the ovarian follicles rupture and release the secondary oocyte ovarian cells. After ovulation, during the luteal phase, the egg will be available to be fertilized by sperm. In addition, the uterine lining (endometrium) is thickened to be able to receive a fertilized egg. If no conception occurs, the uterine lining as well as blood will be shed during menstruation.

Luteinizing hormone is a hormone produced by gonadotropic cells in the anterior pituitary gland. In females, an acute rise of LH triggers ovulation and development of the corpus luteum. In males, where LH had also been called interstitial cell–stimulating hormone (ICSH), it stimulates Leydig cell production of testosterone. It acts synergistically with follicle-stimulating hormone (FSH).

Follicle-stimulating hormone gonadotropin that regulates the development of reproductive processes

Follicle-stimulating hormone (FSH) is a gonadotropin, a glycoprotein polypeptide hormone. FSH is synthesized and secreted by the gonadotropic cells of the anterior pituitary gland, and regulates the development, growth, pubertal maturation, and reproductive processes of the body. FSH and luteinizing hormone (LH) work together in the reproductive system.

Gonadotropin-releasing hormone mammalian protein found in Homo sapiens

Gonadotropin-releasing hormone (GnRH) is a releasing hormone responsible for the release of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) from the anterior pituitary. GnRH is a tropic peptide hormone synthesized and released from GnRH neurons within the hypothalamus. The peptide belongs to gonadotropin-releasing hormone family. It constitutes the initial step in the hypothalamic–pituitary–gonadal axis.

Kallmann syndrome (KS) is a genetic disorder that prevents a person from starting or fully completing puberty. Kallmann syndrome is a form of a group of conditions termed hypogonadotropic hypogonadism. To distinguish it from other forms of hypogonadotropic hypogonadism, Kallmann syndrome has the additional symptom of a total lack of sense of smell (anosmia) or a reduced sense of smell. If left untreated, people will have poorly defined secondary sexual characteristics, show signs of hypogonadism, almost invariably are infertile and are at increased risk of developing osteoporosis. A range of other physical symptoms affecting the face, hands and skeletal system can also occur.

In mammalian species, pseudopregnancy is a physical state whereby all the signs and symptoms of pregnancy are exhibited, with the exception of the presence of a foetus, creating a false pregnancy. The corpus luteum is responsible for the development of maternal behavior and lactation, which are mediated by the continued production of progesterone by the corpus luteum through some or all of pregnancy. In most species, the corpus luteum is degraded in the absence of a pregnancy. However, in some species, the corpus luteum may persist in the absence of pregnancy and cause "pseudopregnancy", in which the female will exhibit clinical signs of pregnancy.

The estrous cycle or oestrous cycle is the set of recurring physiological changes that are induced by reproductive hormones in most mammalian therian females. Estrous cycles start after sexual maturity in females and are interrupted by anestrous phases or by pregnancies. Typically, estrous cycles continue until death. Some animals may display bloody vaginal discharge, often mistaken for menstruation.

Folliculogenesis maturation of the ovarian follicle, a densely packed shell of somatic cells

In biology, folliculogenesis is the maturation of the ovarian follicle, a densely packed shell of somatic cells that contains an immature oocyte. Folliculogenesis describes the progression of a number of small primordial follicles into large preovulatory follicles that occurs in part during the menstrual cycle.

Hypothalamic–pituitary–gonadal axis

The hypothalamic–pituitary–gonadal axis refers to the hypothalamus, pituitary gland, and gonadal glands as if these individual endocrine glands were a single entity. Because these glands often act in concert, physiologists and endocrinologists find it convenient and descriptive to speak of them as a single system.

Follicular phase Phase of the estrous or menstrual cycle during which follicles in the ovary mature ending with ovulation

The follicular phase, also known as the preovulatory phase or proliferative phase, is the phase of the estrous cycle during which follicles in the ovary mature from primary follicle to a fully mature graafian follicle. It ends with ovulation. The main hormones controlling this stage are secretion of gonadotropin-releasing hormone which are follicle-stimulating hormone and luteinising hormone. They are released by pulsatile secretion.

Gonadotropin-releasing hormone agonist

A gonadotropin-releasing hormone agonist is a type of medication which affects gonadotropins and sex hormones. They are used for a variety of indications including in fertility medicine and to lower sex hormone levels in the treatment of hormone-sensitive cancers such as prostate cancer and breast cancer, certain gynecological disorders like heavy periods and endometriosis, high testosterone levels in women, early puberty in children, as a part of transgender hormone therapy, and to delay puberty in transgender youth among other uses. GnRH agonists are given by injections into fat, as implants placed into fat, and as nasal sprays.

Gonadotropin-releasing hormone antagonist

Gonadotropin-releasing hormone antagonists are a class of medications that antagonize the gonadotropin-releasing hormone receptor and thus the action of gonadotropin-releasing hormone (GnRH). They are used in the treatment of prostate cancer, endometriosis, uterine fibroids, female infertility in assisted reproduction, and for other indications.

Ovulation induction is the stimulation of ovulation by medication. It is usually used in the sense of stimulation of the development of ovarian follicles to reverse anovulation or oligoovulation.

Controlled ovarian hyperstimulation is a technique used in assisted reproduction involving the use of fertility medications to induce ovulation by multiple ovarian follicles. These multiple follicles can be taken out by oocyte retrieval for use in in vitro fertilisation (IVF), or be given time to ovulate, resulting in superovulation which is the ovulation of a larger-than-normal number of eggs, generally in the sense of at least two. When ovulated follicles are fertilised in vivo, whether by natural or artificial insemination, there is a very high risk of a multiple pregnancy.

Deslorelin chemical compound

Deslorelin, sold under the brand names Ovuplant, SucroMate, and Suprelorin among others, is an injectable gonadotropin releasing hormone superagonist which is used in veterinary medicine for various indications.

Seasonal breeders are animal species that successfully mate only during certain times of the year. These times of year allow for the optimization of survival of young due to factors such as ambient temperature, food and water availability, and changes in the predation behaviors of other species. Related sexual interest and behaviors are expressed and accepted only during this period. Female seasonal breeders will have one or more estrus cycles only when she is "in season" or fertile and receptive to mating. At other times of the year, they will be anestrus, or have a dearth of their sexual cycle. Unlike reproductive cyclicity, seasonality is described in both males and females. Male seasonal breeders may exhibit changes in testosterone levels, testes weight, and fertility depending on the time of year.

Infertility in polycystic ovary disease (PCOS) is a hormonal imbalance in women that is thought to be one of the leading causes of female infertility. Polycystic ovary syndrome causes more than 75% of cases of anovulatory infertility.

Induction of final maturation of oocytes is a procedure that is usually performed as part of controlled ovarian hyperstimulation to render the oocytes fully developed and thereby resulting in optimal pregnancy chances. It is basically a replacement for the luteinizing hormone (LH) surge whose effects include final maturation in natural menstrual cycles.

Gonadotropin surge-attenuating factor (GnSAF) is a nonsteroidal ovarian hormone produced by the granulosa cells of small antral ovarian follicles in females. GnSAF is involved in regulating the secretion of luteinizing hormone (LH) from the anterior pituitary and the ovarian cycle. During the early to mid-follicular phase of the ovarian cycle, GnSAF acts on the anterior pituitary to attenuate LH release, limiting the secretion of LH to only basal levels. At the transition between follicular and luteal phase, GnSAF bioactivity declines sufficiently to permit LH secretion above basal levels, resulting in the mid-cycle LH surge that initiates ovulation. In normally ovulating women, the LH surge only occurs when the oocyte is mature and ready for extrusion. GnSAF bioactivity is responsible for the synchronised, biphasic nature of LH secretion.

References

  1. Richards, J. S.; Hedin, L. (1988). "Molecular aspects of hormone action in ovarian follicular development, ovulation, and luteinization". Annual Review of Physiology. 50: 441–463. doi:10.1146/annurev.ph.50.030188.002301. ISSN   0066-4278. PMID   3288100.
  2. Strassmann, B. I. (June 1996). "The evolution of endometrial cycles and menstruation". The Quarterly Review of Biology. 71 (2): 181–220. doi:10.1086/419369. ISSN   0033-5770. PMID   8693059.
  3. 1 2 3 4 Bakker, J.; Baum, M. J. (July 2000). "Neuroendocrine regulation of GnRH release in induced ovulators". Frontiers in Neuroendocrinology. 21 (3): 220–262. doi:10.1006/frne.2000.0198. ISSN   0091-3022. PMID   10882541.
  4. Chen, B. X.; Yuen, Z. X.; Pan, G. W. (1985-07-01). "Semen-induced ovulation in the bactrian camel (Camelus bactrianus)". Journal of Reproduction and Fertility. 74 (2): 335–339. doi: 10.1530/jrf.0.0740335 . ISSN   1470-1626. PMID   3900379.
  5. Conaway, C. H. (June 1971). "Ecological adaptation and mammalian reproduction". Biology of Reproduction. 4 (3): 239–247. CiteSeerX   10.1.1.1014.8958 . doi:10.1093/biolreprod/4.3.239. ISSN   0006-3363. PMID   5000279.
  6. Spies, H. G.; Pau, K. Y.; Yang, S. P. (February 1997). "Coital and estrogen signals: a contrast in the preovulatory neuroendocrine networks of rabbits and rhesus monkeys". Biology of Reproduction. 56 (2): 310–319. doi: 10.1095/biolreprod56.2.310 . ISSN   0006-3363. PMID   9116126.
  7. 1 2 Katandukila, Jestina V.; Bennett, Nigel C. (May 2016). "Pattern of ovulation in the East African root rat (Tachyoryctes splendens) from Tanzania: induced or spontaneous ovulator?". Canadian Journal of Zoology. 94 (5): 345–351. doi:10.1139/cjz-2015-0217. hdl: 2263/59996 .
  8. Stephens, Shannon B. Z.; Tolson, Kristen P.; Rouse, Melvin L.; Poling, Matthew C.; Hashimoto-Partyka, Minako K.; Mellon, Pamela L.; Kauffman, Alexander S. (September 2015). "Absent Progesterone Signaling in Kisspeptin Neurons Disrupts the LH Surge and Impairs Fertility in Female Mice". Endocrinology. 156 (9): 3091–3097. doi:10.1210/en.2015-1300. ISSN   1945-7170. PMC   4541622 . PMID   26076042.
  9. 1 2 Johnston, S. D.; O'Callaghan, P.; Nilsson, K.; Tzipori, G.; Curlewis, J. D. (2004-11-01). "Semen-induced luteal phase and identification of a LH surge in the koala (Phascolarctos cinereus)". Reproduction. 128 (5): 629–634. doi: 10.1530/rep.1.00300 . ISSN   1470-1626. PMID   15509709.
  10. Johnson, R.N.; O´Meally, D.; Chen, Z.; Etherington, G.J.; Ho, S.Y.W.; Belov, K. (2018-08-01). "Adaptation and conservation insights from the koala genome". Nat. Genet. 50 (8): 1102–1111. doi:10.1038/s41588-018-0153-5. PMC   6197426 . PMID   29967444.
  11. Shille, V. M.; Munrot, Coralie; Farmer, Susan Walker; Papkoff, H.; Stabenfeld, G. H. (1983-09-01). "Ovarian and endocrine responses in the cat after coitus". Journal of Reproduction and Fertility. 69 (1): 29–39. doi: 10.1530/jrf.0.0690029 . ISSN   1470-1626. PMID   6684161.
  12. Mizinga, K. M.; Verma, O. P. (1984-03-01). "LHRH — Induced ovulation and fertility of anestrous goats". Theriogenology. 21 (3): 435–446. doi:10.1016/0093-691X(84)90405-9. PMID   16725893.
  13. Mead, Rodney A.; Bowles, Mark; Starypan, Greg; Jones, Mike (1993-01-01). "Evidence for pseudopregnancy and induced ovulation in captive wolverines (Gulo gulo)". Zoo Biology. 12 (4): 353–358. doi:10.1002/zoo.1430120405. ISSN   1098-2361.
  14. Kuhl, Juliane; Aurich, Jörg; Aurich, Christine (2017-10-01). "Effects of the Prostaglandin F2α Analogues Cloprostenol and Luprostiol in Combination With hCG on Synchronization of Estrus and Ovulation in Mares". Journal of Equine Veterinary Science. 57: 67–70. doi:10.1016/j.jevs.2017.07.004. ISSN   0737-0806.
  15. Larivière, Serge; Ferguson, Steven H. (2003). "Evolution of induced ovulation in North American carnivores". Journal of Mammalogy. 84 (3): 937–947. doi: 10.1644/bme-003 .
  16. de Morais, Rosana Nogueira. "Reproduction in small felid males." Biology, Medicine, and Surgery of South American Wild Animals (2008): 312.
  17. Mead, Rodney A., et al. "Evidence for pseudopregnancy and induced ovulation in captive wolverines (Gulo gulo)." Zoo Biology 12.4 (1993): 353-358.
  18. Chang, Geng-Ruei; Yang, Chieh-Chung; Hsu, Son-Haur; Lin, Chang; Chiu, Chun-Lung; Chan, Fang-Tse; Mao, Frank Chiahung (2011). "Fecal Reproductive Steroid Profiles for Monitoring Reproductive Patterns in Female Formosan Black Bears (Ursus thibetanus formosanus)". Annales Zoologici Fennici. 48 (5): 275–286. doi:10.5735/086.048.0502.
  19. 1 2 Okano, Tsukasa; Nakamura, Sachiko; Nakashita, Rumiko; Komatsu, Takeshi; Murase, Tetsuma; Asano, Makoto; Tsubota, Toshio (2006). "Incidence of Ovulation without Coital Stimuli in Captive Japanese Black Bears (Ursus thibetanus japonicus) based on Serum Progesterone Profiles". Journal of Veterinary Medical Science. 68 (10): 1133–1137. doi: 10.1292/jvms.68.1133 . PMID   17085899.
  20. Peter, Richard E.; Lin, Hao-Ren; Van Der Kraak, Glen (1988-11-01). "Induced ovulation and spawning of cultured freshwater fish in China: Advances in application of GnRH analogues and dopamine antagonists". Aquaculture. Induced Spawning of Asian Fishes. 74 (1): 1–10. doi:10.1016/0044-8486(88)90080-4.
  21. Bogle, O. A.; Ratto, M. H.; Adams, G. P. (2011-08-01). "Evidence for the conservation of biological activity of ovulation-inducing factor in seminal plasma". Reproduction. 142 (2): 277–283. doi: 10.1530/REP-11-0042 . ISSN   1470-1626. PMID   21652637.
  22. Wiltbank, Milo C.; Pursley, J. Richard (2014-01-01). "The cow as an induced ovulator: Timed AI after synchronization of ovulation". Theriogenology. 81 (1): 170–185. doi:10.1016/j.theriogenology.2013.09.017. PMID   24274420.
  23. De Rensis, F.; Valentini, R.; Gorrieri, F.; Bottarelli, E.; Lopez-Gatius, F. (2008-06-01). "Inducing ovulation with hCG improves the fertility of dairy cows during the warm season". Theriogenology. 69 (9): 1077–1082. doi:10.1016/j.theriogenology.2008.01.020. PMID   18374407.
  24. Yavas, Y.; Wallon, J.S. (2000-07-01). "Induction of ovulation in postpartum suckled beef cows: A review". Theriogenology. 54 (1): 1–23. doi:10.1016/S0093-691X(00)00322-8. ISSN   0093-691X. PMID   10990345.
  25. "Estrus". The University of Sydney. 2012. Retrieved September 12, 2014.
  26. Heape, W. (1905). "Ovulation and degeneration of ova in the rabbit". Proc. R. Soc. B. 76 (509): 260–268. doi: 10.1098/rspb.1905.0019 .
  27. Staples, R.E. (1967). "Behavioural induction of ovulation in the oestrous rabbit". J. Reprod. Fertil. 13 (3): 429–435. doi: 10.1530/jrf.0.0130429 . PMID   6067508.
  28. 1 2 Chen, B.X.; Yuen, Z.X.; Pan, G.W. (1985). "Semen-induced ovulation in the bactrian camel (Camelus bactrianus)". J. Reprod. Fertil. 74 (2): 335–339. doi: 10.1530/jrf.0.0740335 . PMID   3900379.
  29. Bravo, P. W.; Skidmore, J. A.; Zhao, X. X. (2000). "Reproductive aspects and storage of semen in Camelidae" (PDF). Animal Reproduction Science. 62 (1): 173–193. doi:10.1016/s0378-4320(00)00158-5. PMID   10924824.
  30. Fernandez-Baca, S.; Madden, D.H.L.; Novoa, C. (1970). "Effect of different mating stimuli on induction of ovulation in the alpaca". J. Reprod. Fertil. 22 (2): 261–267. doi: 10.1530/jrf.0.0220261 . PMID   5464117.
  31. Adams, G.P.; Ratto, M.H. (2012). "Ovulation-inducing factor in seminal plasma: A review". Animal Reproduction Science. 136 (3): 148–156. doi:10.1016/j.anireprosci.2012.10.004. PMID   23141951.