Pet Avian Medicine
Avian Reproductive Endocrinology
Michael B. Paster, DVM*
Much of the work on avian reproduction has been done on the chicken (Gallus domesticus), the turkey (Meleagris gallopavo), the domestic duck (Anas platyrhynchos domestica) and White-Crowned Sparrows (Zonotrichia leucophyrys gambelii). The anatomic and physiologic characteristics of these birds are similar to other members of the class Aves; however, great variation exists among species. HYPOTHALAMUS Hypothalamic-releasing factors regulate secretion of anterior pituitary hormones. The release of avian gonadotropins is regulated by one or more hypothalamic factors produced by neurosecretory neurons located mainly in the rostral hypothalamus. 43 Extracts of avian hypothalamus cause the release of luteinizing hormone (LH) and follicle-stimulating hormone (FSH). The hypothalamic substance that elicits this gonadotropin release is chemically and immunologically identical to the pure decapeptide that regulates secretion in mammals. 61 This synthesized material is biologically active in birds, causing LH release, ovulation, and gonadal growth. Luteinizing hormone releasing hormone (LH-RH) causes release of LH by the pituitary gland. 33 • 54 Blocks in reproduction can be associated with the failure of the hypothalamus to produce or release releasing hormones. 5 Thyroid-stimulating hormone (TSH) is regulated by hypothalamic secretion of thyrotropin releasing hormone (TRH). 63 TRH is capable of releasing at least two pituitary hormones, as in mammals. TRH causes gonadal growth in Coturnix quail, which indicates it also causes gonadotropin release. Administration ofTRH increases prolactin secretion in birds and mammals. Although the presence of a specific growth hormone releasing factor (GHRF) has not been established, TRH is a candidate for growth hormone releasing hormone (GH-RH). There is considerable evidence that avian somatostatin is growth hormone releasing inhibiting hormone (GHRIH). GHRIH may be involved in the control of GH secretion. GH secretion in domestic fowl and in birds in general appears to be under the hypothalamic control of GHRIH, GHRF, and TRH. 53 · 30 Adrenocorticotropic hormone (ACTH) is regulated by the hypothalmic release of corticotropin releasing factor (CRF). Hypofunction of the gonads, associated with removal of the vascular connections of the chicken anterior pituitary gland to the hypothalamus, caused little change in *Avalon Animal Hospital and Bird Clinic, Inc., Carson, California Veterinary Clinics of North America: Small Animal Practice-Val. 21, No. 6, November 1991
the activity of tht:; thyroid and adrenal glands. 63 The removal of the pituitary glands of several species from their hypothalamic connection has led to decreased prolactin secretion. 63 Prolactin is regulated by prolactin releasing factor (PRF) found in the hypothalmus53 rather than by prolactin inhibiting factor (PIF) as in mammals. Prolactin secretion may be the result of the balance of releasing hormones to inhibiting hormones. 30 ANTERIOR PITUITARY GLAND The anterior pituitary gland secretes the same six hormones as in mammals plus the melanotropic hormone. Individual hormones have been attributed to specific cell types, ~ven though it has not been proved conclusively that such relationship exists. 38 Follicle-Stimulating Hormone FSH is attributed to the beta cells. FSH stimulates the development of ovarian follicles and the secretion of estrogen by the ovaries. FSH stimulates tubular growth of the testes and spermatogenesis in males. Luteinizing Hormone LH is attributed to the gamma cells. LH causes ovulation in females and stimulation of the testes interstitial Leydig cells to produce androgens. Plasma levels of LH are in general higher in male than in female birds. 51 High levels of LH are found in egg-laying domestic ducks and wild Mallards, chickens, turkeys, Japanese Quail, Snow Geese, Herring Gulls, and White-Crowned Sparrows. 2· 5 · 25 Female wild and domestic Mallards, domestic hens, turkeys, Japanese Quail, Herring Gulls, Ring Doves, Bantam Hens, White-Crowned Sparrows, and Snow Geese show a decrease in LH (or estrogens 26) during incubation. 2 · 5 · 25 LH levels increase when a Mallard female looses a clutch.' Injections of LH stimulate the secretion of progesterone and testosterone in laying hens. 54 Studies 58 of plasma LH levels and the stimulation associated with breeding in male Ring Doves showed that LH levels are low in visually isolated males. Plasma LH peaked after pairing with a female and declined during incubation and brooding. Male cockatiels incubate eggs during the day while the females incubate at night. Parents often begin a second clutch within several days of fledging of the first clutch. When this occurs, the female will be laying and incubating while the male takes care of the first clutch fledglings. LH levels are elevated during the time of nest inspection in females and males. 45 • 56 LH levels peak during egg laying in females and decrease during this time in males. In both male and females, LH continues to decline during incubation and care of the young. LH increases if a second clutch is laid. 45 This pattern of increased LH secretion during nest-box presentation and egg laying followed by a decline during incubation is also seen in Zebra Finches, Pied Flycatchers, and Spotted Sandpipers. 45 Prolactin Prolactin is attributed to the beta cells. 38 Prolactin induces broodiness (nesting behavior, nest protection, incubation, cessation of egg laying, and caring for the young) and depresses the production of LH and FSH in both females and males. Circulating prolactin levels are slightly elevated during gonadal development and egg laying and are highest in incubating birds. Prolactin is usually highest in the parent providing the most care. Prolactin is intimately associated with incubation behavior in both altricial and precocial species. Altricial species are characterized by the young hatching naked
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and blind and exothermic with low metabolic rates as compared with the adults. Altricial species' metabolism and body heat production increase during development and usually exceed the capacity of their parents by fledging time. Precocial species' young hatch out covered with down, with eyes open and alert, and the ability to thermoregulate. This ability begins developing in the egg during incubation. Circulating levels of prolactin are highest during the brooding of young and migration. At these times a bird can be in danger of dehydration because of lack of access to free water. 21 Prolactin acts as an adaptive hormone by preventing dehydration through reduction of urine flow and increased food and water intake. 15 Prolactin levels in laying hens were twofold to fourfold higher in broody birds than in laying birds. Prolactin levels varied with light, darkness, or stage of ovulatory cycles. 2 Prolactin levels increase threefold in female Mallards during incubation. 2 In female domestic ducks, prolactin levels fall sharply around the time the eggs hatch. 29 Prolactin increases after the cessation of laying, and LH levels fall at the onset of broodiness in turkey hens. 7 High levels of plasma prolactin found in incubating turkey hens are not initiated nor maintained only by the stimulus of nesting. The cycling in prolactin seen at the end of incubation could be related to the pipping and hatching of eggs and a shift to maternal behavior. 62 The defeathering, vascularization, and epidermal hyperplasia of the brood patch is regulated by prolactin and estrogen and perhaps other steroids. Local anesthesia of the brood patch area for 9 hours caused a significant decrease in plasma prolactin in the female duck. This suggests that the tactile stimulation of the eggs may serve to stimulate the rise in prolactin during the egg-laying period and the maintenance of the secretion of this hormone during incubation. 29 Studies have shown that Mallard drakes, Barhead Geese, and Black Swans have higher prolactin levels at the end of the breeding cycle. 28 Mallard drakes do not participate in incubation and have fairly low prolactin levels compared with other male birds. 25 Prolactin may have a role in gonadal regression, since prolactin injections in sexually mature roosters and pigeons reduce testes weight, size of androgendependent secondary sex characteristics, and male behavior. 28 Prolactin may mediate gonadal regression through the interference of secretion of the gonadotropins. Prolactin secretion in the male starling is related to day lengths and is not a consequence of high gonadotropin or androgen secretion rates. Prolactin levels increase with increasing day length and is associated with photorefractoriness. 23 Prolactin secretion goes through a circadian rhythm that appears to parallel the ACTH cycle. 1 In ducks, levels rise during the night and peak immediately after the onset of light. In cockatiels, prolactin levels increase in both males and females during egg laying, peak during incubation, then decline during the nestling and fledging stages unless a second clutch is begun. 45 Elevated prolactin levels in second clutch male cockatiels indicate that prolactin has a parental function not exclusively related to incubation. 45 Prolactin stimulates development of the crop sac in some Columbiformes as well as the production of crop milk in pigeons and doves. Growth Hormone (Somatotropic Hormone) GH is attributed to the alpha cells. 38 GH levels are high in the early rapid phase of growth52 even though GH is not the only hormone that influences growth. 53 There is a close phase relationship among GH, T4 rhythms, and the stimulation of GH secretion by TRH in fowls and ducks. This may be related to the TRH-TSH cycle. 1 GH has been reported to peak during egg production in turkey hens. 1 Plasma GH levels were found to be significantly increased in brooding turkey hens but not
in hens incubating eggs. 62 An 11-fold 1-day increase in GH occurred immediately after turkey hens left the nest. 62 In male Peking ducks and teals, plasma GH rose during the breeding period and was found to correlate with the annual cycle in thyroxine secretion. No significant changes were observed in plasma thyroxine levels during laying, incubation, and brooding in the turkey hen. 62 GH has a lipolytic effect. The diurnal elevation of GH is associated with elevated plasma free fatty acids (FF A), a major source of energy, espe.cially for flight. 1 A study of domestic laying and broody hens showed no obvious relationship of plasma GH to lighting or the ovulatory cycle. 2 Adrenocorticotropic Hormone ACTH is attributed to the epsilon cells. 38 ACTH controls the production of adrenal corticosteroid~. ACTH mediates ovulation in the hen by its effect on corticosterone production by the adrenal gland. ACTH and corticosterone are responsible for inducing the initial rise in LH at the onset of darkness. Administration of either hormone triggers LH secretion and premature ovulation. 1· 2 A mature follicle capable of progesterone secretion must exist within the ovary before an injection of either ACTH or corticosterone can induce ovulation. 16 Dexamethasone, an inhibitor of ACTH secretion, blocks ovulation. This effect can be bypassed with the use of exogenous ACTH or progesterone. Metapyrone lowers the secretion of corticosterone in the hen and appears to desynchronize the laying pattern and preovulatory LH release. 14 Thyroid-Stimulating Hormone TSH, attributed to delta cells, 38 controls the function of the thyroid glands. Melanotropic Hormone, Intermedin, or Melanophore-Stimulating Hormone Melanotropic hormone, attributed to the kappa cells, 38 controls distribution of pigments.
POSTERIOR PITUITARY HORMONES Mesotocin Mesotocin, which is found in the avian posterior pituitary, has oxytocic activity. 19 It is the analog of mammalian oxytocin in birds. The physiologic role of oxytocin is unknown in birds, 38 and its presence in the avian posterior lobe is questionable. The administration of mesotocin causes a dose-related glomerular diuresis. 39 Levels of plasma mesotocin do not change during oviposition (expulsion of the egg from the oviduct) in hens. Oxytocin or any drug that can induce uterine contractility in the susceptible uterus can cause oviposition. The intravenous injection of posterior pituitary hormone stimulates a sensitized hen to lay an egg in 3 to 4 minutes. 61 Currently the role of mesotocin is unclear. 39 Arginine Vasotocin Arginine vasotocin (AVT) has a hyperglycemic and antidiuretic activity. AVT is the analog of the antidiuretic hormone (ADH) in birds. AVT has high oxytocic activity in the hen. AVT induces contraction of the oviduct and oviposition. Plasma levels of AVT rise with each oviposition and ovulation, even after the last egg of a sequence is laid. Ovarian follicular prostaglandins and an ovarian ovipositioninducing factor may promote an increase in uterine contractility by providing the signal that stimulates contraction of the uterus. 57 Prostaglandin, AVT, and uterine
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contractility are interrelated. AVT release in chickens appears to be stimulated by uterine contractility. 50 Intrauterine prostaglandin induces premature oviposition within 5 minut~s in hens that are due to lay in 3 hours. 50 Injection of AVT produces a rise in levels of blood metabolites, FF A, glucose, and GH. AVT increases male sexual behavior. 19 PINEAL GLAND The pineal gland, through the secretion of the hormone melatonin, modulates the periodic autonomic functions of the photoneuroendocrine system; the central nervous system with the thermoregulation system; and behavioral rhythms and species-specific circadian rhythmic organization in response to periodic changes in the internal and external environments, including responses to the 24-hour adaptation of the environpwnt to the rotation of the earth. 1· 4 · 32 Plasma melatonin was found to be elevated in the dark part of the light-dark cycle (LDC) of laying hens. Elevated plasma melatonin in laying hens is considered essential for regulating the timing of oviposition after the onset of darkness. Melatonin appears to be a primary coupler for other hormones to participate in the entrainment of oviposition to the LDC in the chicken. 41 GONADS The ovary produces estrogens, progestogens, and androgenic compounds. The testes produce testosterones and progesterone. Estrogens Estrogen may facilitate the response of the pituitary gland to LHRH in the domestic hen. 54 The final stages of ovarian follicular development with the fall in the concentration of LH is due to a decrease in the sensitivity of the pituitary gland to LHRH. This is probably caused by the negative feedback of ovarian steroids. In wild starlings, estradiol was highest in April, the period of courtship and greatest nest-building activity. Estradiol decreased during the later stages of the breeding cycle. u Similar observations were made in female American Kestrels 49 and female mallards. 5 Estrone and estradiol-17 beta are detected in high levels in females undergoing yolk deposition and egg laying. 11 · 68 These hormones are undetectable in the plasma of White-crowned Sparrow males. 68 Plasma levels of estrogen have been positively correlated with body weight in wild female birds, e. g., laying captive American Kestrels. 49 Progesterone Progesterone is responsible for the preovulatory LH surges 1 and induction of ovulation. The mechanism of this surge may be associated with a positive feedback interaction between progesterone and LH, rather than by the stimulatory effect of progesterone. 36 Progesterone injected into fowls 61 causes premature molting, stimulates an increase in LH secretion in laying domestic hens lasting several hours, 54 and causes a rapid decrease in blood levels of corticosterone. Progesterone at the level of the pituitary may stimulate the production of FSH 37 and suppress the pituitary-adrenal system, thus affecting the pattern of corticosterone secretion during the ovulatory cycle. 67 In the starling, progesterone was highest in laying birds, reaching a peak in May. Progesterone remained at a lower level during the remainder of the year. 11
Both young and old laying hens have a significantly higher plasma concentration of progesterone than non-laying hens. As the hen ages and egg laying ceases, the steroid-sensitive oviductal tissue undergoes a reduction in the level of magnal nuclear estrogen receptors and cytosol progesterone receptors. This theory explains why the oviduct of the aging hen is refractory to estrogen stimulation. 46 Testosterone The testes are responsible for production of the male gametes and the secretion of the steroid hormones that control development and functional activity of the accessory sexual organs and secondary sexual characteristics. Continuous administration of small amounts of testosterone, about 1 mg/day, suppressed spermatogenesis by inhibiting LH release in quail. However, the continuous administration of much larger amounts of testosterone, about 12 mg/day, did not prevent spermatogenesis even though LH secretion was suppressed. 12 Doses of androgen that suppress LH and FSH, presumably by negative feedback, cause testicular regression. 6 Maximal levels of testosterone and LH in males and females coincide with maximal gonadal weights, defense of territory, courtship, and nesting activity. 68 Androstenedione and dihydroepiandrosterone have been measured at higher levels than testosterone in male pigeons. 68 Androsterone, at non physiologic doses, was the most potent androgen in restoring courtship behavior in castrated pigeons. 68 Castration of photorefractory mallards causes a large rise in plasma LH levels, indicating that the testes are involved in the maintenance of the low LH concentrations of the refractory period. Photorefractoriness in mallards is apparently due to the negative feedback of testicular androgens to the hypothalamo-hypophyseal system. 28 In starlings, plasma testosterone and 5 alpha-dihydrotestosterone are high during April, highest in nest builders, and show a decrease during the later stages of the breeding cycle. 11 In the Japanese Common Pheasant, the circulating levels of testosterone correlate with the levels of FSH. 51 In male and female White-crowned Sparrows, 68 plasma LH and testosterone levels increase before and during migration, which suggests that testosterone may be involved in regulating vernal migration. Testosterone is a biologically active hormone in the laying hen. In fact, injections of testosterone cause an increase in progesterone 9 and can induce premature ovulation in the laying hen. Plasma concentrations of testosterone are maximal 2 to 8 hours before ovulation and always precede an increase in the concentration of LH. Testosterone may be the ovarian excitation hormone that initiates the release of LH from the pituitary,l 7 or it may react directly on the ovary to induce ovulation. 9 Female Zebra Finches have been induced to develop a male-like song system by being exposed to testosterone as nestlings. Testosterone increases the size of the brain nuclei associated with the song system. 48 THYROID GLANDS
The thyroid gland produces two hormones, thyroxine (T4 ) and triiodothyronine (To). The physiologic potency of the thyroid hormones appears to be very similar in most instances. Thyroid hormones stimulate the general metabolism, regulate the growth of the body and the reproductive organs, and regulate body heat in response to environmental temperature. A moderate increase in thyroid hormones accelerates growth and increases egg production. 38 T3 appears to be the main thyroid hormone affecting metabolic rate. 1· 27 T4 is concerned with feather growth. Thyroid hormone secretion displays a circadian rhythmicity-in immature
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chicks, iodine 131 uptake and plasma T4 increased during the dark periods and decreased during lighter periods. T 3 has the opposite cycle, since it rose during the day and fell at night. 1 Other species of birds have shown different results. In the Spotted Munia, a diurnal Indian passerine, both T4 and T3 peaked during the day.' An increase in thyroid hormone precipitates molting, possibly by the stimulation of growth of new feathers. T4 stimulates protein synthesis-feathers are essentially protein. T4 is more effective than an equal dose of T3 in stimulating the regrowth of plucked feathers. 27 The closer to the time of normal molt, the smaller the amount of thyroid hormone that is necessary to stimulate a feather papilla. 61 An intact thyroid gland is essential for the development and termination of photorefractoriness8 and for the release of prolactin that normally follows photostimulation in starlings. 24 The peaking of plasma thyroxine at the onset of photorefractoriness initiates molt in many species. Laying kestrels begin molting after levels of plasma estradiol-17 beta (a thyroxine inhibitor) decrease. The estradiol-17 beta/ thyroxine interaction may be a control mechanism for molt in many species. 49 The maintenance of juvenile refractoriness in the Red-legged Partridge and European Starling is dependent on the presence of thyroid hormones. 8
ADRENAL GLANDS Corticosterone Corticosterone is a hormone associated with metabolism and sodium and potassium secretion. Corticosterone is released during stress. Plasma levels are enhanced during the breeding season. This steroid is lipogenic, and maximal levels may be seen shortly before or during egg laying. 49 Corticosterone acts synergistically with prolactin to induce the elevated energy requirements and behavior associated with avian migration in several species. 49 An annual cycle in plasma corticosterone has been observed in chickens, ducks, quails, pigeons, sparrows, and certain migratory passerines. Plasma levels of corticosterone are elevated in August and September, when American Kestrels are preparing for migration. 49 This pattern is also seen in the White-crowned Sparrow. 68 Basal levels of corticosterone are seen during the prenuptial molt in the Whitecrowned Sparrow. 68 The highest daytime levels of corticosterone in the female Khaki Campbell Duck were associated with the maximal levels of progesterone. At night, the levels of LH paralleled the corticosterone levels. 65 Injections of dexamethasone, an ACTH blocking agent, may deprive a bird of endogenous progesterone. In the egg-laying hen, plasma corticosterone increases at the same time the deep body temperature increases during oviposition. Corticosterone also peaks during ovulation. These increases are probably governed by the hormonal control of oviposition. 3 · 34 Aldosterone Aldosterone is a mineralocorticoid, secreted by the adrenal cortex. It is concerned with the regulation of salt and water balance. Aldosterone plasma levels remain the same throughout the year. 1 11-Deoxycorticosterone, a mineralocorticoid, is also found in birds.
BURSA OF FABRICIUS The literature suggests a possible endocrine function for the bursa of Fabricius. 20 Both the bursa and the thymus are associated with the normal development of
immunity through the production of cellular units and humoral factors. They may be considered as lymphoid extensions of the endocrine system. The bursa grows very rapidly the first 3 to 4 weeks after hatching. Bursa regression occurs in poultry before 4 months of age. There is a definite relationship between the bursa and testes growth. Surgical removal of the testes leads to an increased bursa size, whereas injection of male hormone hastens bursa regression. Bursectomy does not influence the size of the testes. There is an inverse relationship between adrenal gland development and bursal size. The bursa regresses in the presence of adrenal extracts (cortisone and corticosterone) and ACTH. The adrenal is the primary endocrine influence on the bursa. Further evidence for a hormonal role for the bursa is suggest~d by the fact that bursectomy reduces the degree of hyperglycemia in the presence of ACTH. Antibody production has been restored with variable results in bursectomized birds using bursal extracts, bursal section implants, or soluble bursal factor.
MOLT AND REPRODUCTION In many avian species, molt and reproduction are separated in time by a control system. The androgens and estrogens of the reproductive cycle may delay or inhibit molt. The molting cycle is often associated with a marked increase in T, and T4 and basal levels of steroidogenic LH as well as testosterone and estrogen. This pattern has been observed in Peking Ducks, teals, Willow Ptarmigans, Whitecrowned Sparrows, blackbirds, Bar-Headed Geese, and Emperor and Adelie Penguins. Sex hormones have a protective effect on mature feathers as opposed to the thyroid hormones, which have a stimulating action on the early development of new feathers. 26
MALE REPRODUCTIVE SYSTEM Testes are at their maximum size during the breeding season-they may be 200 to 300 times larger than at other times of the year. 61 During the breeding season, the two testes of a duck may equal one-tenth of the body weight. The vas deferens increases in size and storage capacity, especially at its caudal end next to the cloaca. In the robin, Turdus migratorius, this seasonal increase in capacity of the vas deferens may be 120-fold. In some avian species, such as the breeding Zebra Finches, testes size does not change during or between reproductive cycles. 45 The interstitial glandular Leydig cells are considered the source of testosterone. The seasonal enlargement of the testes is associated with an increase in the activity and size of the interstitial cells and an increase in the secretion of androgens into the bloodstream. Increases in the concentration of male hormones in the body excite courtship, songs, and changes in coloration. Maximum plasma LH and gonadal steroids coincide with maximal testes weight and copulation in the Whitecrowned Sparrow and the Emperor Penguin as well as other birds?" The Sertoli cells seasonally acquire the characteristics of steroidogenic cells. 43 These cells may be the locus of intratubular production of androgens that influence the adjacent germinal cells. Injection of mammalian FSH stimulates spermatogenesis and depletion of the cholesterol-rich lipoidal material of the Sertoli cells. FSH might, therefore, stimulate spermatogenesis by stimulating the secretory activity of the Sertoli cells in a way similar to the action of LH on the steroidogenic interstitial Leydig cells. Spermatogenesis can be stimulated 43 by exogenous androgen injections. Fur-
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thermore, injections of testosterone proprionate prevent testicular regression during the postnuptial refractory period and maintain the testes in a sexually active state. Immature hypophysectomized quail treated with testosterone and FSH underwent testicular growth. Pigeons that were hypophysectomized at maturity underwent no testicular regression when supported with exogenous androgens. 6 Castration 43 results in a raised level of LH and FSH due to the absence of an endogenous feedback. Implants of testosterone in the adenohypophysis or hypothalamus of quails result in testicular regression and cause a depression of the high levels of LH in castrated males. In the American Tree Sparrow, hemicastration does not change the photoperiodic response of LH secretion but increases the FSH secretion, apparently by decreasing the intensity of the inhibitory feedback signal for FSH but not LH. Puberty and the Breeding Season The sequence of endocrine events associated with puberty in the cockerel55 has been described as follows. (1) The amount of androstenedione decreases in the testes before evidence of testicular growth; (2) then the testes start to enlarge and there is an increase in the total amount of LH found in the pituitary; (3) after this, there is an increase in the total amount of testosterone in the testes and an increase in the concentration of LH in the plasma; (4) this is followed by an increase in the concentration of testosterone in the plasma; (5) then there is an increase in the rate of growth of the comb and testes; (6) this is followed by an increase in the levels of LH, testosterone, 55 and androstenedione, 10 after which spermatogenesis begins. The concentration of plasma androstenedione exceeds that of testosterone in the juvenile cockerel, whereas in the adult it is about half that of testosterone. 10 Light influences avian gametogenesis, and seasonal fluctuations of the daily photoperiod influence the annual reproductive cycles. 42 Data from the in vitro production of testosterone from House Sparrows and Green-Winged Teals show that a well-defined seasonal cycle closely parallels the spermatogenetic pattern. Furthermore, artificial manipulation of the daily photoperiod influences testosterone synthesis and sperm production. Plasma testosterone levels correlate with testicular weight. Only when light is experienced during an endogenous circadian rhythm of light-sensitive periods is spermatogenetic activity stimulated and plasma testosterone levels increased. Light experienced outside of these times has little or no effect. The temporal position of the photoinducible phase is species specific and has an important influence on the pattern of annual reproductive cycles and the synchronizing effects of the environment. Experiments involving exogenous hormone therapy must be interpreted with caution and cognizance taken of the temporal relationship between administration and the phase relationship of the endogenous hormone. In studies of male birds belonging to the spring breeders of the temperate zones, 1 the most common hormone pattern is that plasma LH and testosterone levels increase as the day length increases, peaking during the breeding season around April to May. Both hormone levels decline rapidly between June and August, depending on the species, and are preceded by a massive postnuptial molt. By August to September, LH and testosterone secretions show a transient rise and are accompanied by a partial recovery of sexual behavior. Plasma androgen levels rise within 4 hours of pairing with a female and remain elevated during courtship. 58 Plasma FSH level follows an annual cycle, with an increase in winter to spring and a decrease in the fall. This annual cycle is less closely related to sex steroid secretion than the LH cycle. 42 The Emperor Penguin, a polar seabird, breeds during the Antarctic winter and is one of the few birds studied in which gonadal growth is coincident with short
days. 26 Adelie Penguins are more like birds from the temperate zones in that they breed as the day lengths increase. The initial phase of gonadal development begins when the birds are still at sea. By the time the males reach the breeding grounds there is an increase in plasma levels of LH, gonadal steroids, and testicular size. Seasonal Reconstruction of the Testis and Epididymis There are three well-defined phases38 seen in the testis and epididymis in bird species that have definite breeding seasons: (1) regeneration phase-the seminiferous tubules, interstitial cells, tunica albuginea, and efferent and connecting ductules epididymis disintegrate to a certain extent and are then reconstructed. The reproductive and endocrine function are restored. (2) Acceleration phase-the gonadotropins induce a renewal and enlargement of the interstitial cells and an great increase in their lipid content. This phase occurs in the autumn or spring. The epithelial cells that line the epididymal ductules begin merocrine secretion. (3) Culmination phase-'-gametogenesis reaches its peak and mating occurs. The lipids of the interstitial cells become depleted and the epididymal ductule epithelial cells undergo intermittent apocrine secretion. These three distinct phases are not seen in the domestic fowl. FEMALE REPRODUCTIVE SYSTEM Only the left ovary develops in most birds. In some birds of prey, e.g., from the genera Accipiter, Cirus, and Falco, both left and right ovaries may be present and functional. 61 If the functional left ovary of a bird is experimentally removed, the vestige of the right ovary develops into a testis-like organ. 61 The ovary and oviduct enlarge greatly during the breeding season and then shrink to very small sizes during the remainder of the year. Feral parakeet populations have definite gonadal cycles. The average diameter of ovarian follicles of non breeding females is 0. 8 mm, whereas the largest follicle of breeding females is 9 mm. 60 During the breeding season, the oviduct weighs from 10 to 50 times as much as during periods of sexual inactivity. The size of the oviduct is under the influence of the ovarian hormones. The ovary grows in two phases. 54 The first phase consists of enlargement of the stroma and the follicles with little deposition of yolk. The second phase of development occurs very rapidly, over a period of 4 to 11 days, depending on the species, when yolk is deposited in a relatively small number of follicles to form a follicular hierarchy. This rapid deposition of yolk can result in a 100-fold increase in ovarian weight. FSH regulates the pattern of growth and maturation of the ovarian follicles. LH stimulates the growth and maturity of the interstitial cells and controls the discharge of the ovum from its follicle. Later in the reproductive cycle, prolactin depresses the production of both the FSH and the LH and initiates broodiness. The interstitial cells and the follicles themselves produce the ovarian hormones: estrogens, androgens, and progesterone. 61 In the female White-crowned Sparrow and Emperor Penguin, plasma concentrations of LH and estrone and the size of ovarian follicles are at their maximum at the time of copulation and ovulation. 26 Albumin (egg white) is synthesized by the albumin-secreting glands of the magnum of the oviduct after activation by ovarian hormones. Lipids of the yolk are synthesized in the liver under the stimulation of estrogens and then transported in the bloodstream to the enlarging oocyte. 26 Estrogens also cause increased levels of plasma calcium and have been reported to increase during vitellogenesis in several avian species. Different species of birds lay their eggs at different times of day. There are
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two categories of layers: determinate layers lay a certain number of eggs and then stop, and .indeterminate layers continue to lay eggs until a definite number have accumulated in the nest. Indeterminate layers replace any eggs that have been removed. In some way, the clutch of eggs then stimulates the secretion of a prolactin-type hormone that induces regression of the ovary and initiates incubation behavior. Fertile Period Prolonged storage of viable spermatozoa in the oviduct occurs in some species ofbirds. 18 In female birds of this type, spermatozoa are received under circumstances in which mating may take place several weeks or months before ovulations occur. The males may not be in the vicinity of the female when ovulation takes place. Specialized simple tubular epithelial sperm-host glands are found on the vaginal side of the shell gland-uterus junction. Prolonged survival of spermatozoa in the oviduct after artificial insemination or mating may lead to fertilization of a number of eggs, owing to sequential ovulation, over a specified period lasting 2 to 3 weeks. 40 This fertile period is well known in domesticated species of birds such as the chicken, turkey, duck, goose, and guinea fowl. This period has been described in wild species of birds, e.g., the Mallard Duck, pheasant, quail, and dove. Blood Chemistry of Laying Birds Phospholipids, fatty acids, and neutral fats increase by a threefold to 18-fold factor. This increase is stimulated by ovarian hormones. There is no increase in plasma cholesterol. Estrogen injected into immature hens and roosters for 10 days increases the concentration of lipids in the blood by seven times and causes deposition offat in the body tissue of both sexes. 61 Blood glucose level in a layer is double that of a nonlayer or a male. 61 However, blood glucose has been found to be significantly depressed in turkey hens during incubation. 62 Blood calcium is doubled in laying birds. As the ovarian follicles grow, they secrete hormones that stimulate an increase in absorption of calcium by the intestines and a rapid storage of calcium by the hollow bones of the body. Estrogen injections in various species have caused increased bone-calcium deposition. 61 Ovulatory Cycle
Ovarian Follicular Hormones. The production of ovarian hormones by the follicles has been studied in detail in the domestic hen. 54 The thecal cells 26 of the enlarging follicle produce increasing quantities of estrogen, which primes the preovulatory release of LH. When the enlarging follicle becomes the second largest follicle in the hierarchy, aromatase activity declines, and progesterone and testosterone synthesis increases. The main hormone produced in the mature preovulatory follicle is progesterone. The follicle's sensitivity to LH increases with increasing levels of adenylate cyclase at the time of the preovulatory LH surge. The steroidogenesis in the developing follicle is regulated by changes in the levels of plasma hormones. 54 • 64 Plasma Hormones. A study of the plasma hormones of the ovulatory cycle of the domestic hen 35 demonstrated the following: Plasma hormones, LH, progesterone, estrone, estradiol-17 beta, and 5-alpha-dihydrotestosterone, were highest 6 hours before ovulation, whereas a peak of testosterone preceded ovulation by 8 hours. Estradiol-17 beta produced by enlarging ovarian follicles facilitates courtship vocalization and posture, primes the brain for induction of ovulation, and induces physiologic changes associated with egg laying. 49 A surge of corticosterone preceded ovulation by 2 hours; this was attributed to oviposition and not to ovulation. A small daily surge of LH occurred at the onset of darkness. 66 In ducks, LH and progesterone
increase with darkness, and nightfall may be the signal for the induction of ovulation. 59 Similar studies have been done in the quail. 47 Prostaglandins E and F increase in both the preovulatory follicle and the plasma before oviposition-ovulation in hens. This may be related to the preovulatory surge of LH, and prostaglandins may play a role in establishment of the follicular hierarchy. 31 Estrogen never stimulates LH release, whereas progesterone stimulates LH secretion when given at any stage of the ovulatory cycle except the stage at which preovulatory LH levels are falling. 54 The lack of response is associated with a loss of responsiveness of the pituitary gland to LHRH. Testosterone and corticosteroids stimulate LH release, but only in nonphysiologic doses. Progesterone is the principal hormone exerting a positive feedback effect on LH release in the hen. This is supported by the fact that ovulation in the hen is blocked by injections of antiprogesterone but not by antiestradiol serum.
EFFECT OF'DOMESTICATION ON AVIAN REPRODUCTION Studies performed on duck reproduction show that domestication results in an increased reproductive potential through earlier nesting and a delay in the termination of reproduction until later in the summer. There is a decrease in the synchronization of male and female hormonal events. In wild migratory populations, there apparently is an interdependence of hormonal events between males and females that are pair bonded. Testicular weights and levels of testosterone found in the plasma are higher in game farm and domestic males than in wild stock; however, the levels of LH are similar. 13 Reproductive Problems It 'has been difficult to breed a number of avian species in captivity, even though the reproduction patterns of feral populations has been studied extensively. 60 Reproductive problems of captive birds are usually associated with the ovaries' failure to develop ovulable follicles. The ovaries grow, but the deposition of sufficient yolk to reach ovulable size fails to occur. Some species respond to the stimulation of injections of gonadotropic hormones and develop functioning ovaries. Injections of pregnant mare's serum gonadotropin (PMSG) in English Sparrows and canaries can induce the formation of an almost normal hierarchy of follicles, which are more numerous and are approximately half the size of normal ovulable follicles. Egg laying can be induced in canaries. However, abnormalities can occur as a result of PMSG treatment. There is a high incidence of soft-shelled eggs, egg binding, eggs laid outside the nest, and a high mortality rate. PMSG did not stimulate the ovaries of feral Mallard Ducks. Administration of PMSG to ovulating domestic hens results in the stimulation of a large number of follicles of similar ovulable size, destroying the hierarchy of follicles, resulting in the interruption of ovulations. 60 Although it has been difficult to breed captive feral females in breeding condition of several species, e.g., the \Vhite-crowned Sparrow, it has not been difficult in these same species to stimulate testosterone secretion, testicular development, and spermatogenesis in the males. 60 Adequate food and water and exposure to sufficiently long photoperiods bring about testicular development in the starling, White-crowned Sparrow, wild Mallards, and many other species. The presence of a male enhances the stimulatory effect of long days on ovarian follicles and stimulates nest-building activity, which can result in successful egg laying. Testicular development was greater when male starlings were housed with females than if housed alone, in spite of the fact that the ovaries of the female showed little follicular development but appeared to secrete testosterone (as is normal for female starlings), as shown by the change in beak color from black to yellow. 60 The testicular
AVIAN REPRODUCTIVE ENDOCRINOLOGY
development of captive photostimulated White-crowned Sparrows is 10% to 20% less, and regression occurs 10 to 40 days sooner than in feral White-Crowned Sparrows: 68 The female of this species controls the onset of breeding, and captive females would be affected more by captivity than males. A study done with stressed Mallard hens suggested that the block in reproduction is a failure of the hypothalamus to produce or release releasing hormones. 5 Other hormonal factors that can lead to infertility are failure of the pituitary to respond to hypothalamic stimulation, failure of the ovary to respond to gonadotropin stimulation, and the release of prolactin or ACTH with stress. In a study done on captive Japanese Quail in small cages undergoing sustaiped egg laying, it was postulated that elevated prolactin levels resulted in the suppression of incubation behavior. 22 Photoperiodism
Reproduction in many avian species from temperate zones is photostimulated by increasing day lengths in the spring and early summer. This time of year is optimum for breeding and survival of offspring. Sexual activity increases with longer day lengths and decreases with shorter day lengths. Gonadotropin production by the pituitary is limited by light restriction, whereas long photoperiods (more than 12 hours) stimulate hormone release. 18 Cockatiels are very susceptible to photostimulation.45 Long days as well as artificial photostimulation induce a rapid increase in the concentration of plasma LH in photosensitive birds, such as the Whitecrowned Sparrows and Japanese Quail. 33 Artificial light regulation is used in commercial chicken and turkey breeding operations to both retard and initiate gonadal activity. Light photostimulation is required to produce eggs at maximum rate. However, chickens lay in continuous darkness and some turkeys lay eggs when exposed to light for as little as 6 hours per day. 18 The breeding season is oflimited duration and the gonads regress spontaneously and become photorefractory while day lengths are still long. Birds do not become photosensitive again until exposed to a period of short day lengths. Prepubertal exposure to a nongonad-stimulating light of short day lengths is required by many avian species before they are able to respond to stimulatory photoperiods. Refractoriness of the hypothalamic-gonadal axis develops when the rhythms of LH and FSH secretion are out of phase. 44 Photorefractoriness prevents breeding and egg laying when day lengths are long and stimulatory, as in the late summer, and ecologic conditions are unfavorable for survival of offspring (e.g., when offspring hatched would have little chance of maturing sufficiently before migration). Light acts on the bird to regulate secretion of hypothalamic-releasing hormones, which act on the pituitary to stimulate release of gonadotropins. Light-stimulated blinded birds are fully able to develop sexually as shown by the photosexual response of blinded house sparrows. 63 Gonadal activity continues in pinealectomized blinded chickens, demonstrating that the pineal gland of birds is not the photoreceptive organ involved in the photosexual response. 4 Light directed onto the hypothalamus of the duck elicits testicular growth. Direct illumination of the medial basal hypothalamus induced testicular growth in White-crowned Sparrows and LH secretion and testicular growth in Japanese Quail. 33 The mechanism of this response to light is as yet unknown, although recent studies have shown that the basal hypothalamus has the capacity to perceive photic information and a rhodopsin-like pigment was found in the hypothalamus. 33 This is evidence of extraretinal light receptors. SUMMARY
Hypothalamic-releasing factors regulate the secretion of anterior pituitary hormones. The anterior pituitary gland secretes the same six hormones as found in
mammals: FSH, LH, prolactin, GH (somatotropic hormone), ACTH, and TSH, plus the melanotropic hormone. The endocrine hormones of the avian posterior pituitary gland concerned with reproduction are mesotocin and AVT. The pineal gland, through the secretion of the hormone melatonin, modulates the periodic autonomic functions of the central nervous system. The ovary produces estrogens, progestogens, and androgenic compounds. The testes produce testosterones and progesterone. The thyroid glands produce two hormones, T4 and T3 • The avian adrenal glands produce corticosterone and aldosterone. The bursa of Fabricius is considered an endocrine organ since it is involved in the production of humoral factors. · The male reproductive system undergoes hormonal changes associated with puberty, the breeding season, and molt. Some avian species undergo a type of disintegration and seasonal reconstruction of the testis and epididymis. The relationship of the ovarian follicular hormones and the plasma hormones varies depending on the stage of the reproductive cycle and the seasonal photostimulation. Female birds may conceive in the absence of a mate as a result of the fertile period phenomena. The blood chemistry of laying birds is different from that seen in nonlaying hens. Domestication has had a definite influence on the hormone cycles of some avian species. This may lead to certain reproductive problems.
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15. Ensor DM: Prolactin and adaptation. In Peaker M (ed): Avian Physiology. London, The Zoological Society of London, Academic Press, 1975, pp 129-146 16. Etches RJ, Craze F: Plasma concentration ofLH, progesterone, and corticosterone during ACT.H and corticosterone induced ovulation in the hen (Gallus domesticus). Gen Comp Endocrinol 50:359-365, 1983 17. Etches RJ, Cunningham FJ: The plasma concentrations of testosterone and LH during the ovulation cycle of the hen (Gallus domesticus). Acta Endocrinol 84:357-366, 1984 18. Follett BK, Davies DT: Photoperiodicity and the neuroendocrine control of reproduction in birds. In Peaker M (ed): Avian Physiology. London, The Zoological Society of London, Academic Press, 1975, pp 199-211 19. George JC: Structure and physiology of posterior lobe hormones. In Epple A, Stetson MH (eds): Avian Endocrinology. New York, Academic Press, 1980, pp 85-115 20. Glick B: The thymus and bursa of Fabricius: Endocrine Organs? In Epple A, Stetson MH (eds): Avian Endocrinology. New York, Academic Press, 1980, pp 209-229 21. Goldsmith AR, Follett BK: Anterior pituitary hormones. In Epple A, Stetson MH (eds): Avian Endocrinology. New York, Academic Press, 1980, pp 147-165 22. Goldsmith AR, Hall M: Prolactin concentrations in the pituitary gland and plasma of Japanese quail in relation to photoperiodically induced sexual maturation and egg laying. Gen Camp Endocrinol 42:449-454, 1980 23. Goldsmith AR, Nicholls TJ: Prolactin is associated with the development of photorefractoriness in intact, castrated, and testosterone-implanted starlings. Gen Comp Endocrinol 54:247-255, 1984 24. Goldsmith AR, Nicholls TJ: Thyroidectomy prevents the development of photorefractoriness and the associated rise in plasma prolactin in starlings. Gen Comp Endocrinol 54:256--263, 1984 25. Goldsmith AR, Williams DM: Incubation in mallards (Anas Platyrhynchos): Changes in plasma levels of prolactin and luteinizing hormone. J Endocrinol 86:371-379, 1980 26. Groscolas R, Jallegeas M, Goldsmith AR, et a!: The endocrine control of reproduction and molt in male and female emperor (Aptenodytes forsteri) and Adelie (Pygoscelis adeliae) penguins. I. Annual changes in plasma levels of gonadal steroids and LH. Gen Camp Endocrinol 62:43-53, 1986 27. Groscolas R, Leloup J: The endocrine control of reproduction and molt in male and female emperor (Aptenodytes forsteri) and Adelie (Pygoscelis adeliae) penguins. II. Annual changes in the plasma levels of thyroxine and triidothyronine. Gen Camp Endocrinol 63:264-274, 1986 28. Haase E: The annual reproductive cycle in mallards. J Steroid Biochem 19:731-737, 1983 29. Hall MR, Goldsmith AR: Factors affecting prolactin secretion during breeding and incubation in the domestic duck (Anas platyrhynchos). Gen Comp Endocrinol 49:270276, 1983 30. Hall TR, Chadwick A: Hypothalamic control of prolactin and growth hormone secretion in the pituitary gland of the pigeon and the chicken: In vitro studies. Gen Camp Endocrinol 49:135-143, 1983 31. Hammond A, Olson DM, Frenkel RB, et al: Prostaglandins and steroid hormones in plasma and ovarian follicles during the ovulation cycle of the domestic hen (Gallus domesticus). Gen Camp Endocrinol 42:195--202, 1980 32. Hartwig H-G: The structure of the pineal gland. In Epple A, Stetson MH (eds): Avian Endocrinology. New York, Academic Press, 1980, pp 33-51 33. Hatanaka F, Wada M: Mechanism controlling photostimulated luteinizing hormone secretion is different from preovulatory luteinizing hormone surge in Japanese quail (Coturnix coturnix japonica). Gen Camp Endocrinol 70:101-108, 1988 34. Johnson AL, van Tienhoven A: Plasma concentration of corticosterone relative to photoperiod, oviposition, and ovulation in the domestic hen. Gen Camp Endocrinol 43:1016, 1981 35. Johnson AL, van Tienhoven A: Plasma concentrations of six steroids and LH during the ovulatory cycle of the hen, Gallus domesticus. Bioi Reprod 23:386-393, 1980 36. Johnson PA, Johnson AL, van Tienhoven T: Evidence for a positive feedback interaction between progesterone and luteinizing hormone in the induction of ovulation in the hen (Gallus domesticus). Gen Camp Endocrinol 58:478-485, 1985 37. Kawashima M, Kamiyoshi M, Tanaka K, et a!: Effects of progesterone on pituitary cells
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60. van Tienhoven A: Environment and reproduction in pet birds. In Proceedings of 1983 Annual Meeting of the Association of Avian Veterinarians, San Diego, CA, 1983, pp 110-161 61. Welty JC, Baptista L: Excretion, Reproduction, and Photoperiodism: The Life of Birds, ed 4. Philadelphia, Saunders College Publishing, 1988, pp 144-170 62. Wentworth BC, Proudman JA, Opel H, et a!: Endocrine changes in the incubating and brooding turkey hen. Bioi Reprod 29:87-92, 1983 63. William HB: Avian reproduction. In Swensen MJ (ed): Dukes' Physiology of Domestic Animals, ed 9. Comstock Publishing Assn., Cornell University Press, 1977, pp 825841 64. Williams JB, Sharp PJ: Control of the preovulatory surge of luteinizing hormone in the hen (Gallus domesticus): The role of progesterone and androgens. J Endocrinol 77:5765, 1978 65. Wilson SC, Cunningham FJ, Morris TJ: Diurnal changes in the plasma concentrations of corticosterone, luteinizing hormone and progesterone during sexual development and the ovulatory cycle of Khaki Campbell Ducks. J Endocrinol 93:267-277, 1982 66. Wilson SC, Jennings RC, Cunningham FJ: An investigation of diurnal and cyclic changes in the secretion of luteinizing hormone in the domestic hen. J Endocrinol 98:137-145, 1983 67. Wilson S, Cunningham FJ: Concentrations of corticosterone and luteinizing hormone in plasma during the ovulatory cycle of the domestic hen and after the administration of gonadal steroids. J Endocrinol 85:209-218, 1985 68. Wingfield JC, Farner DS: The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Bioi Reprod 19:1046-1056, 1978 Address reprint requests to Michael B. Paster, DVM Avalon Animal Clinic and Bird Hospital, Inc. 22404 South Avalon Boulevard Carson, CA 90745