Summary
The ovaries of free-living and captive White-crowned Sparrows, Zonotrichia leucophrys gambelii, were examined for seasonal changes. The ovary develops each year between March and June. It contains small primary oocytes; developing, preovulatory (yolky), and postovulatory follicles; scars; gland cells; and atresias. Most of its eggs are oocytes. Less than 30% are developing follicles. There is a hierarchy of sizes only in laying sparrows. Follicles apparently begin to secrete estrogen when they are 1 mm in diameter. The depletion of cholesterol from the ovary suggests that synthesis of estrogen begins about 1 month before the oviduct matures. There are five kinds of atresia. Most do not rupture. The ovaries of captive sparrows differ in the following ways from those of free-living birds: (a) they lack pre- and postovulatory follicles; (b) they contain more atresias; (c) the stroma is dense and poorly vascularized year-round; (d) the membrana granulosa of developing follicles becomes proliferative earlier in the spring and is always less active mitotically; (e) thecae do not develop beyond formative stages; (f) thecal gland cells become abundant earlier in spring; and (g) stromal gland cells are less numerous. Many of these differences (a, b, d, f, g) suggest that White-crowned Sparrows do not breed in captivity because of an abnormal synthesis and/or secretion of hypophysial gonadotropin.
Similar content being viewed by others
References
Bailey, R. E.: Inhibition with prolactin of light-induced gonad increase in White-crowned Sparrows. Condor 52, 247–251 (1950).
Baillie, A. H., Ferguson, M. M., Hart, D. M.: Developments in steroid histochemistry. New York: Academic Press, Inc. 1966.
Bent, A. C. (ed.): Life histories of North American cardinals, grosbeaks, buntings, towhees, finches, sparrows, and allies. Order Passeriformes: Family Fringillidae. Part III. Genera Zonotrichia through Emberiza. New York: Dover Pub., Inc. 1968.
Berthold, P.: Über die Gonadenentwicklung des Stars (Sturnus vulgaris) in Abhängigkeit von seinem Zugverhalten. Experientia (Basel) 23, 963–968 (1967).
Brambell, F. W. R.: Ovarian changes. In: Marshall's physiology of reproduction (A. S. Parkes ed.), p. 397–542. Boston: Little, Brown, & Co. 1956.
Brant, J. W. A., Nalbandov, A. V.: Role of sex hormones in albumen secretion by the oviduct of chickens. Poultry Sci. 35, 692–700 (1956).
Breneman, W. R.: Steroid hormones and the development of the reproductive system in the pullet. Endocrinology 58, 262–271 (1956).
Chieffi, G., Botte, V.: The distribution of some enzymes involved in the steroidogenesis of hen's ovary. Experientia (Basel) 21, 16–17 (1965).
Dahl, E.: Studies of the fine structure of ovarian interstitial tissue. 3. The innervation of the thecal gland of the domestic fowl. Z. Zellforsch. 109, 212–226 (1970).
— Studies of the fine structure of ovarian interstitial tissue. 4. Effects of steroids on the thecal gland of the domestic fowl. Z. Zellforsch. 113, 111–132 (1971a).
— Studies of the fine structure of ovarian interstitial tissue. 5. Effect of gonadotropins on the thecal gland of the domestic fowl. Z. Zellforsch. 113, 133–156 (1971b).
Davis, D. E.: The bursting of avian follicles at the beginning of atresia. Anat. Rec. 82, 153–165 (1942a).
— The regression of the avian, post-ovulatory follicle. Anat. Rec. 82, 297–307 (1942b).
— The occurrence of burst atretic follicles in birds. Anat. Rec. 90, 307–309 (1944).
DeWolfe, B. B.: Biology of white-crowned sparrows in late summer at College, Alaska. Condor 69, 110–132 (1967).
— Zonotrichia leucophrys gambelii (Nutall). Gambel's white-crowned sparrow. In: Life histories of North American cardinals, grosbeaks, buntings, towhees, finches, sparrows, and allies (A. C. Bent, ed.), p. 1324–1338. New York: Dover Pub., Inc. 1968.
Dubuisson, M.: Dégénérescence des ovules chez le Moineau, la Poule et le Pigeon. C. R. Soc. Biol. (Paris) 59, 472–473 (1905).
Erpino, M. J.: Seasonal cycle of reproductive physiology in the Black-billed Magpie. Condor 71, 267–279 (1969).
Farner, D. S.: Photoperiodic control of annual gonadal cycles in birds. In: Photoperiodism and related phenomena in plants and animals (R. B. Withrow, ed.), p. 717–750. Washington, D.C.: Amer. Ass. Advance. Sci. 1959.
-- Annual endocrine cycles in temperate-zone birds with special attention to the White-crowned Sparrow, Zonotrichia leucophrys gambelii. Proc. Second Int. Congr. Endocr., p. 114–118 (1964a).
— The photoperiodic control of reproductive cycles in birds. Amer. Sci. 52, 137–155 (1964b).
— Follett, B. K.: Light and other environmental factors affecting avian reproduction. J. anim. Sci 25 (Suppl.), 90–118 (1966).
— King, J. R., Morton, M. L.: A quantitative examination of ovarian growth in the White-crowned Sparrow. Biol. Bull. 130, 67–75 (1966).
Floquet, A., Grignon, G.: Etude histologique du follicule postovulatoire chez la Poule. C. R. Soc. Biol. (Paris) 158, 132–135 (1964).
Fraps, R. M.: Ovulation in the domestic fowl. In: Control of ovulation (C. A. Villee, ed.), p. 133–162. New York: Pergamon Press 1961.
Gilbert, A. B.: Observations on the ultrastructure of the postovulatory follicle of the domestic hen. In: VIe Congr. Inst. Reprod. Anim. et Insémination Artificielle (C. Thibault, ed.), vol. II, p. 1629–1631. Paris: Inst. Nat. Rech. Agron. 1968.
— Wood-Gush, D. G. M.: The control of the nesting behaviour of the domestic hen. III. The effect of cocaine in the postovulatory follicle. Anim. Behav. 13, 284–285 (1965).
Herbst, A. L.: Response of rat ovarian cholesterol to gonadotropins and anterior pituitary hormones. Endocrinology 81, 54–60 (1967).
Hilton, F. K.: Relationships of testicular cholesterol to hormonal activity and behavior in the starling. Proc. Soc. exp. Biol. (N.Y.) 107, 653–655 (1961).
Hinde, R. A., Steel, E., Hutchison, R.: Control of oviduct development in ovariectomized canaries by exogenous hormones. J. Zool. (Lond.) 163, 265–276 (1971).
Humason, G. L.: Animal tissue techniques. San Francisco: W. H. Freeman & Co. 1962.
Hutchison, R. E., Hinde, R. A., Bendon, B.: Oviduct development and its relation to other aspects of reproduction in domesticated canaries. J. Zool. (Lond.) 155, 87–102 (1968).
Johnston, D. W.: The annual reproductive cycle of the California Gull. II. Histology and female reproductive system. Condor 58, 206–221 (1956).
King, J. R., Follett, B. K., Farner, D. S., Morton, M. L.: Annual gonadal cycles and pituitary gonadotropins in Zonotrichia leucophrys gambelii. Condor 68, 476–487 (1966).
Korenman, S. G., O'Malley, B. W.: Progesterone action: regulation of avidin biosynthesis by hen oviduct in vivo and in vitro. Endocrinology 83, 11–17 (1968).
Kramer, C. Y.: Extension of multiple range tests to group means with unequal numbers of replications. Biometrics 12, 307–310 (1956).
Laws, D. F., Farner, D. S.: Prolactin and the photoperiodic testicular response in White-crowned Sparrows. Endocrinology 67, 279–281 (1960).
Lehrman, D. S., Brody, P.: Does prolactin induce incubation behaviour in the Ring Dove? J. Endocr. 22, 269–275 (1961).
Marlow, H. W., Richert, D.: Estrogens of the fowl. Endocrinology 26, 531–534 (1940).
Marshall, A. J., Coombs, C. J. F.: The interaction of environmental, internal and behavioural factors in the rook, Corvus f. frugilegus Linnaeus. Proc. zool. soc. Lond. 128, 545–589 (1957).
Marza, V. D., Marza, E. V.: The formation of the hen's egg. I. Morphology and metabolism of yolk-formation. Quart. J. micr. Sci. 78, 134–160 (1935).
Meier, A. H.: Antigonadal effects of prolactin in the White-throated Sparrow, Zonotrichia albicollis. Gen comp. Endocr. 13, 222–225 (1969).
— Dusseau, J. W.: Prolactin and the photoperiodic gonadal response in several avian species. Physiol. Zool. 41, 95–103 (1968).
— Farner, D. S., King, J. R.: A possible endocrine basis for migratory behaviour in the White-crowned Sparrow, Zonotrichia leucophrys gambelii. Anim. Behav. 13, 453–465 (1965).
Mewaldt, L. R., Kibby, S. S., Morton, M. L.: Comparative biology of Pacific coastal White-crowned Sparrows. Condor 70, 14–30 (1968).
Nalbandov, A. V., James, M. F.: The blood-vascular system of the chicken ovary. Amer. J. Anat. 85, 347–377 (1949).
Oka, T., Schimke, R. T.: Interaction of estrogen and progesterone in chick oviduct development. II. Effects of estrogen and progesterone on tubular gland cell function. J. Cell Biol. 43, 123–137 (1969).
Payne, R. B.: The post-ovulatory follicles of blackbirds (Agelaius). J. Morph. 118, 331–351 (1966).
Riddle, O., Lahr, E. L.: On broodiness of ring doves following implants of certain steroid hormones. Endocrinology 35, 255–260 (1944).
Ringoen, A. R.: Effects of injections of testosterone propionate on the reproductive system of the female English Sparrow, Passer domesticus (Linnaeus). J. Morph. 73, 423–439 (1943).
Searcy, R. L., Bergquist, L. M.: A new color reaction for the quantitation of serum cholesterol. Clin. chim. Acta 5, 192–199 (1960).
Simkiss, K.: Calcium metabolism and avian reproduction. Biol. Rev. 36, 321–367 (1961).
Taber, E.: Androgen secretion in the fowl. Endocrinology 48, 6–16 (1951).
Vaugien, L.: Recherches biologiques et expérimentales sur le cycle reproducteur et la mue des Oiseaux passériformes. Bull. Biol. France Belg. 82, 166–213 (1948).
Woods, J. E., Domm, L. V.: A histochemical identification of the androgen-producing cells in the gonads of the domestic fowl and albino rat. Gen. comp. Endocr. 7, 559–570 (1966).
Wyburn, G. M., Aitken, R. N. C., Johnston, H. S.: The ultrastructure of the zona radiata of the ovarian follicle of the domestic fowl. J. Anat. (Lond.) 99, 469–484 (1965).
— Baillie, A. H.: Some observations on the fine structure and histochemistry of the ovarian follicle of the fowl. In: Physiology of the domestic fowl (C. Horton-Smith, and E. C. Amoroso, ed.), p. 30–38. Edinburgh: Oliver & Boyd Ltd. 1966.
Wynne-Edwards, V. C.: Intermittent breeding of the fulmar (Fulmarus glacialis (L.)) with some general observations on non-breeding in seabirds. Proc. zool. Soc. London A 109, 127–132 (1939).
Zarrow, M. X., Clark, J. H.: Gonadotropin regulation of ovarian cholesterol levels in the rat. Endocrinology 84, 340–346 (1969).
Author information
Authors and Affiliations
Additional information
This study was supported by an NIH Training Grant (GM 01276) from the National Institute of General Medical Sciences. It is a pleasure to thank Brina Kessel and George West at the University of Alaska for their assistance during summer collections in 1968. William deGraw helped me throughout the study. Wallace Moreland of the Singer-Friden Company provided a desk calculator. Ari von Tienhoven and William Wimsatt were kind enough to read and criticize the manuscript. Donald Farner, Paul Harrison, Herbert Eastlick, Leonard Kirschner, and in particular James R. King made invaluable suggestions while the work was in progress. This paper is based on a dissertation done in partial fulfillment of the Ph.D. requirements at Washington State University.
Rights and permissions
About this article
Cite this article
Kern, M.D. Seasonal changes in the reproductive system of the female white-crowned sparrow, Zonotrichia leucophrys gambelii, in captivity and in the field. Z.Zellforsch 126, 297–319 (1972). https://doi.org/10.1007/BF00306846
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00306846