Advertisement

Acta Biologica Hungarica

, Volume 61, Issue 3, pp 237–249 | Cite as

Seasonal Changes in Hypothalamic Gonadotropin-Releasing Hormone-I Immunoreactivity in Relation With Testicular Volume in Adult Male Free-Living European Starlings (Sturnus Vulgaris)

  • O. PintérEmail author
  • P. Péczel
Article

Abstract

Birds from the temperate and cold zones show annual sexual activity accompanied by gonadal changes and fuctuation in their brain gonadotropin-releasing hormone (GnRH) levels. However, most of the studies were done on captive birds where the constant environment can profoundly modify periodical changes. Therefore our aim was to reveal annual variations of hypothalamic and gonadal changes in male, free-living European starlings (Sturnus vulgaris) captured directly from their natural environment. We analyzed hypothalamic GnRH-I immunoreactivity and testes volume. Four key time points of the active reproductive cycle and the photorefractory phase were studied. GnRH-I immunoreactivity was analyzed in the preoptic area (POA) and the median eminence (ME). Photorefractory birds (August) with regressed gonads had the lowest level of GnRH-I immunoreactivity compared to other birds from the active reproductive phases. These results suggest that parallel with the gonadal volume GnRH-I undergoes seasonal changes in adult male free-living European starlings.

Keywords

European starling seasonal reproduction GnRH-I testes immunohistochemistry 

Abbrevations

ABC

avidin-biotin complex

FSH

follicle-stimulating hormone

GnRH

gonadotropin-releasing hormone

GnRH-ir

GnRH immunoreactivity

KPBS

potassium-phosphate buffer

L:D

light/dark hours per day

LH

luteinizing hormone

ME

median eminence

POA

preoptic area

TrSM

tractus septomesenchephalicus

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Bentley, G. E., Moore, I. T., Sower, S. A., Wingfield J. C. (2004) Evidence for a novel gonadotropin-releasing hormone in hypothalamic and forebrain areas in songbirds. Brain Behav. Evol. 63, 34–46.CrossRefGoogle Scholar
  2. 2.
    Cho, R. N., Hahn T. R. MacDougall-Shackleton, S. Ball G. F. (1998) Seasonal variation in brain GnRH in free-living breeding and photorefractory house finches (Carpodacus mexicanus). Gen. Comp. Endocrinol. 109, 244–250.CrossRefGoogle Scholar
  3. 3.
    Dawson, A. (2004) Evidence against a period of relative photorefractoriness during the recovery of photosensitivity in common starlings. Gen. Comp. Endocrinol. 136, 117–121.CrossRefGoogle Scholar
  4. 4.
    Dawson, A., Follett, B. K., Goldsmith, A. R., Nicholls T. J. (1987) Hypothalamic gonadotrophin-re-leasing hormone and pituitary and plasma FSH and prolactin during photostimulation and photorefractoriness in intact and thyroidectomized starlings (Sturnus vulgaris). J. Endocrinol. 115, 211–220.CrossRefGoogle Scholar
  5. 5.
    Dawson, A., Goldsmith A. R. (1983) Plasma prolactin and gonadotrophins during gonadal development and the onset of photorefractoriness in male and female starlings (Sturnus vulgaris) on artificial photoperiods. J. Endocrinol. 97, 253–260.CrossRefGoogle Scholar
  6. 6.
    Dawson, A., Goldsmith A. R. (1997) Changes in gonadotrophin-releasing hormone (GnRH-I) in the pre-optic area and median eminence of starlings (Sturnus vulgaris) during the recovery of photosensitivity and during photostimulation. J. Reprod. Fertil. 111, 1–6.CrossRefGoogle Scholar
  7. 7.
    Dittami, J., Gwinner, E., Follett, B. K., Prossinger, H. (2005) Changes in circadian LH-secretion patterns and annual gonadal cycles in the male European starling (Sturnus vulgaris). J. Ornithol. 146, 338–347.CrossRefGoogle Scholar
  8. 8.
    Follett, B. K., Maung S. L. (1978) Rate of testicular maturation, in relation to gonadotrophin and testosterone levels, in quail exposed to various artificial photoperiods and to natural day lengths. J. Endocrinol. 78, 267–280.CrossRefGoogle Scholar
  9. 9.
    Foster, R. G., Panzica, G. C., Parry, D. M., Viglietti-Panzica, C. (1988) Immunocytochemical studies on the LHRH system of the Japanese quail: inluence by photoperiod and aspects of sexual differentiation. Cell Tissue Res. 253, 327–335.CrossRefGoogle Scholar
  10. 10.
    Foster, R. G., Plowman, G., Goldsmith, A. R., Follett B. K. (1987) Immunohistochemical demonstration of marked changes in the LHRH system of photosensitive and photorefractory European starlings (Sturnus vulgaris). J. Endocrinol. 115, 211–220.CrossRefGoogle Scholar
  11. 11.
    Hahn, T. P., Ball G. F. (1995) Changes in brain GnRH associated with photorefractoriness in house sparows (Passer domesticus). Gen. Comp. Endocrinol. 99, 349–363.CrossRefGoogle Scholar
  12. 12.
    Kern, M. D. (1979) Seasonal changes in the reproductive system of the female white-crowned sparrow, Zonotrichia leucophrys gambelii, in captivity and in the field. 2. The incubation patch. Cell Tissue Res. 202, 379–398.CrossRefGoogle Scholar
  13. 13.
    Kordonowy, L. L., McMurtry, J. P., Williams T. D. (2009) Variation in plasma leptin-like immunore-activity in free-living European starlings (Sturnus vulgaris). Gen. Comp. Endocrinol. 166, 47–53.CrossRefGoogle Scholar
  14. 14.
    Lambrechts, M. M., Perret, P. (2000) Along photoperiod overrides non-photoperiodic factors in blue tits’ timing of reproduction. Proc. Biol. Sci. 267, 585–588.CrossRefGoogle Scholar
  15. 15.
    Lambrechts, M. M., Perret, P., Maistre, M., Blondel, J. (1999) Do experiments with captive non-domesticated animals make sense without population field studies? A case study with blue tits’ breeding time. Proc. R. Soc. Lond. B 266, 1311–1315.CrossRefGoogle Scholar
  16. 16.
    Maney, D. L., Richardson, R. D., Wingfield J. C. (1997) Central administration of chicken gonado-tropin-releasing hormone-II enhances courtship behavior in a female sparrow. Horm. Behav. 32, 11–18.CrossRefGoogle Scholar
  17. 17.
    Meddle, S. L., Maney, D. L., Wingfield J. C. (1999) Effects of N-methyl-D-aspartate on luteinizing hormone release and Fos-like immunoreactivity in the male White-crowned sparrow (Zonotrichia leucophrys gambelii). Endocrinol. 140, 5922–5928.CrossRefGoogle Scholar
  18. 18.
    Millam, J. R., Ottinger, M. A., Craig-Veit, C. B., Fan, Y., Chaiseha, Y., el Halawani, M. (1998) Multiple forms of GnRH are released from perifused medial basal hypothalamic/preoptic area (MBH/ POA) expiants in birds. Gen. Comp. Endocrinol. 111, 95–101.CrossRefGoogle Scholar
  19. 19.
    Molnár, Gy. (1982) Populációökológiai vizsgálatok a Sturnus vulgarison. Doktori értekezés. JATE Állattani Tanszék, Szeged (in Hungarian).Google Scholar
  20. 20.
    Nicholls, T. J., Goldsmith, A. R., Dawson, A. (1988) Photorefractoriness in birds and comparison with mammals. Physiol. Rev. 68, 133–176.CrossRefGoogle Scholar
  21. 21.
    Parry, D. M., Goldsmith, A. R., Millar, R. P., Glennie L. M. (1997) Immunocytochemical localization of GnRH precursor in the hypothalamus of European starlings during sexual maturation and photorefractoriness. J. Neuroendocrinal. 9, 235–243.CrossRefGoogle Scholar
  22. 22.
    Pereyra, M. E., Sharbaugh, S. M., Hahn T. P. (2005) Interspecific variation in photo-induced GnRH plasticity among nomadic cardueline finches. Brain. Behav. Evol. 66, 35–49.CrossRefGoogle Scholar
  23. 23.
    Perfito, N., Bentley, G. E., Hau, M. (2006) Tonic activation of brain GnRH immunoreactivity despite reduction of peripheral reproductive parameters in opportunistically breeding zebra finches. Brain Behav. Evol. 67, 123–134.CrossRefGoogle Scholar
  24. 24.
    Phillmore, L. S., Hoshooley, J. S., Hahn, T. P., MacDougall-Shackleton, S.A. (2005) Atest of absolute photorefractoriness and photo-induced neural plasticity of song-control regions in black-capped chickadees (Poecile atricapillus). Can. J. Zool. 83, 747–753.CrossRefGoogle Scholar
  25. 25.
    Riters, L. V., Eens, M., Pinxten, R., Duffy, D. L., Balthazart, J., Ball G. F. (2000) Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm. Behav. 38, 250–261.CrossRefGoogle Scholar
  26. 26.
    Robinson, J. E., Follett B. K. (1982) Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. R. Soc. Lond. B. Biol. Sci. 215, 95–116.CrossRefGoogle Scholar
  27. 27.
    Sharp, P. J., Talbot, R. T., Main, G. M., Dunn, I. C., Fraser, H. M., Huskisson N. S. (1990) Physiological roles of chicken LHRH-I and -II in the control of gonadotropin release in the domestic chicken. J. Endocrinol. 124, 291–299.CrossRefGoogle Scholar
  28. 28.
    Small, W. T., Sharp, P. J., Bentley, G. E., Millar, R. P., Tsutsui, K., Mura, E., Deviche, P. (2008) Photoperiod-independent hypothalamic regulation of luteinizing hormone secretion in a free-living sonoran desert bird, the rufous-winged sparrow (Aimophila carpalis). Brain. Behav. Evol. 71, 127–142.CrossRefGoogle Scholar
  29. 29.
    Stevenson, T. J., Ball G. F. (2009) Anatomical localization of the effects of reproductive state, castration, and social milieu on cells immunoreactive for gonadotropin-releasing hormone-I in male European starlings (Sturnus vulgaris). J. Comp. Neurol. 517, 146–155.CrossRefGoogle Scholar
  30. 30.
    Stevenson, T. J., Bernard, D. J., Ball G. F. (2009) Photoperiodic condition is associated with region-specific expression of GNRH1 mRNA in the preoptic area of the male starling (Sturnus vulgaris). Biol. Reprod. 81, 674–680.CrossRefGoogle Scholar
  31. 31.
    Stevenson, T. J., Lynch, K. S., Lamba, P., Ball, G. F., Bernard D. J. (2009) Cloning of gonadotropin-releasing hormone I complementary DNAs in songbirds facilitates dissection of mechanisms mediating seasonal changes in reproduction. Endocrinol. 150, 1826–1833.CrossRefGoogle Scholar
  32. 32.
    Stevenson, T. J., Macdougall-Shackleton, S. A. (2005) Season- and age-related variation in neural cGnRH-I and cGnRH-II immunoreactivity in house sparrows (Passer domesticus). Gen. Comp. Endocrinol. 143, 33–39.CrossRefGoogle Scholar
  33. 33.
    Ubuka, T., Cadigan, P. A., Wang, A., Liu, J., Bentley G. E. (2009) Identification of European starling GnRH-I precursor mRNA and its seasonal regulation. Gen. Comp. Endocrinol. 162, 301–306.CrossRefGoogle Scholar
  34. 34.
    Ubuka, T., Kim, S., Huang, Y., Reid, J., Jiang, J., Osugi, T., Chowdhury, V. S., Tsutsui, K., Bentley, G E. (2008) Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in european starling brain. Endocrinol. 149, 268–278.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2010

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Laboratory of Molecular Neuroendocrinogy, Institute of Experimental MedicineHungarian Academy of SciencesBudapestHungary
  2. 2.Laboratory of Reproductive Biology, Institute of Animal HusbandrySzent István UniversityGödöllőHungary

Personalised recommendations