|
Sign In to gain access to subscriptions and/or personal tools.
|
Photoperiodic Control of Seasonality in Birds
Alistair Dawson
Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton, Huntingdon, Cambridgeshire, PE28 2LS, UK
Verdun M. King
Department of Anatomy, University of Cambridge, Downing Site, Cambridge CB2 3DY, UK
George E. Bentley
Gregory F. Ball
Department of Psychology, Johns Hopkins University, 3400 N. Charles Street, Baltimore, MD 21218-2686, USA
This review examines how birds use the annual cycle in photoperiod to ensure that seasonal events—breeding, molt, and song production—happen at the appropriate time of year. Differences in breeding strategies between birds and mammals reflect basic differences in biology. Avian breeding seasons tend to be of shorter duration and more asymmetric with respect to changes in photoperiod. Breeding seasons can occur at the same time each year (predictable) or at different times (opportunistic), depending on the food resource. In all cases, there is evidence for involvement of photoperiodic control, nonphotoperiodic control, and endogenous circannual rhythmicity. In predictable breeders (most nontropical species), photoperiod is the predominant proximate factor. Increasing photoperiods of spring stimulate secretion of gonadotropin-releasing hormone (GnRH) and consequent gonadal maturation. However, breeding ends before the return of short photoperiods. This is the consequence of a second effect of long photoperiods—the induction of photorefractoriness. This dual role of long photoperiods is required to impart the asymmetry in breeding seasons. Typically, gonadal regression through photorefractoriness is associated with a massive decrease in hypothalamic GnRH, essentially a reversal to a pre-pubertal condition. Although breeding seasons are primarily determined by photoperiodic control of GnRH neurons, prolactin may be important in determining the exact timing of gonadal regression. In tropical and opportunistic breeders, endogenous circannual rhythmicity may be more important. In such species, the reproductive system remains in a state of "readiness to breed" for a large part of the year, with nonphotic cues acting as proximate cues to time breeding. Circannual rhythmicity may result from a temporal sequence of different physiological states rather than a molecular or cellular mechanism as in circadian rhythmicity. Avian homologues of mammalian clock genes Per2, Per3, Clock, bmal1, and MOP4 have been cloned. At the molecular level, avian circadian clocks appear to function in a similar manner to those of mammals. Photoperiodic time measurement involves interaction between a circadian rhythm of photoinducibility and, unlike mammals, deep brain photoreceptors. The exact location of these remains unclear. Although the eyes and pineal generate a daily cycle in melatonin, this photoperiodic signal is not used to time seasonal breeding. Instead, photoperiodic responses appear to involve direct interaction between photoreceptors and GnRH neurons. Thyroid hormones are required in some way for this system to function. In addition to gonadal function, song production is also affected by photoperiod. Several of the nuclei involved in the song system show seasonal changes in volume, greater in spring than in the fall. The increase in volume is, in part, due to an increase in cell number as a result of neurogenesis. There is no seasonal change in the birth of neurons but rather in their survival. Testosterone and melatonin appear to work antagonistically in regulating volume.
Key Words: birds • photoperiodism • photorefractoriness • gonadotropin-releasing hormone • circadian rhythmicity • pineal • song
Journal of Biological Rhythms, Vol. 16, No. 4,
365-380 (2001)
DOI: 10.1177/074873001129002079
 CiteULike  Complore  Connotea  Del.icio.us  Digg  Reddit  Technorati  Twitter What's this?
This article has been cited by other articles:
|
|
|
|
 
V. S. Chowdhury, K. Yamamoto, T. Ubuka, G. E. Bentley, A. Hattori, and K. Tsutsui
Melatonin Stimulates the Release of Gonadotropin-Inhibitory Hormone by the Avian Hypothalamus
Endocrinology,
January 1, 2010;
151(1):
271 - 280.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Yasuo and T. Yoshimura
Comparative analysis of the molecular basis of photoperiodic signal transduction in vertebrates
Integr. Comp. Biol.,
November 1, 2009;
49(5):
507 - 518.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. A. MacDougall-Shackleton, T. J. Stevenson, H. E. Watts, M. E. Pereyra, and T. P. Hahn
The evolution of photoperiod response systems and seasonal GnRH plasticity in birds
Integr. Comp. Biol.,
November 1, 2009;
49(5):
580 - 589.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Perfito and G. E. Bentley
Opportunism, photoperiodism, and puberty: Different mechanisms or variations on a theme?
Integr. Comp. Biol.,
November 1, 2009;
49(5):
538 - 549.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. J. Stevenson, D. J. Bernard, and G. F. Ball
Photoperiodic Condition Is Associated with Region-Specific Expression of GNRH1 mRNA in the Preoptic Area of the Male Starling (Sturnus vulgaris)
Biol Reprod,
October 1, 2009;
81(4):
674 - 680.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. P. Caro and M. E. Visser
Temperature-induced elevation of basal metabolic rate does not affect testis growth in great tits
J. Exp. Biol.,
July 1, 2009;
212(13):
1995 - 1999.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
U. Lagercrantz
At the end of the day: a common molecular mechanism for photoperiod responses in plants?
J. Exp. Bot.,
July 1, 2009;
60(9):
2501 - 2515.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Deviche
Reproductive Physiology: Songbird Study Removes Long-Standing Neuroendocrinology Research Roadblock
Endocrinology,
April 1, 2009;
150(4):
1561 - 1562.
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. J. Stevenson, K. S. Lynch, P. Lamba, G. F. Ball, and D. J. Bernard
Cloning of Gonadotropin-Releasing Hormone I Complementary DNAs in Songbirds Facilitates Dissection of Mechanisms Mediating Seasonal Changes in Reproduction
Endocrinology,
April 1, 2009;
150(4):
1826 - 1833.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Budki, S. Rani, and V. Kumar
Food deprivation during photosensitive and photorefractory life-history stages affects the reproductive cycle in the migratory Red-headed Bunting (Emberiza bruniceps)
J. Exp. Biol.,
January 15, 2009;
212(2):
225 - 230.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. C. P. Renn, N. Aubin-Horth, and H. A. Hofmann
Fish and chips: functional genomics of social plasticity in an African cichlid fish
J. Exp. Biol.,
September 15, 2008;
211(18):
3041 - 3056.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. J Greives, L. J Kriegsfeld, G. E Bentley, K. Tsutsui, and G. E Demas
Recent advances in reproductive neuroendocrinology: a role for RFamide peptides in seasonal reproduction?
Proc R Soc B,
September 7, 2008;
275(1646):
1943 - 1951.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Nakao, H. Ono, and T. Yoshimura
Thyroid hormones and seasonal reproductive neuroendocrine interactions
Reproduction,
July 1, 2008;
136(1):
1 - 8.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. G. Revel, M. Saboureau, P. Pevet, V. Simonneaux, and J. D. Mikkelsen
RFamide-Related Peptide Gene Is a Melatonin-Driven Photoperiodic Gene
Endocrinology,
March 1, 2008;
149(3):
902 - 912.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. M. Cassone, P. A. Bartell, B. J. Earnest, and V. Kumar
Duration of Melatonin Regulates Seasonal Changes in Song Control Nuclei of the House Sparrow, Passer domesticus: Independence from Gonads and Circadian Entrainment
J Biol Rhythms,
February 1, 2008;
23(1):
49 - 58.
[Abstract]
[PDF]
|
|
|
|
|
|
|
T. W. Small, P. J. Sharp, G. E. Bentley, and P. Deviche
Relative Photorefractoriness, Prolactin, and Reproductive Regression in a Flexibly Breeding Sonoran Desert Passerine, the Rufous-Winged Sparrow, Aimophila carpalis
J Biol Rhythms,
February 1, 2008;
23(1):
69 - 80.
[Abstract]
[PDF]
|
|
|
|
|
|
|
G. F Ball and E. D Ketterson
Sex differences in the response to environmental cues regulating seasonal reproduction in birds
Phil Trans R Soc B,
January 27, 2008;
363(1490):
231 - 246.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. B Martin, Z. M Weil, and R. J Nelson
Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs
Phil Trans R Soc B,
January 27, 2008;
363(1490):
321 - 339.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J Paul, I. Zucker, and W. J Schwartz
Tracking the seasons: the internal calendars of vertebrates
Phil Trans R Soc B,
January 27, 2008;
363(1490):
341 - 361.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Wikelski, L. B Martin, A. Scheuerlein, M. T Robinson, N. D Robinson, B. Helm, M. Hau, and E. Gwinner
Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control
Phil Trans R Soc B,
January 27, 2008;
363(1490):
411 - 423.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Ubuka, S. Kim, Y.-c. Huang, J. Reid, J. Jiang, T. Osugi, V. S. Chowdhury, K. Tsutsui, and G. E. Bentley
Gonadotropin-Inhibitory Hormone Neurons Interact Directly with Gonadotropin-Releasing Hormone-I and -II Neurons in European Starling Brain
Endocrinology,
January 1, 2008;
149(1):
268 - 278.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Voigt, W. Goymann, and S. Leitner
Green Matters! Growing Vegetation Stimulates Breeding under Short-Day Conditions in Wild Canaries (Serinus canaria)
J Biol Rhythms,
December 1, 2007;
22(6):
554 - 557.
[PDF]
|
|
|
|
|
|
|
D. L. Maney, C. T. Goode, J. I. Lake, H. S. Lange, and S. O'Brien
Rapid Neuroendocrine Responses to Auditory Courtship Signals
Endocrinology,
December 1, 2007;
148(12):
5614 - 5623.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. B. Zawilska, A. Lorenc, M. Berezinska, B. Vivien-Roels, P. Pevet, and D. J. Skene
Photoperiod-Dependent Changes in Melatonin Synthesis in the Turkey Pineal Gland and Retina
Poult. Sci.,
July 1, 2007;
86(7):
1397 - 1405.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. J. Greives, A. O. Mason, M.-A. L. Scotti, J. Levine, E. D. Ketterson, L. J. Kriegsfeld, and G. E. Demas
Environmental Control of Kisspeptin: Implications for Seasonal Reproduction
Endocrinology,
March 1, 2007;
148(3):
1158 - 1166.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Watanabe, T. Yamamura, M. Watanabe, S. Yasuo, N. Nakao, A. Dawson, S. Ebihara, and T. Yoshimura
Hypothalamic expression of thyroid hormone-activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals
Am J Physiol Regulatory Integrative Comp Physiol,
January 1, 2007;
292(1):
R568 - R572.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. A. MacDougall-Shackleton, M. Katti, and T. P. Hahn
Tests of absolute photorefractoriness in four species of cardueline finch that differ in reproductive schedule
J. Exp. Biol.,
October 1, 2006;
209(19):
3786 - 3794.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. G. Revel, M. Saboureau, P. Pevet, J. D. Mikkelsen, and V. Simonneaux
Melatonin Regulates Type 2 Deiodinase Gene Expression in the Syrian Hamster
Endocrinology,
October 1, 2006;
147(10):
4680 - 4687.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Proudman and T. D. Siopes
Potential Role of Thyroid Hormones and Prolactin in the Programming of Photorefractoriness in Turkey Hens
Poult. Sci.,
August 1, 2006;
85(8):
1457 - 1461.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. F. Ball
Thyroid Hormone Transport and Photoperiodism: Feeling One's Oatps.
Endocrinology,
March 1, 2006;
147(3):
1065 - 1066.
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Ubuka, K. Ukena, P. J. Sharp, G. E. Bentley, and K. Tsutsui
Gonadotropin-Inhibitory Hormone Inhibits Gonadal Development and Maintenance by Decreasing Gonadotropin Synthesis and Release in Male Quail
Endocrinology,
March 1, 2006;
147(3):
1187 - 1194.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. W. Wilhelms, S. A. Cutler, J. A. Proudman, L. L. Anderson, and C. G. Scanes
Atrazine and the Hypothalamo-Pituitary-Gonadal Axis in Sexually Maturing Precocial Birds: Studies in Male Japanese Quail
Toxicol. Sci.,
July 1, 2005;
86(1):
152 - 160.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. T. Moore, F. Bonier, and J. C. Wingfield
Reproductive asynchrony and population divergence between two tropical bird populations
Behav. Ecol.,
July 1, 2005;
16(4):
755 - 762.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. W Sockman, K. B Sewall, G. F Ball, and T. P Hahn
Economy of mate attraction in the Cassin's finch
Biol Lett,
March 22, 2005;
1(1):
34 - 37.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Ubuka, G. E. Bentley, K. Ukena, J. C. Wingfield, and K. Tsutsui
Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain
PNAS,
February 22, 2005;
102(8):
3052 - 3057.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. T. Moore, J. C. Wingfield, and E. A. Brenowitz
Plasticity of the Avian Song Control System in Response to Localized Environmental Cues in an Equatorial Songbird
J. Neurosci.,
November 10, 2004;
24(45):
10182 - 10185.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Yamamura, K. Hirunagi, S. Ebihara, and T. Yoshimura
Seasonal Morphological Changes in the Neuro-Glial Interaction between Gonadotropin-Releasing Hormone Nerve Terminals and Glial Endfeet in Japanese Quail
Endocrinology,
September 1, 2004;
145(9):
4264 - 4267.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. W. Sockman, T. D. Williams, A. Dawson, and G. F. Ball
Prior Experience with Photostimulation Enhances Photo-Induced Reproductive Development in Female European Starlings: A Possible Basis for the Age-Related Increase in Avian Reproductive Performance
Biol Reprod,
September 1, 2004;
71(3):
979 - 986.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M.M. Ben Saad and D.L. Maurel
Reciprocal Interaction Between Seasonal Testis and Thyroid Activity in Zembra Island Wild Rabbits (Oryctolagus cuniculus): Effects of Castration, Thyroidectomy, Temperature, and Photoperiod
Biol Reprod,
April 1, 2004;
70(4):
1001 - 1009.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. F. Ball and J. Balthazart
Birds Return Every Spring Like Clockwork, but Where Is the Clock?
Endocrinology,
September 1, 2003;
144(9):
3739 - 3741.
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. H. Stehle, C. von Gall, C. Schomerus, and H.-W. Korf
Of Rodents and Ungulates and Melatonin: Creating a Uniform Code for Darkness by Different Signaling Mechanisms
J Biol Rhythms,
August 1, 2001;
16(4):
312 - 325.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M. H. Hastings and B. K. Follett
Toward a Molecular Biological Calendar?
J Biol Rhythms,
August 1, 2001;
16(4):
424 - 430.
[PDF]
|
|
|
|
|
