Light increases the rate of embryonic development: Implications for latitudinal trends in incubation period

Functional Ecology

Volumn 25, Issue 4, 2011, Pages 769-776

  Cooper, Caren B ^a   Voss, Margaret A ^b   Ardia, Daniel R ^c   Austin, Suzanne H ^d   Robinson, W Douglas ^d  

^a Johnson Center for Birds and Biodiversity   (United States)

^b BEHREND COLLEGE   (United States)

^c FRANKLIN AND MARSHALL COLLEGE   (United States)

^d OREGON STATE UNIVERSITY   (United States)

Author keywords

Avian incubation period; Embryonic metabolic rate; House sparrow; Life history evolution; Passer domesticus; Photoacceleration; Photocycles; Photoperiod

Indexed keywords

BIOTIC FACTOR; EMBRYONIC DEVELOPMENT; GAMEBIRD; INCUBATION; LATITUDINAL GRADIENT; LIFE HISTORY TRAIT; LIGHT EFFECT; PHOTOPERIOD; RESOURCE ALLOCATION; SONGBIRD; TROPICAL REGION; WILD POPULATION;

AVES; GALLIFORMES; PASSER DOMESTICUS; PASSERIFORMES;

EID: 79959830466     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2011.01847.x     Document Type: Article

References (69)

1. Akasaka, K., Nasu, T., Katayama, T. & Murakami, N. (1995) Development of regulation of melatonin release in pineal cells in chick embryo. Brain Research, 692, 283-286.
2. Ardia, D.R., Perez, J. & Clotfelter, E.D. (2010) Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proceedings of the Royal Society B-Biological Sciences, 277, 1881-1888.
3. Ardia, D.R., Perez, J.H., Chad, E.K., Voss, M.A. & Clotfelter, E.D. (2009) Temperature and life history: experimental heating leads female tree swallows to modulate egg temperature and incubation behavior. Journal of Animal Ecology, 78, 4-13.
4. Bacon, W.L. (1984) Intermittent light on turkey breeders. Poultry Digest, 43, 114-118.
5. Blount, J.D., Metcalfe, N.B., Arnold, K.E., Surai, P.F. & Monaghan, P. (2006) Effects of neonatal nutrition on adult reproduction in a passerine bird. Ibis, 148, 509-514.
6. Brawn, J.D., Karr, J.R., Nichols, J.D. & Robinson, W.D. 1999. Demography of forest birds in Panama: How do transients affect estimates of survival rates? Proceedings of the International Ornithological Congress, XXII: 297-303.
7. Carey, C., Thompson, E.L., Vleck, C.M. & James, F.C. (1982) Avian reproduction over an altitudinal gradient: incubation period, hatchling mass, and embryonic oxygen consumption. Auk, 99, 710-718.
8. Cooper, C.B., Hochachka, W., Butcher, G. & Dhondt, A.A. (2005) Egg viability as a constraint on seasonal and latitudinal trends in clutch size. Ecology, 86, 2018-2031.
9. Daan, S. & Aschoff, J. (1975) Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia, 18, 269-316.
10. Dawson, A. & Van't Hof, T.J. (2002) Ontogeny of the daily profile of plasma melatonin in European starlings raised under long or short photoperiods. Journal of Biological Rhythms, 17, 259-265.
11. Dawson, A., King, V.M., Bentley, G.E. & Ball, G.F. (2001) Photoperiodic control of seasonality in birds. Journal of Biological Rhythms, 16, 365-380.
12. Ghatpande, A., Ghatpande, S. & Khan, M.Z. (1995) Effect of different intensities of fluorescent light on the early development of chick embryos in ovo. Cellular and Molecular Biology Research, 41, 613-621.
13. Gimeno, M.A., Roberts, C.M. & Webb, J.L. (1967) Acceleration of rate of the early chick embryo heart by visible light. Nature, 214, 1014-1016.
14. Gwinner, E., Zeman, M. & Klaassen, M. (1997) Synchronization by low-amplitude light-dark cycles of 24-hour pineal and plasma melatonin rhythms of hatchling European starlings (Sturnus vulgaris). Journal of Pineal Research, 23, 176-181.
15. Halevy, O., Piestun, Y., Rozenboim, I. & Yablonka-Reuveni, Z. (2006) In ovo exposure to monochromatic green light promotes skeletal muscle cell proliferation and affects myofiber growth in posthatch chicks. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, 290, R1062-R1070.
16. Hill, W.L., Bassi, K.L., Bonaventura, L. & Sacus, J.E. (2004) Prehatch entrainment of circadian rhythms in the domestic chick using different light regimes. Developmental Psychobiology, 45, 174-186.
17. Isakson, S.T., Huffman, B.J. & Siegel, P.B. (1970) Intensities of incandescent light and the development of chick embryos in ovo and in vitro. Comparative Biochemistry & Physiology, 55, 229-235.
18. Johnston, J., White, S., Peach, W. & Gregory, R. (1997) Survival rates of tropical and temperate passerines: a Trinidadian perspective. American Naturalist, 150, 771-789.
19. Karr, J., Nichols, J., Klimkiewicz, M. & Brawn, J. (1990) Survival rates of birds of tropical and temperate forests: will the dogma survive. American Naturalist, 136, 277-291.
20. Karu, T.I. (1988) Molecular mechanisms of the therapeutic effect of low-intensity laser radiation. Lasers in the Life Sciences, 2, 53-74.
21. King, J.R. & Hubbard, J.D. (1981) Comparative patterns of nestling growth in White-crowned Sparrows. Condor, 83, 362-369.
22. Kuehler, C.M., Lieberman, A., McIlraith, B., Everett, W., Scott, T.A., Morrison, M.L. & Winchell, C. (1993) Artificial incubation and hand-rearing of Loggerhead Shrikes. Wildlife Society Bulletin, 21, 165-171.
23. Kuo, Z. (1932) Ontogeny of embryonic behavior in Aves. V. The reflex concept in the light of embryonic behavior in birds. Psychological Review, 39, 499-515.
24. Lack, D.L. 1968. Ecological Adaptations for Breeding in Birds. Methuen, London.
25. Lack, D. & Moreau, R. (1965) Clutch size in tropical birds of forest and savanna. In Oiseau et la Revue Francaise d'Ornithologie, (Suppl.), 76-89.
26. Lauber, J.K. (1975) Photoacceleration of avian embryogenesis. Comparative Biochemistry and Physiology, 51A, 903-907.
27. Lowther, Peter.E. & Cink, Calvin.L. (2006) House Sparrow (Passer domesticus). The Birds of North America Online (ed. A. Poole). Cornell Lab of Ornithology, Ithaca; Retrieved from the Birds of North America Online: doi.
28. Lynch, H.J., Deng, M. & Wurtman, R.J. (1984) Light intensities required to suppress nocturnal melatonin secretion in albino and pigmented rats. Life Sciences, 35, 841-847.
29. Martin, T.E. (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecological Monographs, 65, 101-127.
30. Martin, T.E. & Schwabl, H. (2008) Variation in maternal effects and embryonic development rates among passerine species. Proceedings of the Royal Society of London, Series B, 363, 1663-1674.
31. Martin, T.E., Martin, P.R., Olson, C.R., Heidinger, B.J. & Fontaine, J.J. (2000) Parental care and clutch sizes in North and South American birds. Science, 287, 1482-1485.
32. Martin, T.E., Auer, S.K., Bassar, R.D., Niklison, A.M. & Lloyd, P. (2007) Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution, 61, 2558-2569.
33. Mead, P.S. & Morton, M.L. (1985) Hatching asynchrony in the Mountain White-crowned Sparrow (Zonotrichia leucophrys oriantha): a selected or incidental trait? Auk, 102, 781-792.
34. Moreau, R. (1944) Clutch-size: a comparative study with special reference to African birds. Ibis, 86, 286-347.
35. Moriya, K., Höchel, J., Pearson, J. & Tazawa, H. (1999) Cardiac rhythms in developing chicks. Comparative Biochemistry and Physiology, 124, 461-468.
36. Morton, M.L. (1976) Adaptive strategies of Zonotrichia breeding at high latitude or high altitude. Proceedings of the 16th International Ornithologists Congress, 322-336.
37. Nakao, N., Yasuo, S., Nishimura, A., Yamamura, T., Watanabe, T., Anraku, T., Okano, T., Fukada, Y., Sharp, P.J., Ebihara, S. & Yoshimura, T. (2007) Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology, 148, 3031-3038.
38. Nichelmann, M. (2004) Perinatal epigenetic temperature adaptation in avian species: comparison of turkey and muscovy duck. Journal of Thermal Biology, 29, 613-619.
39. Nichelmann, M., Hochel, J. & Tzschentke, B. (1999) Biological rhythms in birds - development, insights and perspectives. Comparative Biochemistry and Physiology, 124A, 429-437.
40. Okabayashi, N., Yasuoa, S., Watanabea, M., Namikawab, T., Ebiharaa, S. & Yoshimura, T. (2003) Ontogeny of circadian clock gene expression in the pineal and the suprachiasmatic nucleus of chick embryo. Brain Research, 990, 231-234.
41. Preda, V., Mihalca, I., Cristea, M., Onea, O., Stanesca-Carpen, E., Muresanu, D. & Schuster, N. (1962) The actuon of medium conditions on the development of the embryo of the hen: IX. The influence of permanent light on the metabolic processes of the liver, the kidneyw, the brain, and heart of the embryo. Academie Republicii Populare Romine, Filala Cluj, Studii Cercetari Biology, 12, 235-251.
42. Prinzinger, R. & Hinninger, C. (1992) (Endogenous?) diurnal rhythm in the energy metabolism of pigeon embryos. Naturwissenschaften, 79, 278-279.
43. Rahn, H. & Paganelli, C.V. (1989) Shell mass, thickness and density of avian eggs derived from the tables of Schönwetter. Journal of Ornithology, 130, 59-68.
44. Ricklefs, R.E. (1969) The nesting cycle of songbirds in tropical and temperate regions. Living Bird, 8, 165-175.
45. Ricklefs, R.E. (1976) Growth rate of birds in the humid New World tropics. Ibis, 118, 176-207.
46. Ricklefs, R.E. & Wikelski, M. (2002) The physiology/life-history nexus. Trends in Ecology and Evolution, 17, 462-468.
47. Robinson, W.D., Styrsky, J.D., Payne, B.J., Given Harper, R. & Thompson, C.F. (2008) Why are incubation periods longer in the tropics? A common-garden experiment with House Wrens reveals it is all in the egg. American Naturalist, 171, 532-535.
48. Romanoff, A.L. & Romanoff, A.J. (1949) The Avian Egg. John Wiley & Sons, New York.
49. Romanoff, A.L. & Romanoff, A.J. 1967. Biochemistry of the Avian Embryo; a Quantitative Analysis of Prenatal Development. Interscience Publishers, New York.
50. Rompré, G.R. & Robinson, W.D. (2008) Predation, nest attendance, and long incubation periods of two Neotropical antbirds. Ecotropica, 14, 81-87.
51. Rowland, K.W. (1985) Intermittent lighting for laying fowls: a review. World Poultry Science, 1, 5-19.
52. Rozenboim, I., Piestun, Y., Mobarkey, N., Barak, M., Hoyzman, A. & Halevy, O. (2004) Monochromatic light stimuli during embryogenesis enhance embryo development and posthatch growth. Poultry Science, 83, 1413-1419.
53. Schaefer, H.C., Eshlamwata, G.W., Munyekenye, F.B. & Bohning-Gaese, K. (2004) Life-history of two African Sylvia warblers: low annual fecundity and long post-fledging care. Ibis, 146, 427-437.
54. Shafey, T. (2004) Effect of lighted incubation on embryonic growth and hatchability performance of two strains of layer breeder eggs. British Poultry Science, 45, 223-229.
55. Shafey, T., Ghannam, M.M., Al-Batshan, H.A. & Al-Ayed, M.S. (2004) Effect of pigment intensity and region of eggshell on the spectral transmission of light that passes through the eggshell of chickens. International Journal of Poultry Science, 3, 228-233.
56. Shutze, J.V., Lauber, J.K., Kato, M. & Wilson, W.O. (1962) Influence of incandescent and colored light on chicken embryos during incubation. Nature, 4854, 594-595.
57. Siegel, P.B., Isakson, S.T., Coleman, F.N. & Huffman, B.J. (1969) Photoacceleration of development in chick embryos. Comparative Biochemistry and Physiology, 28, 753-758.
58. Skutch, A.F. (1949) Do tropical birds rear as many young as they can nourish? Ibis, 91, 430-455.
59. Skutch, A.F. (1985) Clutch size, nesting success, and predation on nests of neotropical birds, reviewed. Ornithological Monographs, 36, 575-594.
60. Slaugh, B.T., Johnston, N.P., Patten, J.D. & White, G.W. (1988) Effects of photoperiod and intermittent lighting on reproduction in pheasant hens. Theriogenology, 30, 291-301.
61. Styrsky, J., Berthold, P. & Robinson, W. (2004) Endogenous control of migration and calendar effects in an intratropical migrant, the yellow-green vireo. Animal Behavior, 67, 1141-1149.
62. Tieleman, B.I., Williams, J.B. & Ricklefs, R.E. (2004) Nest attentiveness and egg temperature do not explain the variation in incubation periods in tropical birds. Functional Ecology, 18, 571-577.
63. Wai, M.S.M., Lorke, D.E., Kung, L.S. & Yew, D.T.W. (2006) Morphogenesis of the different types of photoreceptors of the chicken (Gallus domesticus) retina and the effect of Amblyopia in neonatal chicken. Microscopy Research and Technique, 69, 99-107.
64. Walter, J.H. & Voitle, R.A. (1972) Effects of photoperiod during incubation on embryonic and post-embryonic development of broilers. Poultry Science, 51, 1122-1126.
65. Walter, J.H. & Voitle, R.A. (1973) Effects of photoperiod during incubation on embryonic and post-embryonic development of quail and chickens. British Poultry Science, 14, 533-540.
66. Wetherbee, D.K. & Wetherbee, N.S. (1961) Artificial incubation of eggs of various bird species and some attributes of neonates. Bird-Banding, 32, 141-159.
67. Wiersma, P., Muñoz-Garcia, A., Walker, A. & Williams, J.B. (2007) Tropical birds have a slow pace of life. Proceedings of the National Academy of Sciences of the United States of America, 104, 9340-9345.
68. Wikelski, M., Martin, L., Scheuerlein, A., Robinson, M., Robinson, N., Helm, B., Hau, M. & Gwinner, E.. (2008) Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 411.
69. Zeman, M., Gwinner, E., Herichova, I., Lamosová, D. & Kost'al, L. (1999) Perinatal development of circadian melatonin production in domestic chicks. Journal of Pineal Research, 26, 28-34.