Variation in eggshell traits between geographically distant populations of pied flycatchers Ficedula hypoleuca

Journal of Avian Biology

Volumn 44, Issue 2, 2013, Pages 111-120

  Morales, Judith ^a   Ruuskanen, Suvi ^b   Laaksonen, Toni ^b   Eeva, Tapio ^b   Mateo, Rafael ^c   Belskii, Eugen ^d   Ivankina, Elena V ^e   Järvinen, Antero ^f   Kerimov, Anvar ^e   Korpimäki, Erkki ^b   Krams, Indrikis ^g   Mänd, Raivo ^h   Morosinotto, Chiara ^b   Orell, Markku ⁱ   Qvarnström, Anna ^j   Siitari, Heli ^k   Slater, Fred M ^l   Tilgar, Vallo ^h   Visser, Marcel E ^m   Winkel, Wolfgang ⁿ   Zang, Herwig ^o   Moreno, Juan ^a   more..

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b UNIVERSITY OF TURKU   (Finland)

^c INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^d INSTITUTE OF PLANT AND ANIMAL ECOLOGY   (Russian Federation)

^e MOSCOW STATE UNIVERSITY   (Russian Federation)

^f UNIVERSITY OF HELSINKI   (Finland)

^g DAUGAVPILS UNIVERSITY   (Latvia)

^h UNIVERSITY OF TARTU   (Estonia)

ⁱ UNIVERSITY OF OULU   (Finland)

^j UPPSALA UNIVERSITY   (Sweden)

^k UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^l CARDIFF UNIVERSITY   (United Kingdom)

^m NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

ⁿ INSTITUTE OF AVIAN RESEARCH VOGELWARTE HELGOLAND   (Germany)

^o Inst of Avian Research 'Vogelwarte Helgoland' ^*

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; DEVELOPMENTAL BIOLOGY; EGGSHELL; ENVIRONMENTAL FACTOR; GAS EXCHANGE; GENE EXPRESSION; GEOGRAPHICAL REGION; HABITAT TYPE; PASSERINE; POPULATION STRUCTURE; RESOURCE ALLOCATION; SPATIAL VARIATION;

ANIMALIA; AVES; FICEDULA HYPOLEUCA;

EID: 84874525209     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.1600-048X.2012.05782.x     Document Type: Article

References (72)

1. Anderson D. W. and Hickey J. J. 1970. Oological data on egg and breeding characteristics of brown pelicans. Wilson Bull. 82: 14-28.
2. Ar A., Paganelli C. V., Reeves R. B., Greene D. G. and Rahn H. 1974. The avian egg: water vapor conductance, shell thickness, and functional pore area. Condor 76: 153-158.
3. Ar A., Rahn H. and Paganelli C. V. 1979. The avian egg: mass and strength. Condor 81: 331-337.
4. Arad Z., Gavrielilevin I. and Marder J. 1988. Adaptation of the pigeon egg to incubation in hot, dry environments. Physiol. Zool. 61: 293-300.
5. Avilés J. M., Stokke B. G., Moksnes A., Røskaft E. and Møller A. P. 2007. Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus. Behav. Ecol. Sociobiol. 61: 475-485.
6. Blondel J., Dias P. C., Maistre M. and Perret P. 1993. Habitat heterogeneity and life-history variation of mediterranean blue tits (Parus caeruleus). Auk 110: 511-520.
7. Bourgault P., Thomas D. W., Blondel J., Perret P. and Lambrechts M. M. 2007. Between-population differences in egg composition in blue tits (Cyanistes caeruleus). Can. J. Zool. 85: 71-80.
8. Cassey P., Maurer G., Duval C., Ewen J. G. and Hauber M. E. 2010. Impact of time since collection on avian eggshell color: a comparison of museum and fresh egg specimens. Behav. Ecol. Sociobiol. 64: 1711-1720.
9. Cramp S. and Perrins C. M. 1993. The birds of the Western Palearctic. Vol. VII. - Oxford Univ. Press.
10. Davies R. A. G. and Randall R. M. 1989. Historical and geographical patterns in eggshell thickness of African fish eagles Haliaeetus vocifer, in relation to pesticide use within Southern Africa. - In: Meyburg B. U. and Chancellor R. D. (eds), Raptors in the modern world. WWGBP, pp. 501-513.
11. Davis T. A. and Ackerman R. A. 1985. Adaptations of black tern (Chlidonias niger) eggs for water-loss in a moist nest. Auk 102: 640-643.
12. Davis T. A., Platter-Reiger M. F. and Ackerman R. A. 1984. Incubation water loss by pied-billed grebe eggs: adaptations to a hot, wet nest. Physiol. Zool. 57: 384-391.
13. Deeming D. C. 2002. Avian incubation: behaviour, environment, and evolution. - Oxford Univ. Press.
14. Eeva T. and Lehikoinen E. 1995. Egg-shell quality, clutch size and hatching success of the great tit (Parus major) and the pied flycatcher (Ficedula hypoleuca) in an air-pollution gradient. Oecologia 102: 312-323.
15. Eeva T. and Lehikoinen E. 2004. Rich calcium availability diminishes heavy metal toxicity in pied flycatcher. Funct. Ecol. 18: 548-553.
16. Eeva T., Lehikoinen E., Rönkä M., Lummaa V. and Currie D. 2002. Different responses to cold weather in two pied flycatcher populations. Ecography 25: 705-713.
17. Eeva T., Ruuskanen S., Salminen J.-P., Belskii E., Järvinen A., Kerimov A., Korpimäki E., Krams I., Moreno J., Morosinotto C., Mänd R., Orell M., Qvärnström A., Siitari H., Slater F. M., Tilgar V., Visser M. E., Winkel W., Zang H. and Laaksonen T. 2010. Geographical trends in the yolk carotenoid composition of the pied flycatcher (Ficedula hypoleuca). Oecologia 165: 277-287.
18. Falchuk K. H., Contin J. M., Dziedzic T. S., Feng Z. L., French T. C., Heffron G. J. and Montorzi M. 2002. A role for biliverdin IX alpha in dorsal axis development of Xenopus laevis embryos. Proc. Natl Acad. Sci. USA 99: 251-256.
19. García-Navas V., Sanz J. J., Merino S., Martínez-de la Puente J., Lobato E., del Cerro S., Rivero J., Ruiz-de Castañeda R. and Moreno J. 2011. Experimental evidence for the role of calcium in eggshell pigmentation pattern and breeding performance in blue tits Cyanistes caeruleus. J. Ornithol. 152: 71-82.
20. Gosler A. G., Higham J. P. and Reynolds S. J. 2005. Why are birds' eggs speckled? Ecol. Lett. 8: 1105-1113.
21. Graveland J., van der Wal R., van Balen J. H. and van Noordwijk A. J. 1994. Poor reproduction in forest passerines from decline of snail abundance on acidified soils. Nature 368: 446-448.
22. Hanley D. and Doucet S. M. 2012. Does environmental contamination influence egg coloration? A long-term study in herring gulls. J. Appl. Ecol. doi: 10.1111/j.1365-2664.2012.02184.x
23. Hanley D., Heiber G. and Dearborn D. C. 2008. Testing an assumption of the sexual-signalling hypothesis: does blue-green egg color reflect maternal antioxidant capacity? Condor 110: 767-771.
24. Hanley D., Doucet S. M. and Dearborn D. C. 2010. A blackmail hypothesis for the evolution of conspicuous egg coloration in birds. Auk 127: 453-459.
25. Hargitai R., Herényi M. and Török J. 2008. Eggshell colouration in relation to female condition, male attractiveness and egg quality in the collared flycatcher (Ficedula albicollis). J. Avian Biol. 39: 413-422.
26. Hargitai R., Moskát C., Bán M., Gil D., López-Rull I. and Solymos E. 2010. Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism? J. Avian Biol. 41: 177-185.
27. Hargitai R., Mateo R. and Török J. 2011. Shell thickness and pore density in relation to shell colouration, female characteristics, and environmental factors in the collared flycatcher Ficedula albicollis. J. Ornithol. 152: 579-588.
28. Hempleman S. C., Adamson T. P. and Bebout D. E. 1993. Oxygen and avian eggshell formation at high altitude. Resp. Physiol. 92: 1-12.
29. Higham J. P. and Gosler A. 2006. Speckled eggs: water-loss and incubation behaviour in the great tit Parus major. Oecologia 149: 561-570.
30. Jagannath A., Shore R. F., Walker L. A., Ferns P. N. and Gosler A. 2008. Eggshell pigmentation indicates pesticide contamination. J. Appl. Ecol. 45: 133-140.
31. Järvinen A. 1989. Geographical variation in temperature variability and predictability and their implications for the breeding strategy of the pied flycatcher Ficedula hypoleuca. Oikos 54: 331-336.
32. Järvinen A. 1996. Correlation between egg size and clutch size in the pied flycatcher Ficedula hypoleuca in cold and warm summers. Ibis 138: 620-623.
33. Järvinen A. and Väisänen R. A. 1984. Reproduction of pied flycatchers (Ficedula hypoleuca) in good and bad breeding seasons in a northern marginal area. Auk 101: 439-450.
34. Kern M. D., Cowie R. J. and Yeager M. 1992. Water loss, conductance, and structure of eggs of pied flycatchers during egg laying and incubation. Physiol. Zool. 65: 1162-1187.
35. Klein Tank A. M. G., Wijngaard J. B., Können G. P., Böhm R., Demarée G., Gocheva A., Mileta M., Pashiardis S., Hejkrlik L., Kern-Hansen C., Heino R., Bessemoulin P., Müller-Westermeier G., Tzanakou M., Szalai S., Pálsdóttir T., Fitzgerald D., Rubin S., Capaldo M., Maugeri M., Leitass A., Bukantis A., Aberfeld R., van Engelen A. F. V., Forland E., Mietus M., Coelho F., Mares C., Razuvaev V., Nieplova E., Cegnar T., Antonio López J., Dahlström B., Moberg A., Kirchhofer W., Ceylan A., Pachaliuk O., Alexander L. V. and Petrovic P. 2002. Daily dataset of 20th-century surface air temperature and precipitation series for the European Climate Assessment. Int. J. Climatol. 22: 1441-1453, data and metadata available at < http://eca.knmi.nl >.
36. Lessells C. M. and Boag P. T. 1987. Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
37. Littell R. C., Milliken G. A., Stroup W. W. and Wolfinger R. D. 2006. SAS system for mixed models, 2nd ed. - SAS Inst., Cary, NC, USA.
38. López-Rull I. and Gil D. 2009. Do female spotless starlings Sturnus unicolor adjust maternal investment according to male attractiveness? J. Avian Biol. 40: 254-262.
39. López-Rull I., Mikšík I. and Gil D. 2008. Egg pigmentation reflects female and egg quality in the spotless starling Sturnus unicolor. Behav. Ecol. Sociobiol. 62: 1877-1884.
40. Mänd R. 1996. Increased eggshell porosity in replacement clutches of the black-headed gull Larus ridibundus. Ornis Fenn. 73: 131-136.
41. Mänd R., Tilgar V. and Leivits A. 2000. Calcium, snails, and birds: a case study. Web Ecol. 1: 63-69.
42. Mänd R., Tilgar V., Lõhmus A. and Leivits A. 2005. Providing nest boxes for hole-nesting birds - does habitat matter? Biodivers. Conserv. 14: 1823-1840.
43. Massaro M. and Davis L. S. 2004. The influence of laying date and maternal age on eggshell thickness and pore density in yellow-eyed penguins. Condor 106: 496-505.
44. Mateo R., Castells G., Grenn A. J., Godoy C. and Cristòfol C. 2004. Determination of porphyrins and biliverdin in bile and excreta of birds by a single liquid chromatography-ultraviolet detection analysis. J. Chromatogr. B 810: 305-311.
45. Maurer G., Portugal S. J. and Cassey P. 2011. Review: an embryo's eye view of avian eggshell pigmentation. J. Avian Biol. 42: 494-504.
46. McDonagh A. F. 2001. Turning green to gold. Nat. Struct. Biol. 8: 198-200.
47. Morales J., Sanz J. J. and Moreno J. 2006. Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird. Biol. Lett. 2: 334-336.
48. Morales J., Velando A. and Moreno J. 2008. Pigment allocation to eggs decreases plasma antioxidants in a songbird. Behav. Ecol. Sociobiol. 63: 227-233.
49. Morales J., Kim S.-Y., Lobato E., Merino S., Tomás G., Martínez-de la Puente J. and Moreno J. 2010. On the heritability of blue-green eggshell coloration. J. Evol. Biol. 23: 1783-1791.
50. Morales J., Velando A. and Torres R. 2011. Biliverdin-based egg coloration is enhanced by carotenoid supplementation. Behav. Ecol. Sociobiol. 65: 197-203.
51. Moreno J. and Osorno J. L. 2003. Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol. Lett. 6: 803-806.
52. Moreno J., Morales J., Lobato E., Merino S., Tomás G. and Martínez-de la Puente J. 2005. Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca. Behav. Ecol. 16: 931-937.
53. Moreno J., Lobato E., Morales J., Merino S., Tomás G., Martínez-de la Puente J., Sanz J. J., Mateo R. and Soler J. J. 2006. Experimental evidence that egg color indicates female condition at laying in a songbird. Behav. Ecol. 17: 651-655.
54. Moreno J., Lobato E. and Morales J. 2011. Eggshell blue-green colouration fades immediately after oviposition: a cautionary note about the proper measurement of natural egg colours. Ornis. Fenn. 88: 51-56.
55. Mousseau T. A. and Fox C. W. 1998. Maternal effects as adaptations. - Oxford Univ. Press.
56. Ojanen M. 1983. Effects of laying sequence and ambient temperature on the composition of eggs of the great tit Parus major and the pied flycatcher Ficedula hypoleuca. Ann. Zool. Fenn. 20: 65-71.
57. Packard G. C., Sotherland P. R. and Packard M. J. 1977. Adaptive reduction in permeability of avian eggshells to water vapour at high altitudes. Nature 266: 255-256.
58. Rahn H., Paganelli C. V. and Ar A. 1987. Investment in egg size: environment- and population-specific effects on offspring performance. Oecologia 142: 546-553.
59. Räsänen K. and Kruuk L. E. B. 2007. Maternal effects and evolution at ecological time-scales. Funct. Ecol. 21: 408-421.
60. Ruuskanen S., Siitari H., Eeva T., Belskii E., Järvinen A., Kerimov A., Krams I., Moreno J., Morosinotto C., Mänd R., Möstl E., Orell M., Qvärnström A., Salminen J.-P., Slater F. M., Tilgar V., Visser M. E., Winkel W., Zang H. and Laaksonen T. 2011. Geographical variation in egg mass and egg content in a passerine bird. PLoS One 6: 1-10.
61. Ryckman D. P., Weseloh D. V., Hamr P., Fox G. A., Collins B., Ewins P. J. and Norstrom R. J. 1998. Spatial and temporal trends in organochlorine contamination and bill deformities in double-crested cormorants (Phalacrocorax auritus) from the Canadian Great Lakes. Environ. Monit. Assess. 53: 169-195.
62. Sahin N., Onderci M. and Sahin K. 2002. Effects of dietary chromium and zinc on egg production, egg quality, and some blood metabolites of laying hens reared under low ambient temperature. Biol. Trace Elem. Res. 85: 47-58.
63. Sahin N., Onderci M. and Sahin K. 2003. Vitamin E and selenium supplementation to alleviate cold-stress-associated deterioration in egg quality and egg yolk mineral concentrations of Japanese quails. Biol. Trace Elem. Res. 96: 179-189.
64. Sanz J. J. 1997. Geographical variation in breeding parameters of the pied flycatcher Ficedula hypoleuca. Ibis 139: 107-114.
65. Siefferman L., Navara K. J. and Hill G. E. 2006. Egg colouration is associated with female condition in eastern bluebirds (Sialia sialis). Behav. Ecol. Sociobiol. 59: 651-656.
66. Stein L. R. and Badyaev A. V. 2011. Evolution of eggshell structure during rapid range expansion in a passerine bird. Funct. Ecol. 25: 1215-1222.
67. Stocker R., Yorihiro Y., McDonagh A. F., Glazer A. N. and Ames B. N. 1987. Bilirubin is an antioxidant of possible physiological properties. Science 235: 1043-1046.
68. Tilgar V., Mänd R. and Leivits A. 1999a. Effect of calcium availability and habitat quality on reproduction in pied flycatcher Ficedula hypoleuca and great tit Parus major. J. Avian Biol. 30: 383-391.
69. Tilgar V., Mänd R. and Leivits A. 1999b. Breeding in calcium-poor habitats: are there any extra costs? Acta Ornithol. 34: 215-218.
70. Veen T., Sheldon B. C., Weissing F. J., Visser M. E., Qvarnström A. and Sætre G.-P. 2010. Temporal differences in food abundance promote coexistence between two congeneric passerines. Oecologia 162: 873-884.
71. Wallace A. R. 1889. Darwinism: an exposition of the theory of natural selection with some of its applications. - Macmillan.
72. Zang H. 1998. Effects of "acid rain" on a population of great tit (Parus major) in the higher regions of the Harz Mountains. J. Ornithol. 139: 263-268.