Colouration in Atlantic puffins and blacklegged kittiwakes: Monochromatism and links to body condition in both sexes

Journal of Avian Biology

Volumn 44, Issue 5, 2013, Pages 451-460

  Doutrelant, Claire ^a   Grégoire, Arnaud ^a   Gomez, Doris ^a   Staszewski, Vincent ^a   Arnoux, Emilie ^b   Tveraa, Torkild ^c   Faivre, Bruno ^b   Boulinier, Thierry ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c NORWEGIAN INSTITUTE FOR NATURE RESEARCH   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BODY CONDITION; CAROTENOID; COLOR; CRYPSIS; SEABIRD; SEXUAL DIMORPHISM; SEXUAL SELECTION; SPECTROPHOTOMETRY;

ATLANTIC OCEAN;

AVES; FRATERCULA; FRATERCULA ARCTICA; LARIDAE; LARUS; RISSA; RISSA TRIDACTYLA;

EID: 84884723069     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.1600-048X.2013.00098.x     Document Type: Article

References (104)

1. Anderson M. 1994. Sexual selection. - Princeton Univ. Press.
2. Andersson S. and Prager M. 2006. Quantifying colors. - In: Hill G. E. and McGraw K. J. (eds), Harvard Univ. Press, pp. 41-89.
3. Andersson S., Örnborg J. and Andersson M. 1998. Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc. R. Soc. B 265: 445-450.
4. Andersson S., Pryke S. R., Örnborg J., Lawes M. J. and Andersson M. 2002. Multiple receivers, multiple ornaments, and a tradeoff between agonistic and epigamic signaling in a widowbird. Am. Nat. 160: 684-691.
5. Anker-Nilssen T., Bakken V., Strøm H., Golovkin A. N., Bianki V. V. and Tatarinkova I. P. 2000. The status of marine birds breeding in the Barents sea region. - Tromsø Norsk Polar Inst.
6. Anker-Nilssen T., Kleven K., Aarvak T. and Lifjeld J. T. 2008. No evidence of extrapair paternity in the Atlantic puffin Fratercula arctica. Ibis 150: 619-622.
7. Armenta J. K., Dunn P. O. and Whittingham L. A. 2008. Quantifying avian sexual dichromatism: a comparison of methods. J. Exp. Biol. 211: 2423-2430.
8. Badyaev A. V. and Hill G. E. 2000. Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration. Biol. J. Linn. Soc. 69: 153-172.
9. Badyaev A. V. and Hill G. E. 2003. Avian sexual dichromatism in relation to phylogeny and ecology. Annu. Rev. Ecol. Evol. Syst. 34: 27-49.
10. Barrett R. T. 2001a. The breeding demography and egg size of North Norwegian Atlantic puffins Fratercula arctica and razorbills Alca torda during 20 years of climatic variability. Atl. Seabird 3: 97-112.
11. Barrett R. T. 2001b. Monitoring the Atlantic puffin Fratercula arctica, common guillemot Uria aalge and black-legged kittiwake Rissa tridactyla breeding populations on Hornøya, northeast Norway, 1980-2000. - Fauna Norv. Ser. 21: 1-10.
12. Barrett R. T., Fieler R., Anker-Nilssen T. and Rikardsen F. 1985. Measurements and weight changes of Norwegian adult puffins Fratercula arctica and kittiwakes Rissa tridactyla during breeding season. Ringing Migration 6: 102-112.
13. Bennett A. T. D. and Cuthill I. C. 1994. Ultraviolet vision in birds: what is its function? Vision Res. 11: 1471-1498.
14. Bertrand S., Alonso-Alvarez C., Devevey G., Faivre B., Prost J. and Sorci G. 2006. Carotenoids modulate the tradeoff between egg production and resistance to oxidative stress in zebra finches. Oecologia 147: 576-584.
15. Blount J. D., Surai P. F., Nager R. G., Houston D. C., Moller A. P., Trewby M. L. and Kennedy M. W. 2002. Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc. R. Soc. B 269: 29-36.
16. Blount J. D., Metcalfe N. B., Birkhead T. R. and Surai P. F. 2003. Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300: 125-127.
17. Boulet M., Crawford J. C., Charpentier M. J. E. and Drea C. M. 2010. Honest olfactory ornamentation in a female- dominant primate. J. Evol. Biol. 23: 1558-1563.
18. Boulinier T., Mccoy K. D., Yoccok N. G., Gasparini J. and Tveraa T. 2008 Public information affects breeding dispersal in a colonial bird: kittiwakes cue on neighbours. Biol. Lett. 4: 538-540.
19. Britton G., Liaaen-Jensen S. and Pfander H. 1995. Carotenoids: handbook. - Birkhäuser Verlag.
20. Campenhausen M. V. and Kirschfeld K. 1998. Spectral sensivity of the accessory optic system of the pigeon. J. Comp. Physiol. A 183: 1-6.
21. Clutton-Brock T. 2007. Sexual selection in males and females. Science 318: 1882-1885.
22. Costantini D. 2008. Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11: 1238-1251.
23. Costantini D. and Møller A. P. 2008. Carotenoids are minor antioxidants for birds. Funct. Ecol. 22: 367-370.
24. Coulson J. C. 1972. The significance of the pair-bond in the kittiwake (Rissa tridactyla). - Proc. Int. Ornithol. Congr. XV, pp. 424-433.
25. Coulson J. C. 2009. Sexing black-legged kittiwakes by measurement. Ringing Migration 24: 233-239.
26. Coulson J. C. 2011. The kittiwake. - T. and A. D. Poyser.
27. Coulson J. C. and Johnson M. 1993 The attendance and absence of adult kittiwakes Rissa tridactyla from the nest site during the chick stage. Ibis 135: 372-378.
28. Creelman E. and Storey A. E. 1991. Sex differences in reproductive behaviour of Atlantic puffins. Condor 93: 390-398.
29. De Heij M. E., Van Den Hout P. J. and Tinbergen J. M. 2006. Fitness cost of incubation in great tits (Parus major) is related to clutch size. Proc. R. Soc. B 273: 2353-2361.
30. Delhey K., Johnsen A., Peters A., Andersson S. and Kempenaers B. 2003. Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus). Proc. R. Soc. B 270: 2057-2063.
31. Doutrelant C., Gregoire A., Grnac N., Gomez D., Lambrechts M. M. and Perret P. 2008. Female coloration indicates female reproductive capacity in blue tits. J. Evol. Biol. 21: 226-233.
32. Doutrelant C., Grégoire A., Midamegbe A., Lambrechts M. M. and Perret P. 2012. Female plumage coloration is sensitive to the cost of reproduction. An experiment in blue tits. J. Anim. Ecol. 81: 87-96.
33. Eaton M. D. 2005. Human vision fails to distinguish widespread sexual dichromatism among sexually 'monochromatic' birds. Proc. Natl Acad. Sci. USA 102: 10942-10946.
34. Endler J. A. and Mielke P. W. 2005. Comparing entire colour patterns as birds see them. Biol. J. Linn. Soc. 86: 405-431.
35. Faivre B., Gregoire A., Preault M., Cezilly F. and Sorci G. 2003. Immune activation rapidly mirrored in a secondary sexual trait. Science 300: 103.
36. Fridolfsson A. K. and Ellegren H. 1999. A simple and universal method for molecular sexing of non-ratite birds. J. Avian Biol. 30: 116-121.
37. Gasparini J., Mccoy K. D., Tveraa T. and Boulinier T. 2002. Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecol. Lett. 5: 519-524.
38. Gauthier P., Barroca M., Bertrand S., Eraud C., Gaillard M., Hamman M., Motreuil S., Sorci G. and Faivre B. 2008. The presence of females modulates the expression of a carotenoid-based sexual signal. Behav. Ecol. Sociobiol. 62: 1159-1166.
39. Gomez D. 2010. AVICOL v5. a program to analyse spectrometric data. - Free program available from the author upon request at dodogomez@yahoo.fr or by download from < http://sites.google.com/site/avicolprogram/ >.
40. Gomez D. and Thery M. 2007. Simultaneous crypsis and conspicuousness in color patterns: comparative analysis of a neotropical rainforest bird community. Am. Nat. 169: S42-S61.
41. Grafen A. 1990. Biological signals as handicaps. J. Theor. Biol. 144: 517-546.
42. Griffith S. C., Ornborg J., Russell A. F., Andersson S. and Sheldon B. C. 2003. Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit. J. Evol. Biol. 16: 1045-1054.
43. Hanssen S. A., Hasselquist D., Folstad I. and Erikstad K. E. 2005. Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proc. R. Soc. B 272: 1039-1046.
44. Harris M. P. and Wanless S. 2011. The puffin. - Poyser.
45. Hart N. S. 2001. The visual ecology of avian photoreceptors. Progr. Retina Eye Res. 20: 675-703.
46. Hartley R. C. and Kennedy M. W. 2004. Are carotenoids a red herring in sexual display? Trends Ecol. Evol. 19: 353-354.
47. Håstad O. and Ödeen A. 2008. Different ranking of avian colors predicted by modeling of retinal function in humans and birds. Am. Nat. 171: 831-838.
48. Håstad O., Victorsson J. and Ödeen A. 2005. Differences in color vision make passerines less conspicuous in the eyes of their predators. Proc. Natl Acad. Sci. USA 102: 6391-6394.
49. Hatch S. A., Roberts B. D. and Fadely B. S. 1993. Adult survival of blacklegged kittiwakes Rissa tridactyla in a Pacific colony. Ibis 135: 247-254.
50. Helfenstein F., Tirard C., Danchin E. and Wagner R. H. 2004. Low frequency of extra-pair paternity and high frequency of adoption in black-legged kittiwakes. Condor 106: 149-155.
51. Hill G. E. and Mcgraw K. J. 2006. Bird coloration. Function and evolution. - Harvard Univ. Press.
52. Hill G. E., Hood W. R. and Huggins K. 2009. A multifactorial test of the effects of carotenoid access, food intake and para site load on the production of ornamental feathers and bill coloration in American goldfinches. J. Exp. Biol. 212: 1225-1233.
53. Huchard E., Raymond M., Benavides J., Marshall H., Knapp L. A. and Cowlishaw G. 2010. A female signal reflects MHC genotype in a social primate. BMC Evol. Biol. 10: 96.
54. Isaksson C. and Andersson S. 2007. Carotenoid diet and nestling provisioning in urban and rural great tits Parus major. J. Avian Biol. 38: 564-57.
55. Iwasa Y. and Pomiankowski A. 1994. The evolution of mate preferences for multiple sexual ornaments. Evolution 48: 853-867.
56. Iwasa Y. and Pomiankowski A. 1999. Good parent and good genes models of handicap evolution. J. Theor. Biol. 200: 97-109.
57. Jodice P. G. R., Lanctot R. B., Gill V. A., Roby D. D. and Hatch S. A. 2000. Sexing adult black-legged kittiwakes by DNA, behavior, and morphology. Waterbirds 23: 405-415.
58. Jones I. L. and Hunter F. M. 1993. Mutual sexual selection in a monogamous seabird. Nature 362: 238-239.
59. Korsten P., Lessells C. M., Mateman A. C., Van Der Velde M. and Komdeur J. 2006. Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits. Behav. Ecol. 17: 539-546.
60. Kraaijeveld K., Kraaijeveld-Smit F. J. L. and Komdeur J. 2007. The evolution of mutual ornamentation. Anim. Behav. 74: 657-677.
61. Kristiansen K. O., Bustnes J. O., Folstad I. and Helberg M. 2006. Carotenoid coloration in great black-backed gull Larus marinus reflects individual quality. J. Avian Biol. 37: 6-12.
62. Lande R. 1980. Sexual dimorphism, sexual selection, and adap tation in polygenic characters. Evolution 34: 292-305.
63. Lebas N. R. 2006. Female finery is not for males. Trends Ecol. Evol. 21: 170-173.
64. Leclaire S., White J., Arnoux E., Faivre B., Vetter N., Hatch S. A. and Danchin E. 2011. Integument coloration signals reproductive success, heterozygosity, and antioxidant levels in chick-rearing black-legged kittiwakes. Naturwissenschaften 98: 773-782.
65. Lessells C. M. and Boag P. T. 1987. Unrepeatable repeatabilities - a common mistake. Auk 104: 116-121.
66. Lozano G. A. 1994. Carotenoids, parasites and sexual selection. Oikos 70: 309-311.
67. Massaro M., Davis L. S. and Darby J. T. 2003. Carotenoid- derived ornaments reflect parental quality in male and female yellow-eyed penguins (Megadyptes antipodes). Behav. Ecol. Sociobiol. 55: 169-175.
68. Mcgraw K. J. and Ardia D. R. 2003. Carotenoids, immuno competence and the information content of sexual colors: an experimental test. Am. Nat. 162: 704-712.
69. Mcgraw K. J., Mackillop E. A., Dale J. and Hauber M. E. 2002. Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. J. Exp. Biol. 205: 3747-3755.
70. Mcgraw K. J., Hudon J., Hill G. E. and Parker R. S. 2005a. A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behav. Ecol. Sociobiol. 57: 391-397.
71. Mcgraw K. J., Safran R. J. and Wakamatsu K. 2005b. How feather colour reflects its melanin content. Funct. Ecol. 19: 816-821.
72. Mennill D. J., Ramsay S. M., Boag P. T. and Ratcliffe L. M. 2004. Patterns of extrapair mating in relation to male dominance status and female nest placement in black-capped chickadees. Behav. Ecol. 15: 757-765.
73. Midamegbe A., Gregoire A., Perret P. and Doutrelant C. 2011. Female-female aggressiveness is influenced by female oloration in blue tits. Anim. Behav. 82: 245-253.
74. Midamegbe A., Grégoire A., Lambrechts M. M., Perret P., Boulinier T., Staszewski V. and Doutrelant C. 2013. Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge. Oecologia in press.
75. Møller A. P., Biard C., Blount J. D., Houston D. C., Ninni P., Saino N. and Surai P. F. 2000. Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult. Biol. Rev. 11: 137-159.
76. Montgomerie R. 2006. Analyzing colors. - In: Hill G. E. and McGraw K. J. (eds), Bird colors: mechanisms and measurements. Harvard Univ. Press, pp. 90-147.
77. Morales J., Velando A. and Moreno J. 2008. Pigment allocation to eggs decreases plasma antioxidants in a songbird. Behav. Ecol. Sociobiol. 63: 227-233.
78. Morrow E. H. and Pitcher T. E. 2003. Sexual selection and the risk of extinction in birds. Proc. R. Soc. B 270: 1793-1799.
79. Navarro C., Perez-Contreras T., Aviles J. M., Mcgraw K. J. and Soler J. J. 2010. Beak colour reflects circulating carotenoid and vitamin A levels in spotless starlings (Sturnus unicolor). Behav. Ecol. Sociobiol. 64: 1057-1067.
80. Naves L. C., Monnat J. Y. and Cam E. 2006. Breeding performance, mate fidelity and nest-site fidelity in a long-lived seabird: behaving against the current? Oikos 115: 263-276.
81. Nolan P. M., Dobson F. S., Nicolaus M., Karels T. J., Mcgraw K. J. and Jouventin P. 2010. Mutual mate choice for colorful traits in king penguins. Ethology 116: 635-644.
82. Ödeen A. and Håstad O. 2003. Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol. Biol. Evol. 20: 855-861.
83. Ödeen A., Håstad O. and Alström P. 2010. Evolution of ultraviolet vision in shorebirds (Charadriiformes). Biol. Lett. 6: 370-374.
84. Olson V. A. and Owens I. P. F. 1998. Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol. Evol. 13: 510-514.
85. Olsson M., Wilson M., Isaksson C., Uller T. and Mott B. 2008. Carotenoid intake does not mediate a relationship between reactive oxygen species and bright colouration: experimental test in a lizard. J. Exp. Biol. 211: 1257-1261.
86. Ord T. J. and Stuart-Fox D. 2006. Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change. J. Evol. Biol. 19: 797-808.
87. Osorio D., Vorobyev M. and Jones C. D. 1999. Colour vision of domestic chicks. J. Exp. Biol. 202: 2951-2959.
88. Owens I. P. F. 2006. Ecological explanations for interspecific variability in coloration. - In: Hill G. E. and McGraw K. J. (eds), Bird coloration. Harvard Univ. Press, pp. 380-416.
89. Roulin A., Jungi T. W., Pfister H. and Dijkstra C. 2000. Female barn owls (Tyto alba) advertise good genes. Proc. R. Soc. B 267: 937-941.
90. Roulin A., Riols C., Dijkstra C. and Ducrest A. L. 2001. Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav. Ecol. 12: 103-110.
91. Rubenstein D. R. and Lovette I. J. 2009. Reproductive skew and selection on female ornamentation in social species. Nature 462: 786-789.
92. Seddon N., Tobias J. A., Eaton M. and Ödeen A. 2010. Human vision can provide a valid proxy for avian perception of sexual dichromatism. Auk 127: 283-292.
93. Sheldon B. C., Andersson S., Griffith S. C., Ornborg J. and Sendecka J. 1999. Ultraviolet colour variation influences blue tit sex ratios. Nature 402: 874-877.
94. Siefferman L. and Hill G. E. 2005. Evidence for sexual selection on structural plumage coloration in female eastern bluebirds (Sialia sialis). Evolution 59: 1819-1828.
95. Smiseth P. T. and Amundsen T. 2000. Does female plumage coloration signal parental quality? A male removal experiment with the bluethroat (Luscinia s. svecica). Behav. Ecol. Sociobiol. 47: 205-212.
96. Svensson P. A. and Wong B. B. M. 2011. Carotenoid-based signals in behavioural ecology: a review. Behaviour 148: 131-189.
97. Torres R. and Velando A. 2005. Male preference for female foot colour in the socially monogamous blue-footed booby, Sula nebouxii. Anim. Behav. 69: 59-65.
98. Van Noordwijk A. J. and de Jong G. 1986 Acquisition and allocation of resources - their influence on variation in life-history tactics. Am Nat 128: 137-142.
99. Velando A., Beamonte-Barrientos R. and Torres R. 2006. Pigment-based skin colour in the blue-footed booby: an honest signal of current condition used by females to adjust repro ductive investment. Oecologia 149: 535-542.
100. Vinkler M. and Albrecht T. 2010. Carotenoid maintenance handicap and the physiology of carotenoid-based signalisation of health. Naturwissenschaften 97: 19-28.
101. Visser M. E. and Lessells C. M. 2001. The costs of egg production and incubation in great tits (Parus major). Proc. R. Soc. B 268: 1271-1277.
102. Von Schantz T., Bensch S., Grahn M., Hasselquist D. and Wittzell H. 1999. Good genes, oxitative stress and condition-dependent sexual signals. Proc. R. Soc. B 266: 1-12.
103. Vorobyev M. 2003 Coloured oil droplets enhance colour discrimination. Proc. R. Soc. B 270: 1255-1261.
104. Zahavi A. 1975. Mate selection - a selection for a handicap. J. Theor. Biol 53: 205-214.