Abstract
Many of the brilliant plumage coloration displays of birds function as signals to conspecifics. One species in which the function of plumage ornaments has been assessed is the Eastern bluebird (Sialia sialis). Studies of a population breeding in Alabama (USA) have established that plumage ornaments signal quality, parental investment, and competitive ability in both sexes. Here we tested the additional hypotheses that (1) Eastern bluebird plumage ornamentation signals nest defense behavior in heterospecific competitive interactions and (2) individual variation in plumage ornamentation reflects underlying differences in circulating hormone levels. We also tested the potential for plumage ornaments to signal individual quality and parental investment in a population breeding in Oklahoma (USA). We found that Eastern bluebirds with more ornamented plumage are in better condition, initiate breeding earlier in the season, produce larger clutches, have higher circulating levels of the stress hormone corticosterone, and more ornamented males have lower circulating androgen levels. Plumage coloration was not related to nest defense behavior. Thus, plumage ornamentation may be used by both sexes to assess the physiological condition and parental investment of prospective mates. Experimental manipulations of circulating hormone levels during molt are needed to define the role of hormones in plumage ornamentation.
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Almasi B, Jenni L, Jenni-Eiermann S, Roulin A (2010) Regulation of stress response is heritable and functionally linked to melanin-based coloration. J Evol Biol 23:987–996
Amundsen T (2000) Female ornaments: genetically correlated or sexually selected? In: Espmark Y, Amundsen T, Rosenquist G (eds) Animal signals: signalling and signal design in animal communication. Tapir Academic Press, Trondheim, pp 133–154
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KL (eds) Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge, pp 41–89
Badyaev AV, Hill GE (2002) Paternal care as a conditional strategy: distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch. Behav Ecol 13:591–597
Balenger SL, Johnson LS, Brubaker JL, Ostlind E (2007) Parental effort in relation to structural plumage coloration in the mountain bluebird (Sialia currucoides). Ethol 113:838–846
Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc Lond B 268:1337–1344
Budden AE, Dickinson JL (2009) Signals of quality and age: the information content of multiple plumage ornaments in male western bluebirds Sialia mexicana. J Avian Biol 40:18–27
Butler MW, Leppert LL, Dufty AM (2010) Effects of small increases in corticosterone levels on morphology, immune function, and feather development. Physiol Biochem Zool 83:78–86
DesRochers DW, Reed JM, Awerman J, Kluge JA, Wilkinson J, van Griethuijsen LI, Aman J, Romero LM (2009) Exogenous and endogenous corticosterone alter feather quality. Comp Biochem Physiol A Mol Integr Physiol 152:46–52
Duckworth RA (2006) Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression. Behav Ecol 17:1011–1019
Duckworth RA, Mendonca MT, Hill GE (2004) Condition-dependent sexual traits and social dominance in the house finch. Behav Ecol 15:779–784
Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510
Dunn PO, Whittingham LA, Freeman-Gallant CR, DeCoste J (2008) Geographic variation in the function of ornaments in the common yellowthroat Geothlypis trichas. J Avian Biol 39:66–72
Dunn PO, Garvin JC, Whittingham LA, Freeman-Gallant CR, Hasselquist D (2010) Carotenoid and melanin-based ornaments signal similar aspects of male quality in two populations of the common yellowthroat. Func Ecol 24:149–158
Evans MR, Goldsmith AR, Norris SRA (2000) The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 47:156–163
Friedman SL, Brasso RL, Condon AM (2008) An improved, simple nest-box trap. J Field Ornithol 79:99–101
Gonzalez G, Sorci G, Smith LC, de Lope F (2001) Testosterone and sexual signalling in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 50:557–562
Gowaty PA (1984) House sparrows kill eastern bluebirds. J Field Ornithol 55:378–380
Gowaty PA, Plissner J (1998) Eastern bluebird (Sialia sialis). In: Poole A, Gill F (eds) The birds of North America. Cornell Lab of Ornithology, Ithaca
Griggio M, Serra L, Licheri D, Campomori C, Pilastro A (2009) Moult speed affects structural feather ornaments in the blue tit. J Evol Biol 22:782–792
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387
Heywood JS (1989) Sexual selection by the handicap mechanism. Evolution 43:1387–1397
Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339
Hill GE (1994) Geographic variation in male ornamentation and female mate preference in the house finch—a comparative test of models of sexual selection. Behav Ecol 5:64–73
Hill GE (2006) Environmental regulation of ornamental coloration. In: Hill GE, McGraw KL (eds) Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge, pp 507–560
Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634
Hill GE, McGraw KJ (2006) Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge
Hoelzer GA (1989) The good parent process of sexual selection. Anim Behav 38:1067–1078
Husak JF, Moore IT (2008) Stress hormones and mate choice. Trends Ecol Evol 23:532–534
Jawor JM, Breitwisch R (2003) Melanin ornaments, honesty, and sexual selection. Auk 120:249–265
Jawor JM, Breitwisch R (2004) Multiple ornaments in male northern cardinals, Cardinalis cardinalis, as indicators of condition. Ethol 110:113–126
Jawor JM, Gray N, Beall SM, Breitwisch R (2004) Multiple ornaments correlate with aspects of condition and behaviour in female northern cardinals, Cardinalis cardinalis. Anim Behav 67:875–882
Johnsen A, Delhey K, Schlicht E, Peters A, Kempenaers B (2005) Male sexual attractiveness and parental effort in blue tits: a test of the differential allocation hypothesis. Anim Behav 70:877–888
Jovani R, Blas J (2004) Adaptive allocation of stress-induced deformities on bird feathers. J Evol Biol 17:294–301
Keyser AJ, Hill GE (2000) Structurally based plumage coloration is an honest signal of quality in male blue grosbeaks. Behav Ecol 11:202–209
Kimball RT (2006) Hormonal control of coloration. In: Hill GE, McGraw KL (eds) Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge, pp 431–468
Komdeur J, Oorebeek M, van Overveld T, Cuthill IC (2005) Mutual ornamentation, age, and reproductive performance in the European starling. Behav Ecol 16:805–817
Krebs EA, Hunte W, Green DJ (2004) Plume variation, breeding performance and extra-pair copulations in the cattle egret. Behaviour 141:479–499
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities—a common mistake. Auk 104:116–121
Linville SU, Breitwisch R, Schilling AJ (1998) Plumage brightness as an indicator of parental care in northern cardinals. Anim Behav 55:119–127
Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models. SAS Institute Inc, Cary
Lovern MB, Adams AL (2008) The effects of diet on plasma and yolk steroids in lizards (Anolis carolinensis). Integr Comp Biol 48:428–436
McGraw KJ, Mackillop EA, Dale J, Hauber ME (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
McGraw KJ, Wakamatsu K, Ito S, Nolan PM, Jouventin P, Dobson FS, Austic RE, Safran RJ, Siefferman LM, Hill GE, Parker R (2004) You can’t judge a pigment by its color: carotenoid and melanin content of yellow and brown feathers in swallows, bluebirds, penguins, and domestic chickens. Condor 106:390–395
Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KL (eds) Bird coloration: mechanisms and measurements. Harvard University Press, Cambridge, pp 90–147
Montgomerie R (2008) CLR, version 1.05. Queen’s University, Kingston, Canada. http://post.queensu.ca/~mont/color/analyze.html
Neuman CR, Safran RJ, Lovette IJ (2007) Male tail streamer length does not predict apparent or genetic reproductive success in North American barn swallows Hirundo rustica erythrogaster. J Avian Biol 38:28–36
Örnborg J, Andersson S, Griffith SC, Sheldon BC (2002) Seasonal changes in an ultraviolet structural colour signal in blue tits, Parus caeruleus. Biol J Linn Soc 76:237–245
Palokangas P, Korpimaki E, Hakkarainen H, Huhta E, Tolonen P, Alatalo RV (1994) Female kestrels gain reproductive success by choosing brightly ornamented males. Anim Behav 47:443–448
Peters A, Delhey K, Goymann W, Kempenaers B (2006) Age-dependent association between testosterone and crown UV coloration in male blue tits (Parus caeruleus). Behav Ecol Sociobiol 59:666–673
Peters A, Kurvers R, Roberts ML, Delhey K (2011) No evidence for general condition-dependence of structural plumage colour in blue tits: an experiment. J Evol Biol 24:976–987
Pinkowski BC (1975) Growth and development of eastern bluebirds. Bird-Banding 46:273–289
Pitts TD (1985) Identification of second-year and after-second year eastern bluebirds. J Field Ornithol 56:422–424
Quesada J, Senar JC (2007) The role of melanin- and carotenoid-based plumage coloration in nest defence in the great tit. Ethol 113:640–647
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Reyer HU, Fischer W, Steck P, Nabulon T, Kessler P (1998) Sex-specific nest defense in house sparrows (Passer domesticus) varies with badge size of males. Behav Ecol Sociobiol 42:93–99
Roberts ML, Ras E, Peters A (2009) Testosterone increases UV reflectance of sexually selected crown plumage in male blue tits. Behav Ecol 20:535–541
Robinson TJ, Siefferman LM, Risch TS (2004) A quick, inexpensive trap for use with nest boxes. N Amer Bird Bander 29:116–117
Rohde PA, Johnsen A, Lifjeld JT (1999) Female plumage coloration in the bluethroat: no evidence for an indicator of maternal quality. Condor 101:96–104
Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24
Roulin A, Riols C, Dijkstra C, Ducrest AL (2001) Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110
Roulin A, Almasi B, Rossi-Pedruzzi A, Ducrest AL, Wakamatsu K, Miksik I, Blount JD, Jenni-Eiermann S, Jenni L (2008) Corticosterone mediates the condition-dependent component of melanin-based coloration. Anim Behav 75:1351–1358
Saetre GP, Fossnes T, Slagsvold T (1995) Food provisioning in the pied flycatcher: do females gain direct benefits from choosing bright-colored males? J Anim Ecol 64:21–30
Schluter D, Price T (1993) Honesty, perception and population divergence in sexually selected traits. Proc R Soc Lond B 253:117–122
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163
Serra L, Griggio M, Licheri D, Pilastro A (2007) Moult speed constrains the expression of a carotenoid-based sexual ornament. J Evol Biol 20:2028–2034
Shawkey MD, Estes AM, Siefferman LM, Hill GE (2003) Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colours. Proc R Soc Lond B 270:1455–1460
Shawkey MD, Estes AM, Siefferman L, Hill GE (2005) The anatomical basis of sexual dichromatism in non-iridescent ultraviolet-blue structural coloration of feathers. Biol J Linn Soc 84:259–271
Shawkey MD, Pillai SR, Hill GE, Siefferman LM, Roberts SR (2007) Bacteria as an agent for change in structural plumage color: correlational and experimental evidence. Am Nat 169:S112–S121
Shizuka D, Dickinson JL (2005) Using molt limits to age western bluebirds. J Field Ornithol 76:193–196
Siefferman L, Hill GE (2003) Structural and melanin coloration indicate parental effort and reproductive success in male eastern bluebirds. Behav Ecol 14:855–861
Siefferman L, Hill GE (2005a) Evidence for sexual selection on structural plumage coloration in female eastern bluebirds (Sialia sialis). Evolution 59:1819–1828
Siefferman L, Hill GE (2005b) Male eastern bluebirds trade future ornamentation for current reproductive investment. Biol Lett 1:208–211
Siefferman L, Hill GE (2005c) UV-blue structural coloration and competition for nestboxes in male eastern bluebirds. Anim Behav 69:67–72
Siefferman L, Hill GE (2007) The effect of rearing environment on blue structural coloration of eastern bluebirds (Sialia sialis). Behav Ecol Sociobiol 61:1839–1846
Siefferman L, Hill GE, Dobson FS (2005) Ornamental plumage coloration and condition are dependent on age in eastern bluebirds Sialia sialis. J Avian Biol 36:428–435
Smiseth PT, 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
Smiseth PT, Örnborg J, Andersson S, Amundsen T (2001) Is male plumage reflectance correlated with paternal care in bluethroats? Behav Ecol 12:164–170
Stutchbury BJ, Robertson RJ (1986) A simple trap for catching birds in nest boxes. J Field Ornithol 57:64–65
Takahashi M, Arita H, Hiraiwa-Hasegawa M, Hasegawa T (2008) Peahens do not prefer peacocks with more elaborate trains. Anim Behav 75:1209–1219
Wingfield JC, Farner DS (1975) Determination of five steroids in avian plasma by radioimmunoassay and competitive protein binding. Steroids 26:311–327
Zahavi A (1975) Mate selection-a selection for a handicap. J Theor Biol 53:205–214
Acknowledgments
We would like to thank the student volunteers that assisted with fieldwork, in particular Emily Clark. We thank Robert Montgomerie for the use of his CLR5 program for analysis of feather color and Lynn Siefferman for advice on color analyses. Funding was provided by research grants from Bob and Julia Bollinger and the Payne County Audubon Society to JLB and a Niblack Research Fellowship and Oklahoma Louis Stokes Alliance for Minority Participation in Science fellowship to AHS. Support was also provided by the Department of Zoology and the College of Arts and Sciences at Oklahoma State University.
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The authors declare that they have no conflict of interest.
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Research was approved by the Oklahoma State University Institutional Animal Care and Use Committee and complies with the laws and regulations of the United States of America.
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Grindstaff, J.L., Lovern, M.B., Burtka, J.L. et al. Structural coloration signals condition, parental investment, and circulating hormone levels in Eastern bluebirds (Sialia sialis). J Comp Physiol A 198, 625–637 (2012). https://doi.org/10.1007/s00359-012-0735-0
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DOI: https://doi.org/10.1007/s00359-012-0735-0