Abstract
The simultaneous exhibition of more than one secondary sexual trait is a widespread phenomenon in nature, though it has rarely been explored. It has been proposed that different ornaments may convey complementary or back-up information about a single aspect of individual quality (redundancy hypothesis) or that each ornament may convey unique information (multiple-messages hypothesis). During a 5-year period, we measured several carotenoid-based (eye ring, bill cere and tarsi skin) and melanin-based (head, back, rump and tail feathers) potential ornamental colours in male common kestrels. We analysed whether multiple ornaments can convey different or related information about individual quality. We explored whether different ornaments can express different information depending on the pigment (carotenoids or melanins), the time-scale over which the ornament can change (dynamic vs. static) and the season of the year when the ornament is formed. We found that both melanin- and carotenoid- based traits correlated with indexes of quality, including body condition, body condition of their partners and laying date. However, not all ornaments correlated with the same measures of quality. In addition, some ornaments were intercorrelated within the same individuals while others were not. These results suggest that different ornaments can convey information about different qualities, as predicted by the multiple-messages hypothesis. In addition, this study suggests that the predominant pigment (e.g. carotenoid vs. melanin, eumelanin vs. pheomelanin), the time-scale over which the trait is developed (static feathers vs. dynamic skin) and the season of the year at which the ornament is produced can be potential mechanisms to convey different messages in male common kestrels.
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References
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Andersson S, Pryke SR, Örnburg J, Lawes MJ, Andersson M (2002) Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. Am Nat 160:683–691
Aparicio JM (1994) The seasonal decline in clutch size: an experiment with supplementary food in the kestrel, Falco tinnunculus. Oikos 71:451–458
Badyaev AV, Hill GE (2000) Evolution of sexual dichormatism: contribution of carotenoid- versus melanin-based colouration. Biol J Linn Soc 69:153–172
Blums P, Nichols JD, Hines JE, Ms L, Mednis A (2005) Individual quality, survival variation and patterns of phenotypic selection on body condition and timing of nesting in birds. Oecologia 143:365–376
Bókony V, Lendvai AZ, Liker A (2006) Multiple cues in status signalling: the role of wingbars in aggressive interactions of male house sparrows. Ethology 112:947–954
Bortolotti GR (2006) Natural selection and coloration: protection, concealment, advertisement, or deception? In: Hill GE, McGraw KJ (eds) Bird coloration, vol.2: function and evolution. Harvard University Press, Cambridge, MA, pp 3–35
Bro-Jørgensen J (2010) Dynamics of multiple signalling systems: an animal communication in a world in flux. Trends Ecol Evol 25:292–300
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595
Candolin U (2005) Why do multiple traits determine mating success? Differential use in female choice and male competition in a water boatman. Proc R Soc Lond B 272:47–52
Casagrande S, Csermely D, Pini E, Bertacche V, Tagliavini J (2006) Skin carotenoid concentration correlates with male hunting skill and territory quality in the kestrel (Falco tinnunculus). J Avian Biol 37:190–196
Casagrande S, Costantini D, Fanfani A, Tagliavini J, Dell’Omo G (2007) Patterns of plasma carotenoid accumulation and skin colour variation in nestling kestrels in relation to breeding conditions and different terms of carotenoid supplementation. J Comp Physiol B 177:237–245
Casagrande S, Costantini D, Tagliavini J, Dell’Omo G (2009) Phenotypic, genetic, and environmental causes of variation in yellow skin pigmentation and serum carotenoids in Eurasian kestrel nestlings. Ecol Res 24:273–279
Chaine AS, Lyon BE (2008a) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462
Chaine AS, Lyon BE (2008b) Intrasexual selection on multiple plumage ornaments in the lark bunting. Anim Behav 76:657–667
Daan S, Dijkstra C, Tinbergen JM (1990) Family planning in the kestrel, Falco tinnunculus: variations in optimal laying date and clutch size with food supply. Behaviour 114:83–116
Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London
De Neve L, Fargallo JA, Vergara P, Lemus JA, Jarén-Galán M, Luaces I (2008) Effects of maternal carotenoid availability in relation to sex, parasite infection and health status of nestling kestrels Falco tinnunculus. J Exp Biol 211:1257–1261
Dunn PO, Garvin JC, Whittinghanm 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. Funct Ecol 24:149–158
Fargallo JA, Laaksonen T, Korpimäki E, Wakamatsu K (2007a) A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol Ecol 21:157–171
Fargallo JA, Martínez-Padilla J, Toledano-Díaz A, Santiago-Moreno J, Davila JA (2007b) Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels. J Anim Ecol 76:201–209
Fargallo JA, Martínez-Padilla J, Viñuela J, Blanco G, Torre I, Vergara P, De Neve L (2009) Kestrel-prey dynamic in a Mediterranean region: the effect of generalist predation and climatic factors. PlosOne 4:e4311
Galvan I, Solano F (2009) The evolution of eu- and pheomelanic traits may respond to an economy of pigments related to environmental oxidative stress. Pig Cell Mel Res 22:339–342
Griffith SC, Parker TH, Olson VA (2006) Melanin- versus carotenoid-based sexual signals: is the difference really so black and red? Anim Behav 71:749–763
Haase E, Ito S, Sell A, Wakamatsu K (1992) Melanin concentrations in feathers from wild and domestic pigeons. J Hered 83:64–67
Hill GE (2006a) Environmental regulation of ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, vol I. Harvard University Press, Cambridge, pp 507–560
Hill GE (2006b) Female mate choice for ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, vol II. Harvard University Press, Cambridge, pp 137–200
James FC, McCulloch CE (1990) Multivariate analysis in ecology and systematic: panacea or Pandora’s box? Annu Rev Ecol Syst 21:129–166
Karubian J, Swaddle JP, Varian-Ramos CW, Webster MS (2009) The relative importance of male tail length and nuptial plumage on social dominance and mate choice in the red-backed fairy-wren Malurus melanocephalus: evidence for the multiple receiver hypothesis. J Avian Biol 40:559–568
Korpimäki E, Wiehn J (1998) Clutch size of kestrels: seasonal decline and experimental evidence for food limitation under fluctuating food conditions. Oikos 83:259–272
Lessells CM, Boag PT (1987) Unrepeatable repeatabilites: a common mistake. Auk 104:116–121
Martínez-Padilla J, Mougeot F, Pérez-Rodríguez L, Bortolotti GR (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. Biol Lett 3:161–164
McGraw KJ (2006a) Mechanics of melanin-based coloration. In: Hill GE, Hill KJ (eds) Bird coloration, Vol. I. Harvard University Press, Cambridge, pp 243–294
McGraw KJ (2006b) Mechanics of carotenoid-based coloration. In: Hill GE, Hill KJ (eds) Bird coloration, vol. I. Harvard University Press, Cambridge, pp 177–242
McGraw KJ (2008) An update on the honesty of melanin-based color signal in birds. Pig Cell Mel Res 21:133–138
Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176
Mougeot F, Pérez-Rodríguez L, Sumozas N, Terraube J (2009) Parasites, condition, cellular immunity and carotenoid based ornamentation in male red-legged partridge Alectoris rufa. J Avian Biol 40:67–74
Mougeot F, Martínez-Padilla J, Bortolotti GR, Webster LMI, Piertney SB (2010) Physiological stress links parasites to carotenoid-based colour signals. J Evol Biol 23:643–650
Nakawaba S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045
Palokangas P, Korpimäki 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
Pannkuk EL, Siefferman LM, Butts JA (2010) Colour phases of the eastern screech owl: a comparison of biochemical variables of body contour feathers. Funct Ecol 24:347–353
Parejo D, Silva N (2009) Methionine supplementation influences melanin-based plumage colouration in Eurasian kestrel, Falco tinnunculus, nestlings. J Exp Biol 212:3576–3582
Pérez-Rodríguez L (2008) Carotenoid-based ornamentation as a dynamic but consistent individual trait. Behav Ecol Sociobiol 62:995–1005
Pérez-Rodríguez L (2009) Carotenoids in evolutionary ecology: re-evaluating the antioxidant role. BioEssays 31:1116–1126
Pérez-Rodríguez L, Viñuela J (2008) Carotenoid-based bill and eye ring coloration as honest signals of condition: an experimental test in the red-legged partridge (Alectoris rufa). Naturwissenschaften 95:821–830
Roulin A (2009a) Covariation between eumelanic pigmentation and body mass only under specific conditions. Naturwissenschaften 96:375–382
Roulin A (2009b) Melanin-based coloration covaries with ovary size in an age-specific manner in the barn owl. Naturwissenschaften 96:1177–1184
Roulin A, Gasparini J, Bize P, Ritschard M, Richner H (2008a) Melanin-based colorations signal strategies to cope with poor and rich environments. Behav Ecol Sociobiol 62:507–519
Roulin A, Almasi B, Pedruzzi AR, Ducrest A-L, Wakamatsu K, Miksik I, Blount J, Jenni-Eiermann S, Jenni L (2008b) Corticosterone mediates the condition-dependent of melanin-based coloration. Anim Behav 75:1351–1358
Senar JC, Camerino M, Copete JL, Metcalfe NB (1993) Variation in black bib of the Eurasian siskin (Carduelis spinus) and its role as a reliable badge of dominance. Auk 110:924–927
Senar JC, Copete JL, Martin AJ (1998) Behavioral and morphological correlates in the extent of postjuvenil moult in the Siskin Carduelis spinus. Ibis 140:661–669
Senar JC, Figuerola J, Domènech J (2003) Plumage coloration and nutritional condition in the great tit Parus major: the roles of carotenoids and melanins differ. Naturwissenschaften 90:234–237
Sirkiä PM, Laaksonen T (2009) Distinguishing between male and territory quality: females choose multiple traits in the pied flycatcher. Anim Behav 78:1051–1060
van Dongen WFD, Mulder RA (2008) Male and female golden whistlers respond differently to static and dynamic signals of male intruders. Behav Ecol 19:1025–1033
Vergara P, Fargallo JA (2007) Delayed plumage maturation in Eurasian kestrels: female mimicry, subordination signalling or both? Anim Behav 74:1505–1513
Vergara P, Fargallo JA (2008) Sex, melanic colouration and sibling competition during the post-fledging dependence period. Behav Ecol 19:847–853
Vergara P, De Neve L, Fargallo JA (2007) Agonistic behaviour prior to laying predicts clutch size in Eurasian kestrels: an experiment with natural decoys. Anim Behav 74:1515–1523
Vergara P, Fargallo JA, Martínez-Padilla J, Lemus JA (2009) Inter-annual variation and information content of melanin-based colouration in female Eurasian kestrels. Biol J Linn Soc 97:781–790
Vergara P, Fargallo JA, Martínez-Padilla J (2010) Reaching independence: food supply, parent quality, and offspring phenotypic characters in kestrels. Behav Ecol 21:507–512
Verhulst S, Nilsson J-Å (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc B 363:399–410
Village A (1990) The kestrel. T. and A.D, Poyser, London
Zampiga E, Gaibani G, Csermely D (2008a) Ultraviolet reflectance and female mating preferences in the common kestrel (Falco tinnunculus). Can J Zool 86:479–483
Zampiga E, Gaibani G, Csermely D (2008b) Sexual dimorphic colours and female choice in the common kestrel. Ital J Zool 75:155–159
Acknowledgments
We thank the Finat family and Juan San Teodoro for their collaboration in our studies. J. Martínez-Padilla, L. De Neve, I. López-Rull, M.C. López Agúndez and J. Navarro helped in the field. L. Pérez-Rodríguez, A. Roulin and three anonymous referees provided valuable comments. L. Pérez-Rodríguez helped with colour measurements. J. Haines revised the English. P. Vergara was supported by a postdoctoral contract from Ministerio de Educación y Ciencia, We held all the necessary licences for catching kestrels. This study was financed by the Ministerio de Educación y Ciencia of Spain (Project: CGL2004-04479/BOS).
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Vergara, P., Fargallo, J.A. Multiple coloured ornaments in male common kestrels: different mechanisms to convey quality. Naturwissenschaften 98, 289–298 (2011). https://doi.org/10.1007/s00114-011-0767-2
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DOI: https://doi.org/10.1007/s00114-011-0767-2