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Ultraviolet reflectance influences female preference for colourful males in the European serin

Abstract

Avian plumage colouration is one of the most impressive displays in nature and is frequently used as sexual signal. There is now considerable evidence that females consistently prefer males with the most elaborated colour displays. Bird colour vision expands into the ultraviolet (UV) range, which prompted several studies to test the importance of UV in mate choice, revealing that females are affected by the UV light component. These studies were mostly performed on structural plumage, whereas carotenoid-based plumage was rarely considered, although it also has a typical reflection peak in the UV. Our study tested the female choice over male yellow colouration, and whether it is influenced by UV removal, in the European serin (Serinus serinus), a sexually dichromatic cardueline finch, with males showing a conspicuous carotenoid-based yellow plumage. We shows that females preferred yellower males and that male attractiveness was lost when the UV colouration was blocked, with either of the UV-blocking techniques used. The results of our study indicate that the UV component of carotenoid colouration is important in the female mate assessment in serins and highlights the importance of considering colour perception in avian mate choice.

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References

  • Amundsen T, Forsgren E, Hansen LTT (1997) On the function of female ornaments: male bluethroats prefer colourful females. Proc R Soc Lond B 264:1579–1586

    Article  Google Scholar 

  • Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Andersson S, Amundsen T (1997) Ultraviolet colour vision and ornamentation in bluethroats. Proc R Soc Lond B 264:1587–1591

    Article  Google Scholar 

  • Ballentine B, Hill GE (2003) Female mate choice in relation to structural plumage coloration in blue grosbeaks. Condor 105:593–598

    Article  Google Scholar 

  • Barta A, Horvath G (2004) Why is it advantageous for animals to detect celestial polarization in the ultraviolet? Skylight polarization under clouds and canopies is strongest in the UV. J Theor Biol 226:429–437

    Article  PubMed  Google Scholar 

  • Behnke JM, McGregor PK, Shepherd M, Wiles R, Barnard C, Gilbert FS, Hurst JL (1995) Identity, prevalence and intensity of infestation with wing feather mites on birds (Passeriformes) from the Setubal Peninsula of Portugal. Exp Appl Acarol 19:443–458

    Google Scholar 

  • Bennett ATD, Cuthill IC, Partridge JC, Maier EJ (1996) Ultraviolet vision and mate choice in zebra finches. Nature 380:433–435

    Article  CAS  Google Scholar 

  • Bennett ATD, Cuthill IC, Partridge JC, Lunau K (1997) Ultraviolet plumage colors predict mate preferences in starlings. Proc Natl Acad Sci U S A 94:8618–8621

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brawner WR, Hill GE, Sundermann CA (2000) Effects of coccidial and mycoplasmal infection on carotenoid-based plumage pigmentation in male house finches. Auk 177:952–963

    Article  Google Scholar 

  • Bruzzone OA, Corley JC (2011) Which is the best experimental design in animal choice tests? Anim Behav 82:161–169

    Article  Google Scholar 

  • Burley NT, Enstrom DA, Chitwood L (1994) Extra-pair relations in zebra finches: differential male success results from female tactics. Anim Behav 48:1031–1041

    Article  Google Scholar 

  • Butler M, Toomey M, McGraw K (2011) How many color metrics do we need? Evaluating how different color-scoring procedures explain carotenoid pigment content in avian bare-part and plumage ornaments. Behav Ecol Sociobiol 65:401–413

    Article  Google Scholar 

  • Cardoso GC, Mota PG (2008) Speciational evolution of coloration in the genus Carduelis. Evolution 62:753–762

    Article  PubMed  Google Scholar 

  • Church SC, Bennett ATD, Cuthill IC, Partridge JC (1998) Ultraviolet cues affect the foraging behaviour of blue tits. Proc R Soc Lond B 265:1509–1514

    Article  Google Scholar 

  • Cuthill IC, Partridge JC, Bennett ATD (2000a) Avian UV vision and sexual selection. In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals: signalling and signal design in animal communication. Tapir Academic, Trondheim, pp 61–82

    Google Scholar 

  • Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000b) Ultraviolet vision in birds. Adv Study Behav 29:159–214

    Google Scholar 

  • Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London

    Google Scholar 

  • Delhey K, Peters A (2008) Quantifying variability of avian colours: are signalling traits more variable? PLoS ONE 3:e1689

    Article  PubMed Central  PubMed  Google Scholar 

  • Delhey K, Peters A, Biedermann P, Kempenaers B (2008) Optical properties of the uropygial gland secretion: no evidence for UV cosmetics in birds. Naturwissenschaften 95:939–946

    Article  CAS  PubMed  Google Scholar 

  • Doucet SM, Mennill DJ, Montgomerie R, Boag PT, Ratcliffe LM (2005) Achromatic plumage reflectance predicts reproductive success in male black-capped chickadees. Behav Ecol 16:218–222

    Article  Google Scholar 

  • Figuerola J, Senar CJ (2007) Serins with intermediate brightness have a higher survival in the wild. Oikos 116:636–641

    Article  Google Scholar 

  • Freeman-Gallant CR, Taff CC, Morin DF, Dunn PO, Whittingham LA, Tsang SM (2010) Sexual selection, multiple male ornaments, and age- and condition-dependent signaling in the common yellowthroat. Evolution 64:1007–1017

    Article  PubMed  Google Scholar 

  • García-Navas V, Ferrer ES, Sanz JJ (2012) Plumage yellowness predicts foraging ability in the blue tit Cyanistes caeruleus. Biol J Linn Soc 106:418–429

    Article  Google Scholar 

  • Griggio M, Devigili A, Hoi H, Pilastro A (2009) Female ornamentation and directional male mate preference in the rock sparrow. Behav Ecol 20:1072–1078

    Article  Google Scholar 

  • Griggio M, Hoi H, Pilastro A (2010a) Plumage maintenance affects ultraviolet colour and female preference in the budgerigar. Behav Process 84:739–744

    Article  Google Scholar 

  • Griggio M, Zanollo V, Hoi H (2010b) UV plumage color is an honest signal of quality in male budgerigars. Ecol Res 25:77–82

    Article  Google Scholar 

  • Hausmann F, Arnold KE, Marshall NJ, Owens IPF (2003) Ultraviolet signals in birds are special. Proc R Soc Lond B 270:61–67

    Article  Google Scholar 

  • Heindl M, Winkler H (2003) Female canaries (Serinus canaria) associate more with males that contrast strongly against the background. Ethology 109:259–271

    Article  Google Scholar 

  • Hill GE (1999) Mate choice, male quality, and carotenoid-based plumage coloration. In: Adams N, Slotow R (eds) Proceedings of the 22nd international ornithological congress. BirdLife South Africa, Durban, pp 1654–1668

    Google Scholar 

  • Hill GE (2000) Energic constrains on expression of carotenoid-based plumage coloration. J Avian Biol 31:559–566

    Article  Google Scholar 

  • Hill GE (2006) Female mate choice for ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration: function and evolution, vol II. Harvard University Press, Cambridge, pp 137–200

    Google Scholar 

  • Hill GE, McGraw KJ (eds) (2006) Bird coloration: mechanisms and measurements, vol I. Harvard University Press, Cambridge

    Google Scholar 

  • Hill GE, Montgomerie R (1994) Plumage colour signals nutritional condition in the house finch. Proc R Soc Lond B 258:47–52

    Article  Google Scholar 

  • Hunt S, Cuthill IC, Swaddle JP, Bennett ATD (1997) Ultraviolet vision and band-colour preferences in female zebra finches, Taeniopygia guttata. Anim Behav 54:1383–1392

    Article  PubMed  Google Scholar 

  • Hunt S, Cuthill IC, Bennett ATD, Griffiths R (1999) Preferences for ultraviolet partners in the blue tit. Anim Behav 58:809–815

    Article  PubMed  Google Scholar 

  • Hunt S, Cuthill IC, Bennett ATD, Church SC, Partridge JC (2001) Is the ultraviolet waveband a special communication channel in avian mate choice? J Exp Biol 204:2499–2507

    CAS  PubMed  Google Scholar 

  • Jacot A, Romero-Diaz C, Tschirren B, Richner H, Fitze P (2010) Dissecting carotenoid from structural components of carotenoid-based coloration: a field experiment with great tits (Parus major). Am Nat 176:55–62

    Article  PubMed  Google Scholar 

  • Johnsen A, Andersson S, Örnborg J, Lifjeld JT (1998) Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment. Proc R Soc Lond B 265:1313–1318

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Keyser AJ, Hill GE (1999) Condition-dependent variation in the blue-ultraviolet coloration of a structurally based plumage ornament. Proc R Soc Lond B 266:771–777

    Article  Google Scholar 

  • Korsten P, Limbourg T, Lessells KM, Komdeur J (2007) Effectiveness of a commonly-used technique for experimentally reducing plumage UV reflectance. J Avian Biol 38:399–403

    Google Scholar 

  • Kurvers RHJM, Delhey K, Roberts ML, Peters A (2010) No consistent female preference for higher crown UV reflectance in blue tits Cyanistes caeruleus: a mate choice experiment. Ibis 152:393–396

    Article  Google Scholar 

  • Limbourg T, Mateman A, Andersson S, Lessells C (2004) Female blue tits adjust parental effort to manipulated male UV attractiveness. Proc R Soc Lond B 271:1903–1911

    Article  Google Scholar 

  • Liu M, Siefferman L, Hill GE (2007) An experimental test of female choice relative to male structural coloration in eastern bluebirds. Behav Ecol Sociobiol 61:623–630

    Article  Google Scholar 

  • Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311

    Article  Google Scholar 

  • Maddocks SA, Bennett ATD, Hunt S, Cuthill IC (2001) Context-dependent visual preferences in starlings and blue tits: mate choice and light environment. Anim Behav 63:69–75

    Article  Google Scholar 

  • Maier EJ (1993) To deal with the invisible: on the biological significance of ultraviolet sensitivity in birds. Naturwissenschaften 80:476–478

    Article  Google Scholar 

  • McGraw KJ (2006) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration: function and evolution, vol II. Harvard University Press, Cambridge, pp 177–242

    Google Scholar 

  • McGraw KJ, Hill GE, Parker RS (2005) The physiological costs of being colourful: nutritional control of carotenoid utilization in the American goldfinch, Carduelis tristis. Anim Behav 69:653–660

    Article  Google Scholar 

  • Montgomerie R (2006) Analyzing colors. In: Hill GE, Mcgraw KJ (eds) Birds coloration: mechanisms and measurements, vol I. Harvard University Press, Cambridge, pp 41–89

    Google Scholar 

  • Mougeot F, Martínez-Padilla J, Pérez-Rodríguez L, Bortolotti G (2007) Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse. Behav Ecol Sociobiol 61:741–751

    Article  Google Scholar 

  • Nolan PM, Hill GE (2004) Female choice for song characteristics in the house finch. Anim Behav 67:403–410

    Article  Google Scholar 

  • Nolan PM, Stephen Dobson F, Nicolaus M, Karels TJ, McGraw KJ, Jouventin P (2010) Mutual mate choice for colorful traits in king penguins. Ethology 116:635–644

    Google Scholar 

  • Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  CAS  PubMed  Google Scholar 

  • Pagani-Núñez E, Senar JC (2012) Changes in carotenoid-based plumage colour in relation to age in European serins Serinus serinus. Ibis 154:155–160

    Article  Google Scholar 

  • Pérez-Rodríguez L, Mougeot F, Bortolotti G (2011) The effects of preen oils and soiling on the UV–visible reflectance of carotenoid-pigmented feathers. Behav Ecol Sociobiol 65:1425–1435

    Article  Google Scholar 

  • Peters A, Denk AG, Delhey K, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. Evol Biol 17:1111–1120

    CAS  Google Scholar 

  • Pohl H (1992) Ultraviolet radiation: a zeitgeber for the circadian clock in birds. Naturwissenschaften 79:227–229

    Article  Google Scholar 

  • Pryke SR, Andersson S, Lawes MJ (2001) Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display. Evolution 55:1452–1463

    CAS  PubMed  Google Scholar 

  • Saks L, McGraw K, Horak P (2003a) How feather colour reflects its carotenoid content. Funct Ecol 17:555–561

    Article  Google Scholar 

  • Saks L, Ots I, Hõrak P (2003b) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134:301–307

    PubMed  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Serra L, Griggio M, Licheri D, Pilastro A (2007) Moult speed constrains the expression of a carotenoid-based sexual ornament. Evol Biol 20:2028–2062

    CAS  Google Scholar 

  • Shawkey MD, Hill GE (2005) Carotenoids need structural colours to shine. Biol Lett 1:121–124

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shawkey MD, Hill GE, McGraw KJ, Hood WR, Huggins K (2006) An experimental test of the contributions and condition dependence of microstructure and carotenoids in yellow plumage coloration. Proc R Soc Lond B 273:2985–2991

    Article  CAS  Google Scholar 

  • Sheldon BC, Andersson S, Griffith SC, Ornborg J, Sendecka J (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877

    Article  CAS  Google Scholar 

  • Siitari H, Huhta E (2002) Individual color variation and male quality in pied flycatchers (Ficedula hypoleuca): a role of ultraviolet reflectance. Behav Ecol 13:737–741

    Article  Google Scholar 

  • Siitari H, Honkavaara J, Huhta E, Viitala J (2002) Ultraviolet reflection and female mate choice in the pied flycatcher, Ficedula hypoleuca. Anim Behav 63:97–102

    Article  Google Scholar 

  • Sirkiä PM, Laaksonen T (2009) Distinguishing between male and territory quality: females choose multiple traits in the pied flycatcher. Anim Behav 78:1051–1060

    Article  Google Scholar 

  • Stevens M, Cuthill IC (2007) Hidden messages: are ultraviolet signals a special channel in avian communication? Bioscience 57:501–507

    Article  Google Scholar 

  • Stradi R, Celentano G, Rossi E, Rovati G, Pastore M (1995) Carotenoids in bird plumage—I. The carotenoid pattern in a series of palearctic carduelinae. Comp Biochem Physiol B 110:131–143

    Article  Google Scholar 

  • Swaddle JP, Cuthill IC (1994) Preference for symmetric males by female zebra finches. Nature 367:165–166

    Article  Google Scholar 

  • Tovée MJ (1995) Ultra-violet photoreceptors in the animal kingdom: their distribution and function. Trends Ecol Evol 10:455–460

    Article  PubMed  Google Scholar 

  • Werner SJ, Tupper SK, Carlson JC, Pettit SE, Ellis JW, Linz GM (2012) The role of a generalized ultraviolet cue for blackbird food selection. Physiol Behav 106:597–601

    Article  CAS  PubMed  Google Scholar 

  • Zampiga E, Hoi H, Pilastro A (2004) Preening, plumage reflectance and female choice in budgerigars. Ethol Ecol Evol 16:339–349

    Article  Google Scholar 

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Acknowledgments

We thank Caterina Funghi, Gonçalo Cardoso, Marta Costa, Sandra Trigo and Teresa Mamede for helping in capturing and maintenance of birds and for their helpful comments. We are grateful to the Editors and to two anonymous referees for their valuable comments. This research was supported by the project PTDC/BIA-BEC/105325/2008 to PGM from the Fundação para a Ciência e a Tecnologia.

Ethical standards

This work was performed in accordance with the Portuguese National Authority for Animal Health (DGAV). Permits for animal capture, transport, maintenance, handling and experiments were carried out under the Institute for Nature Conservation and Biodiversity licences (63/2008/CAPT and 28/2011/CAPT) to PGM, according to Portuguese legislation.

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The authors declare that they have no conflict of interest.

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Correspondence to Paulo G. Mota.

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Communicated by K. McGraw

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Leitão, A.V., Monteiro, A.H. & Mota, P.G. Ultraviolet reflectance influences female preference for colourful males in the European serin. Behav Ecol Sociobiol 68, 63–72 (2014). https://doi.org/10.1007/s00265-013-1623-5

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