Abstract
Colourful plumage is typical of males in species with conventional sex roles, in which females care for offspring and males compete for females, as well as in many monogamous species in which both sexes care for offspring. Reversed sexual dichromatism—more colourful females than males—is predominant in species with sex role reversal. In the latter species, males care for offspring and females compete for mates, the mating system is mainly polyandrous and there is reversed size dimorphism—females are larger than males. Here, we document a case of reversed dichromatism, in the greater flamingo Phoenicopterus roseus, in which there is no sex role reversal and no reversed size dimorphism. Although theoretical models postulate that cases of reversed dichromatism should be rare among monogamous ornamented birds, our findings show that the use of cosmetics might be a mechanism for the occurrence of more ornamented females than males. Indeed, the concentrations of carotenoids in the uropygial secretions used as make-up were higher in females than in males. Apparently, there was a trade-off between coloration and antioxidant defence, as the concentrations of carotenoids in the uropygial secretions were lower during chick provisioning than in other periods, contrary to those in plasma. In this system, the application of make-up would act as a dynamic signal, which would allow a rapid reallocation of resources used for signalling among functions depending on needs. Cases like this may have evolved to signal the ability to provide parental care when females are more physiologically stressed than males.
Significance statement
For species in which there is no sex role reversal, but females are ornamented and the resources allocated to ornaments are important for offspring viability, it has even been suggested that females should be less ornamented than males. This may be because for females, it would be better to invest directly in fecundity rather than in costly ornaments. We show a case of reversed sexual dichromatism in a monogamous bird with no sex role reversal, the greater flamingo, where females apply make-up over feathers. In the case of this species, there could be directional male mate preferences for female plumage coloration because the costs of signalling would not affect breeding investment in females, since cosmetic coloration is not used after it is no longer required, thus allowing the resources used in make-up (carotenoids) to be used in other functions.
Similar content being viewed by others
References
Agresti A (2002) Categorical data analysis, 2nd edn. Wiley, New York
Amat JA, Rendón MA (2017) Flamingo coloration and its significance. In: Anderson M (ed) Flamingos: behavior, biology, and relationship with man. Nova Scientific Publishers, New York, pp 77–95
Amat JA, Rendón MA, Rendón-Martos M, Garrido A, Ramírez JM (2005) Ranging behaviour of greater flamingos during the breeding and post-breeding periods: linking connectivity to biological processes. Biol Conserv 125:183–192. https://doi.org/10.1016/j.biocon.2005.02.018
Amat JA, Rendón MA, Garrido-Fernández J, Garrido A, Rendón-Martos M, Pérez-Gálvez A (2011) Greater flamingos Phoenicopterus roseus use uropygial secretions as make-up. Behav Ecol Sociobiol 65:665–673. https://doi.org/10.1007/s00265-010-1068-z
Amundsen T, Pärn H (2006) Female coloration: review of functional and non-functional hypotheses. In: Hill GE, McGraw KJ (eds) Bird coloration. Volume II. Function and evolution. Harvard University Press, Cambridge, MS, pp 280–345
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Botero CA, Rubenstein DR (2012) Fluctuating environments, sexual selection and the evolution of flexible mate choice in birds. PLoS One 7:e32311. https://doi.org/10.1371/journal.pone.0032311
Bowler JM (1994) The condition of Bewick’s swans Cygnus columbianus bewickii in winter as assessed by their abdominal profiles. Ardea 82:241–248
Broughton DR, Schneider BC, McGraw KJ, Ardia DR (2017) Carotenoids buffer the acute phase response on fever, sickness behavior, and rapid bill color change in zebra finches. J Exp Biol (published online, https://doi.org/10.1242/jeb.155069)
Bulluck LP, Foster MJ, Kay S, Cox DE, Viverette C, Huber S (2017) Feather carotenoid content is correlated with reproductive success and provisioning rate in prothonotary warblers. Auk 134:229–239. https://doi.org/10.1642/AUK-16-151.1
Butler MW, Toomey MB, McGraw KJ (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. https://doi.org/10.1007/s00265-010-1074-1
Cézilly F (1993) Nest desertion in the greater flamingo, Phoenicopterus ruber roseus. Anim Behav 45:1038–1040. https://doi.org/10.1006/anbe.1993.1125
Chenoweth SF, Doughty P, Kokko H (2006) Can non-directional male mating preferences facilitate honest female ornamentation? Ecol Lett 9:179–184. https://doi.org/10.1111/j.1461-0248.2005.00867.x
Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885. https://doi.org/10.1126/science.1133311
Clutton-Brock T (2009) Sexual selection in females. Anim Behav 77:3–11. https://doi.org/10.1016/j.anbehav.2008.08.026
Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org
Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London
Delhey K, Peters A, Johnsen A, Kempenaers B (2006) Seasonal changes in blue tit crown color: do they signal individual quality? Behav Ecol 17:790–798. https://doi.org/10.1093/beheco/arl012
Delhey K, Peters A, Kempenaers B (2007) Cosmetic coloration in birds: occurrence, function, and evolution. Am Nat 169:S145–S158. https://doi.org/10.1086/510095
Dell Inc (2015) STATISTICA (data analysis software system), version 12, www.statsoft.com
Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91. https://doi.org/10.2307/2408316
Endler JA, Mielke P (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431. https://doi.org/10.1111/j.1095-8312.2005.00540.x
Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103. https://doi.org/10.1126/science.1081802
Freeman HD, Valuska AJ, Taylor RR, Ferrie GM, Grand AP, Leighty KA (2016) Plumage variation and social partner choice in the greater flamingo (Phoenicopterus roseus). Zoo Biol 35:409–414. https://doi.org/10.1002/zoo.21321
Gladbach A, Gladbach DJ, Kempenaers B, Quillfeldt P (2010) Female-specific colouration, carotenoids and reproductive investment in a dichromatic species, the upland goose Chloephaga picta leucoptera. Behav Ecol Sociobiol 64:1779–1789. https://doi.org/10.1007/s00265-010-0990-4
Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075. https://doi.org/10.1046/j.1365-294x.1998.00389.x
Heinsohn R, Legge S, Endler JA (2005) Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309:617–619. https://doi.org/10.1126/science.1112774
Henschen AE, Whittingham LA, Dunn PA (2016) Oxidative stress is related to both melanin- and carotenoid-based ornaments in the common yellowthroat. Funct Ecol 30:749–758. https://doi.org/10.1111/1365-2435.12549
Hill GE (2002) A red bird in a brown bag: the function and evolution of ornamental plumage coloration in the house finch. Oxford University Press, Oxford
Hill GE (2014) Stress, condition, and ornamentation. Integr Comp Biol 54:533–538. https://doi.org/10.1093/icb/icu086
Hodos W (1993) The visual capabilities of birds. In: Zeigler PH, Bischof H-J (eds) Vision, brain and behavior in birds. MIT Press, Cambridge, MS, pp 63–76
Hutton P, Seymoure BM, McGraw KJ, Ligon RA, Simpson RK (2015) Dynamic color communication. Curr Opin Behav Sci 6:41–49. https://doi.org/10.1016/j.cobeha.2015.08.007
Isaksson C, Andersson S (2008) Oxidative stress does not influence carotenoid mobilization and plumage pigmentation. Proc R Soc Lond B 275:309–314
Jenni-Eiermann S, Jenni L, Smith S, Constantini D (2014) Oxidative stress in endurance flight: an unconsidered factor in bird migration. PLoS One 9:e95650. https://doi.org/10.1371/journal.pone.0097650
Johnson A, Cézilly F (2007) The greater flamingo. Poyser, London
Johnson IP, Sibly RM (1993) Pre-breeding behaviour affects condition, assessed by abdominal profile, and hence breeding success of Canada geese Branta canadensis. Wildfowl 44:60–68
Kraaijeveld K (2003) Degree of mutual ornamentation in birds is related to divorce rate. Proc R Soc Lond B 270:1785–1791. https://doi.org/10.1098/rspb.2003.2450
Kraaijeveld K, Kraaijeveld-Smit FLJ, Komdeur J (2007) The evolution of mutual ornamentation. Anim Behav 74:657–677. https://doi.org/10.1016/j.anbehav.2006.12.027
Maia R, White TE (2018) Comparing colors using visual models. Behav Ecol 29:649–659. https://doi.org/10.1093/beheco/ary017
Maia R, Eliason CM, Bitton P-P, Doucet SM, Shawkey MD (2013) Pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:609–613. https://doi.org/10.1111/2041-210X.12069
Mair P, Schoenbrodt F, Wilcox R (2017) WRS2: Wilcox robust estimation and testing. R package v 0.9–2, https://cran.r-project.org/web/packages/WRS2
Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford
McGraw KJ (2006) Mechanisms of carotenoid-based coloration. In: McGraw KJ (ed) Hill GE. Bird coloration.Volume I. Mechanisms and measurements. Harvard University Press, Cambridge, MS, pp 177–242
Montgomerie R (2006) Cosmetic and adventitious colors. In: McGraw KJ (ed) Hill GE. Bird coloration.Volume I. Mechanisms and measurements. Harvard University Press, Cambridge, MS, pp 399–427
Negro JJ, Tella JL, Blanco G, Forero MG, Garrido-Fernández J (2000) Diet explains interpopulation variation of plasma carotenoids and skin pigmentation in nestling white storks. Physiol Biochem Zool 73:97–101. https://doi.org/10.1086/316724
Nordeide JT, Kekäläinen J, Janhunen M, Kortet R (2013) Females ornaments revisted—are they correlated with offspring quality? J Anim Ecol 82:26–38. https://doi.org/10.1111/1365-2656.12021
Ödeen A, Håstad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855–862. https://doi.org/10.1093/molbev/msg108
Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593–599. https://doi.org/10.1098/rspb.1996.0089
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. https://doi.org/10.1007/s00114-008-0389-5
Perrot C, Béchet A, Hanzen C, Arnaud A, Pradel R, Cézilly F (2016) Sexual-display complexity varies non-linearly with age and predicts breeding status in greater flamingos. Sci Rep 6:36242. https://doi.org/10.1038/srep36242
Powell DM (1997) Display behaviour and breeding biology of Caribbean flamingos (Phoenicopterus ruber ruber). Anim Keepers Forum 24:395–405
Rendón MA, Garrido A, Ramírez JM, Rendón-Martos M, Amat JA (2001) Despotic establishment of breeding colonies of greater flamingos, Phoenicopterus ruber, in southern Spain. Behav Ecol Sociobiol 50:55–60. https://doi.org/10.1007/s002650100326
Rendón MA, Garrido A, Amat JA, Rendón-Martos M (2009) Monitoring of greater flamingo colonies: some proposals for measuring and interpreting results. Flamingo 1:62–75
Rendón MA, Garrido A, Guerrero JC, Rendón-Martos M, Amat JA (2012) Crop size as an index of chick provisioning in the greater flamingo Phoenicopterus roseus. Ibis 154:379–388. https://doi.org/10.1111/j.1474-919X.2012.01218.x
Rendón MA, Garrido A, Rendón-Martos M, Ramírez JM, Amat JA (2014) Assessing sex-related chick provisioning in greater flamingo Phoenicopterus roseus parents using capture-recapture models. J Anim Ecol 83:479–490. https://doi.org/10.1111/1365-2656.12138
Rosenthal MF, Murphy TG, Darling N, Tarvin KA (2012) Ornamental bill color rapidly signals changing condition. J Avian Biol 43:553–564. https://doi.org/10.1111/j.1600-048X.2012.05774.x
Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton
Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton
Simons MJP, Cohen AA, Verhulst S (2012) What does carotenoid-dependent coloration tell? Plasma carotenoid level signals immunocompetence and oxidative stress state in birds—a meta-analysis. PLoS One 7:e43088. https://doi.org/10.1371/journal.pone.0043088
Studer-Thiersch A (1986) Tarsus length as an indication of sex in the flamingo genus Phoenicopterus. Int Zoo Yearb 24(25):240–243. https://doi.org/10.1111/j.1748-1090.1985.tb02546.x
Svensson PA, Forsgren E, Amundsen T, Nilsson Sköld H (2005) Chromatic interaction between egg pigmentation and skin chromatophores in the nuptial coloration of females two-spotted gobies. J Exp Biol 208:4391–4397. https://doi.org/10.1242/jeb.01925
Tavecchia G, Pradel R, Boy V, Johnson AR, Cézilly F (2001) Sex- and age-related variation in survival and cost of first reproduction in greater flamingos. Ecology 82:165–174. https://doi.org/10.1890/0012-9658(2001)082[0165:SAARVI]2.0.CO;2
Tobias JA, Montgomerie R, Lyon B (2012) The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Phil Trans R Soc B 367:2274–2293. https://doi.org/10.1098/rstb.2011.0280
Torres R, Velando A (2003) A dynamic trait affects continuous pair assessment in the blue-footed booby, Sula nebouxii. Behav Ecol Sociobiol 55:65–72. https://doi.org/10.1007/s00265-003-0669-1
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer-Verlag New York Inc., New York
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358. https://doi.org/10.1098/rspb.1998.0302
Vorobyev M, Osorio D, Bennett ATD, Marshall N, Cuthill I (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633. https://doi.org/10.1007/s003590050286
Woodall AA, Lee SW-M, Weesie RJ, Jackson MJ, Britton G (1997) Oxidation of carotenoids by free radicals: relationship between structure and reactivity. Biochim Biophys Acta 1336:33–42. https://doi.org/10.1016/S0304-4165(97)00006-8
Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305. https://doi.org/10.1126/science.287.5451.303
Zillich U, Black J (2002) Body mass and abdominal profile index of captive Hawaiian geese. Wildfowl 53:67–77
Acknowledgments
We thank “Cañada de los Pájaros” for providing facilities. M. I. Adrián, O. González, P. Rodríguez, and M. Vázquez helped to capture flamingos and taking samples. Mónica Gutiérrez, from LEM-EBD, did the molecular sexing. Two anonymous reviewers and the editors commented on an earlier version.
Funding
Funds were received from Ministerio de Educación y Ciencia of Spain with EU-EURF support (research grants BOS2002-04695 and CGL2005-01136/BOS).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
International, national, and institutional guidelines for the use and capture of animals were followed. Consejería de Medio Ambiente from the Junta de Andalucía (Regional Government) gave permission to conduct the study. An approval from an ethics committee was not needed.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by E. Fernandez-Juricic
Electronic supplementary material
ESM 1
(PDF 5353 kb)
Rights and permissions
About this article
Cite this article
Amat, J.A., Garrido, A., Portavia, F. et al. Dynamic signalling using cosmetics may explain the reversed sexual dichromatism in the monogamous greater flamingo. Behav Ecol Sociobiol 72, 135 (2018). https://doi.org/10.1007/s00265-018-2551-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-018-2551-1