The Science of Nature

, 105:31 | Cite as

Superciliums in white-eared hummingbirds as badges of status signaling dominance

  • Juan Manuel González-García
  • Carlos Lara
  • Javier Quesada
  • Carlos A. Chávez-Zichinelli
  • Martín A. Serrano-Meneses
Original Paper


The role of badges as indicators of contest ability has been previously described. In hummingbirds, the exhibition of a badge is expected to save energy expenditure in agonistic interactions and to favor energy intake. Here, we investigate whether variable supercilium size in the white-eared hummingbird has a role in dominance status signaling. Firstly, 45 hummingbird males were captured and their superciliums were photographed to investigate variation in size and any possible allometric relationships. Secondly, 42 male birds were used to analyze whether the supercilium has a role in dominance status signaling in a dyadic contest. We found that supercilium size varied continuously but that despite variability between individuals, there was no relationship between supercilium size and body size. However, our dyad experiment indicated that birds with larger badges were able to make more visits to the feeders than individuals with smaller badges. We suggest a status signaling function of the supercilium.


Dominance Hylocharis leucotis Recognizing dominance Signal reliability Status badge 



We would like to thank M. J. Pérez-Crespo and V. Mendiola for their assistance in the field and their logistical support. To Mike Lockwood for the revision of the manuscript in English. Pietro K. Maruyama and three anonymous reviewers provided useful comments on previous versions of the manuscript. Permission to conduct our fieldwork was granted by the Mexican government (SEMARNAT, FAUT-0296). This work constitutes partial fulfillment of JMG’s doctorate at the Universidad Autónoma de Tlaxcala.


The Consejo Nacional de Ciencia y Tecnología (CONACYT: 365006/248109) provided the first author with financial support in the form of a scholarship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All experiments comply with the current Mexican laws.


  1. Akaike H (1981) Likelihood of a model and information criteria. J Econ 16:3–14. CrossRefGoogle Scholar
  2. Altshuler DL, Stiles FG, Dudley YR (2004) Of hummingbirds and helicopters: hovering costs, competitive ability and foraging strategies. Am Nat 163:16–25. CrossRefPubMedGoogle Scholar
  3. Álvarez HA, Serrano-Meneses MA, Reyes-Márquez I, Jiménez-Cortés JG, Córdoba-Aguilar A (2013) Allometry of a sexual trait in relation to diet experience and alternative mating tactics in two rubyspot damselflies (Calopterygidae: Hetaerina). Biol J Linn Soc 108:521–533. CrossRefGoogle Scholar
  4. Barnard CJ (1984) The evolution of food-scrounging strategies within and between species. In: Barnard CJ (ed) Producers and scroungers: strategies of exploitation and parasitism. Croom Helm, London, pp 95–127CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects model using Eigen and S4. R package version 1.1–6. Available at: (Accessed April 2015)
  6. Bleiweiss R (1985) Iridescent polychromatism in a female hummingbird: is it related to feeding strategies? Auk 102:701–713Google Scholar
  7. Brown JL, Orians GH (1970) Spacing patterns in mobile animals. Annu Rev Ecol Evol Syst 1:239–262. CrossRefGoogle Scholar
  8. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. (Accessed March 2018)
  9. Butcher GS, Rohwer S (1989) The evolution of conspicuous and distinctive coloration for communication in birds. In: Power DM (ed) Current ornithology, vol 6. Plenum Press, New York, pp 51–108CrossRefGoogle Scholar
  10. Calisi RM, Malone JH, Hews DK (2008) Female secondary coloration in the mexican boulder spiny lizard is associated with nematode load. J Zool 276:358–367. CrossRefGoogle Scholar
  11. Camfield AF (2006) Resource value affects territorial defense by broad-tailed and rufous hummingbirds. J Field Ornithol 77:120–125. CrossRefGoogle Scholar
  12. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595. CrossRefPubMedGoogle Scholar
  13. Carpenter FL, Hixon MA, Russell RW, Paton DC, Temeles EJ (1993) Interference asymmetries among age-sex clases of rufous hummingbird during migratory stopovers. Behav Ecol Sociobiol 33:297–304. Google Scholar
  14. Chaine AS, Roth AM, Shizuka D, Lyon BE (2013) Experimental confirmation that avian plumage traits function as multiple status signals in winter contests. Anim Behav 86:409–415. CrossRefGoogle Scholar
  15. Chávez-Zichinelli CA, Gómez L, Ortiz-Pulido R, Lara C, Valdéz R, Romano MC (2014) Testosterone levels in feces predict risk-sensitive foraging in hummingbirds. J Avian Biol 45:501–506. CrossRefGoogle Scholar
  16. Dearborn DC (1998) Interspecific territoriality by a rufous-tailed hummingbird (Amazilia tzacatl): effects of intruder size and resource value. Biotropica 30:306–313. CrossRefGoogle Scholar
  17. Dunlap KD, Schall J (1995) Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol Zool 68:608–621. CrossRefGoogle Scholar
  18. Endler JA (1978) A predator’s view of animal color patterns. Evol Biol 11:319–364. Google Scholar
  19. Ewald PW (1985) Influence of asymmetries in resource quality and age on aggression and dominance in black-chinned hummingbirds. Anim Behav 33:705–719. CrossRefGoogle Scholar
  20. Ewald PW, Rohwer S (1980) Age, coloration and dominance in nonbreeding hummingbirds: a test of the asymmetry hypothesis. Behav Ecol Sociobiol 7:273–279. CrossRefGoogle Scholar
  21. Feinsinger P, Colwell RK (1978) Community organization among neotropical nectar-feeding birds. Am Zool 18:779–795. CrossRefGoogle Scholar
  22. Fitzpatrick S (1998) Birds’ tails as signaling devices: markings, shape, length, and feather quality. Am Nat 151:157–173. CrossRefPubMedGoogle Scholar
  23. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622. CrossRefGoogle Scholar
  24. Fowlie MK, Krüger O (2003) The evolution of plumage polymorphism in birds of prey and owls: the apostatic selection hypothesis revisited. J Evol Biol 16:577–583. CrossRefPubMedGoogle Scholar
  25. Gass CL (1979) Territory regulation, tenure, and migration in rufous hummingbirds. Can J Zool 57:914–923. CrossRefGoogle Scholar
  26. Goloff BM, Burch S (2012) Stress response in the rufous hummingbird (Selasphorus rufus): mechanisms of personality and social dominance. Friday Harbor Laboratories Student Research Papers. University of Washington
  27. Goodwin TW (1984) The biochemistry of the carotenoids. Chapman and Hall, LondonCrossRefGoogle Scholar
  28. Gould SJ (1974) The origin and function of “bizarre” structures: antler size in the “Irish elk”, Megaloceros giganteus. Evolution 28:191–220. PubMedGoogle Scholar
  29. 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. CrossRefGoogle Scholar
  30. Gustafsson L, Qvarnström A, Sheldon BC (1995) Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers. Nature 375:311–313. CrossRefGoogle Scholar
  31. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387. CrossRefPubMedGoogle Scholar
  32. Hixon MA, Carpenter FL, Paton DC (1983) Territory area, flower density, and time budgeting in hummingbirds: an experimental and theoretical analysis. Am Nat 122:366–391. CrossRefGoogle Scholar
  33. Howell SN, Webb S (1995) A guide to the birds of Mexico and northern central America. Oxford University PressGoogle Scholar
  34. Husak JF, Henningsen JP, Vanhooydonck B, Irschick DJ (2015) A performance-based approach to studying costs of reliable signals. In: Animal signaling and function: an integrative approach (Irschick DJ, Briffa M, Podos J, eds). John Wiley and Sons. p. 4774Google Scholar
  35. Ingles J (1976) Observations on the hummingbirds Orthorhynchucsr istatus and Eulampis jugularis of Martinique (West Indies). Gerfaut 66:129–132Google Scholar
  36. Justino DG, Maruyama PK, Oliveira PE (2012) Floral resource availability and hummingbird territorial behaviour on a Neotropical savanna shrub. J Ornithol 153:189–197. CrossRefGoogle Scholar
  37. Justyn NM, Peteya JA, D’Alba L, Shawkey (2017) Preferential attachment and colonization of the keratinolytic bacterium Bacilius licheniformis on black and white-striped feathers. Auk 134:466–473. CrossRefGoogle Scholar
  38. Kodric-Brown A, Brown JH (1978) Influence of economics, interspecific competition and sexual dimorphism on territoriality of migrant rufous hummingbirds. Ecology 59:285–296. CrossRefGoogle Scholar
  39. Kodric-Brown A, Sibly RM, Brown JH (2006) The allometry of ornaments and weapons. Proc Natl Acad Sci U S A 103:8733–8738. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kose M, Møller AP (1999) Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the barn swallow (Hirundo rustica). Behav Ecol Sociobiol 45:430–436. CrossRefGoogle Scholar
  41. Krebs JR, Davies NB (1987) An introduction to behavioural ecology, 2nd edn. Blackwell Scientific Publications, OxfordGoogle Scholar
  42. Lank DB (2002) Diverse processes maintain plumage polymorphisms in birds. J Avian Biol 33:327–330. CrossRefGoogle Scholar
  43. Lara C (2006) Temporal dynamics of flower use by hummingbirds in a temperate forest in Mexico. Ecoscience 13:23–29. CrossRefGoogle Scholar
  44. Lyon BE, Montgomerie R (2012) Sexual selection is a form of social selection. Philos Trans R Soc Lond Ser B Biol Sci 367:2266–2273. CrossRefGoogle Scholar
  45. Matta NE, Lotta IA, Valkiūnas G, González AD, Pacheco MA, Escalante AA, Moncada LI, Rodríguez-Fandiño OA (2014) Description of Leucocytozoon quynzae sp. nov.(Haemosporida, Leucocytozoidae) from hummingbirds, with remarks on distribution and possible vectors of leucocytozoids in South America. Parasitol Res 113:457–468. CrossRefPubMedGoogle Scholar
  46. McGlothlin JW, Parker PG, Nolan V Jr, Ketterson ED (2005) Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos. Evolution 59:658–671. CrossRefPubMedGoogle Scholar
  47. McGlothlin JW, Duffy DL, Henry-Freeman JL, Ketterson ED (2007) Diet quality affects an attractive white plumage pattern in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 61:1391–1399. CrossRefGoogle Scholar
  48. Mercadante A, Hill GE (2014) An experimental test of the role of structural blue and melanin- based chestnut coloration in aggressive contests in male eastern bluebirds. Front Ecol Evol 2:24. CrossRefGoogle Scholar
  49. Møller AP (1987) Variation in badge size in male house sparrows Passer domesticus: evidence for status signalling. Anim Behav 35:1637–1644. CrossRefGoogle Scholar
  50. Montgomerie RD, Gass CL (1981) Energy limitation of hummingbird population in tropical and temperate communities. Oecologia 50:162–165. CrossRefPubMedGoogle Scholar
  51. Muck C, Goymann W (2011) Throat patch size and darkness covaries with testosterone in females of a sex-role reversed species. Behav Ecol 22:1312–1319. CrossRefGoogle Scholar
  52. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956. PubMedGoogle Scholar
  53. Németh Z, Moore FR (2012) Differential timing of spring passage of ruby-throated hummingbirds along the northern coast of the Gulf of Mexico. J Field Ornithol 83:26–31. CrossRefGoogle Scholar
  54. Ornelas JF, Ordano M, Hernández A, López JC, Mendoza L, Perroni Y (2002) Nectar oasis produced by Agave marmorata Roezl. (Agavaceae) lead to spatial and temporal segregation among nectarivores in the Tehuacán Valley, México. J Arid Environ 52:37–51. CrossRefGoogle Scholar
  55. Parker GA (1974) Assessment strategy and the evolution of fighting behaviour. J Theor Biol 47:223–243. CrossRefPubMedGoogle Scholar
  56. Pascual J, Senar JC (2014) Antipredator behavioural compensation of proactive personality trait in male Eurasian siskins. Anim Behav 90:297–303. CrossRefGoogle Scholar
  57. Paton D, Caryl PG (1986) Communication by agonistic displays: 1. variation in information content between samples. Behaviour 98:213–239. CrossRefGoogle Scholar
  58. Petrie M (1988) Intraspecific variation in structures that display competitive ability: large animals invest relatively more. Anim Behav 36:1174–1179. CrossRefGoogle Scholar
  59. Petrie M (1992) Are all secondary sexual display structures positively allometric and, if so, why? Anim Behav 43:173–175. CrossRefGoogle Scholar
  60. Pitelka FA (1942) Territoriality and related problems in north American hummingbirds. Condor 44:189–204. CrossRefGoogle Scholar
  61. Pryke SR (2013) Bird contests: from hatching to fertilisation. In: Hardy IC, Briffa M (eds) Animal contests. Cambridge University Press, New York, pp 287–303CrossRefGoogle Scholar
  62. Pyle P (1997) Identification guide to north American birds, Part I. Slate Creek Press, BolinasGoogle Scholar
  63. Quesada J, Chávez-Zichinelli CA, Senar JC, Schondube JE (2013) Plumage coloration of the blue grosbeak has no dual function: a test of the armament-ornament model of sexual selection. Condor 115:902–909. CrossRefGoogle Scholar
  64. R Core Team (2014) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (Accessed 2 April 2015)
  65. Rat M, van Dijk RE, Covas R, Doutrelant C (2015) Dominance hierarchies and associated signalling in a cooperative passerine. Behav Ecol Sociobiol 69:437–448. CrossRefGoogle Scholar
  66. Rémy A, Grégoire A, Perret P, Doutrelant C (2010) Mediating male–male interactions: the role of the UV blue crest coloration in blue tits. Behav Ecol Sociobiol 64:1839–1847. CrossRefGoogle Scholar
  67. Ressel S, Schall JJ (1989) Parasites and showy males: malarial infection and color variation in fence lizards. Oecologia 78:158–164. CrossRefPubMedGoogle Scholar
  68. Rohwer SA (1975) The social significance of avian winter plumage variability. Evolution 29:593–610. CrossRefPubMedGoogle Scholar
  69. Rohwer SA (1982) The evolution of reliable and unreliable badges of fighting ability. Am Zool 22:531–546. CrossRefGoogle Scholar
  70. Salvador A, Veiga JP, Martin J, Lopez P, Abelenda M, Puerta M (1996) The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation. Behav Ecol 7:145–150. CrossRefGoogle Scholar
  71. Santos ES, Scheck D, Nakagawa S (2011) Dominance and plumage traits: meta-analysis and metaregression analysis. Anim Behav 82:3–19. CrossRefGoogle Scholar
  72. Schuchmann KL (1999) Family Trochilidae (Hummingbirds). In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the Birds of the World, vol 5. Lynx Editions, Barcelona, pp 468–680Google Scholar
  73. Senar JC (2006) Color displays as intrasexual signals of aggression and dominance. In: Hill GE, McGraw KJ (eds) Bird Coloration, vol 2. Harvard University Press, Cambridge, pp 87–136Google Scholar
  74. Senar J, Camerino M, Metcalfe N (1990) Familiarity breeds tolerance: the development of social stability in flocking siskins (Carduelis spinus). Ethology 85:13–24. CrossRefGoogle Scholar
  75. Senar JC, Camerino M, Copete JL, Metcalfe NB (1993) Variation in the black bib of the eurasian siskin (Carduelis spinus) and its role as a reliable badge of dominance. Auk 110:924–927. CrossRefGoogle Scholar
  76. Skutch AF (1940) Accounts in life histories of North American cuckoos, goatsuckers, hummingbirds and their allies (A. C. Bent). US Natl Mus Bull 176Google Scholar
  77. Smith MJ, Harper DG (1995) Animal signals: models and terminology. J Theor Biol 177:305–311. CrossRefGoogle Scholar
  78. Smith MJ, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  79. Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research, 4th edn. Freeman, San FranciscoGoogle Scholar
  80. Stiles FG (1981) Geographical aspects of bird-flower coevolution, with particular reference to Central America. Ann Mo Bot Gard 68:323–351. CrossRefGoogle Scholar
  81. Stiles FG (1982) Aggressive and courtship displays of the male Anna’s hummingbird. The Condor 84:208–225. CrossRefGoogle Scholar
  82. Stiles FG (1995) Behavioral, ecological and morphological correlates of foraging for arthropods by the hummingbirds of a tropical wet forest. Condor 97:853–878. CrossRefGoogle Scholar
  83. Stiles FG, Wolf LL (1979) Ecology and evolution of lek mating behavior in the Long-tailed Hermit hummingbird. Ornithol Monogr 27:1–78. Google Scholar
  84. Stiles FG, Altshuler DL, Dudley R (2005) Wing morphology and flight behavior of some North American hummingbird species. Auk 122:872–886. CrossRefGoogle Scholar
  85. Stuart-Fox DM, Moussalli A, Marshall NJ, Owens IP (2003) Conspicuous males suffer higher predation risk: visual modeling and experimental evidence from lizards. Anim Behav 66:541–550. CrossRefGoogle Scholar
  86. Studd VM, Robertson RJ (1985) Evidence for reliable badges of status in territorial yellow warblers (Dendroica petechia). Anim Behav 33:1102–1113. CrossRefGoogle Scholar
  87. Tibbetts EA, Dale J (2004) A socially enforced signal of quality in a paper wasp. Nature 423:218–222. CrossRefGoogle Scholar
  88. Tiebout HM (1996) Costs and benefits of interspecific dominance rank: are subordinates better at finding novel food locations? Anim Behav 5:1375–1381. CrossRefGoogle Scholar
  89. Tobias JA, Montgomerie R, Lyon BE (2012) The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philos Trans R Soc B 367:2274–2293. CrossRefGoogle Scholar
  90. Török J, Hegyi G, Garamszegi LZ (2003) Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. Behav Ecol 14:382–388. CrossRefGoogle Scholar
  91. Vedder O, Schut E, Magrath MJ, Komdeur J (2010) Ultraviolet crown colouration affects contest outcomes among male blue tits, but only in the absence of prior encounters. Funct Ecol 24:417–425. CrossRefGoogle Scholar
  92. Villers RL, Rojas GF, Tenorio LP (2006) Botanic guide to the La Malinche National Park Tlaxcala-Puebla. Universidad Nacional Autónoma de México. México. D.FGoogle Scholar
  93. Wagner HO (1946) Food and feeding habits of Mexican hummingbirds. Willson Bull 58:69–132Google Scholar
  94. Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3—an R package for estimation and inference about allometric lines. Methods in Ecol Evol 3:257–259. CrossRefGoogle Scholar
  95. Whitfield DP (1987) Plumage variability, status signalling and individual recognition in avian flocks. Trends Ecol Evol 2:13–18. CrossRefGoogle Scholar
  96. Williamson SL (2001) A field guide to hummingbirds of North America. Houghton Mifflin Harcourt, New YorkGoogle Scholar
  97. Wolf LL (1969) Female territoriality in a tropical hummingbird. Auk 86:490–504. CrossRefGoogle Scholar
  98. Wolf LL, Stiles FG (1970) Evolution of pair cooperation in a tropical hummingbird. Evolution 24:759–773. CrossRefPubMedGoogle Scholar
  99. Wolf LL, Stiles FG, Hainsworth FR (1976) Ecological organization of a tropical, highland hummingbird community. J Anim Ecol 45:349–379. CrossRefGoogle Scholar
  100. Young CM, Cain KE, Svedin N, Backwell PRY, Pryke SR (2015) The role of pigment based plumage traits in resolving conflicts. J Avian Biol 47:167–175. CrossRefGoogle Scholar
  101. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Juan Manuel González-García
    • 1
  • Carlos Lara
    • 2
  • Javier Quesada
    • 3
  • Carlos A. Chávez-Zichinelli
    • 4
  • Martín A. Serrano-Meneses
    • 5
  1. 1.Doctorado en Ciencias BiológicasUniversidad Autónoma de TlaxcalaPueblaMexico
  2. 2.Centro de Investigación en Ciencias BiológicasUniversidad Autónoma de TlaxcalaTlaxcalaMexico
  3. 3.Natural History Museum of Barcelona, Chordates LaboratoryBarcelonaSpain
  4. 4.El Colegio de PueblaLa PazMexico
  5. 5.Universidad de las Américas PueblaPueblaMexico

Personalised recommendations