Behavioral Ecology and Sociobiology

, Volume 68, Issue 6, pp 1007–1017 | Cite as

Defeated chameleons darken dynamically during dyadic disputes to decrease danger from dominants

  • Russell A. LigonEmail author
Original Paper


Research on intraspecific aggression has typically focused on dominant individuals, but a better understanding of the consequences and mechanisms of agonistic encounters requires a balanced perspective that includes knowledge of subordinate animal behaviors. In contrast to signals of fighting ability, signals of submission are an understudied component of agonistic communication that could provide important insights into the dynamics, function, and evolution of intraspecific competition. Here, I use a series of staged agonistic trials between adult male veiled chameleons Chamaeleo calyptratus to test the hypothesis that rapid skin darkening serves as a submissive signal to resolve agonistic activity. Concordant with this hypothesis, I found that losing chameleons darkened over the course of aggressive trials while winners brightened, and the likelihood of darkening increased when individuals were attacked more aggressively. Additionally, I found that the degree of brightness change exhibited by individual chameleons was tied to both overall and net aggression experienced during a trial, with chameleons who received high levels of aggression relative to their own aggression levels darkening to a greater extent than individuals receiving relatively less aggression. Lastly, I found that aggression increased for losers and winners prior to the onset of darkening by the eventual loser but that both chameleons reduced aggression after the losing chameleon began to darken. Based on the theoretical prediction that signals of submission should be favored when retreat options are restricted, I suggest that limited escapability imposed by chameleon morphology, physiology, and ecology favored the evolution of a pigment-based signal of submission in this group.


Submissive signals Physiological color change Aggression Communication Reptiles Chamaeleo calyptratus Color signals 



I thank Megan Best, Sarah Bruemmer, Brianna Bero-Buell, and Andrea Carpenter for their invaluable assistance with experimental procedures, data collection, and dedicated chameleon care. I thank the Animal Behavior Society, the American Society for Ichthyologists and Herpetologists, the ASU chapter of Sigma Xi, and the ASU Graduate and Professional Students Association for financial support of this research. I also thank my parents, David and Sandy Ligon, as well as Richard and Janet Steele and two anonymous donors for their generous financial support to this project. I thank my advisor Kevin McGraw, Dale DeNardo, and members of the McGraw lab group for input that greatly improved this manuscript. I also thank my wife, Veronica Ligon, for her support throughout this project.

Supplementary material

265_2014_1713_MOESM1_ESM.pdf (7 kb)
ESM 1 (PDF 6 kb)
265_2014_1713_MOESM2_ESM.pdf (47 kb)
ESM 2 (PDF 47 kb)

(MP4 11615 kb)


  1. Abu-Ghalyun Y, Greenwald L, Hetherington TE, Gaunt AS (1988) The physiological basis of slow locomotion in chamaeleons. J Exp Zool 245:225–231PubMedCrossRefGoogle Scholar
  2. Batista G, Zubizarreta L, Perrone R, Silva A (2012) Non-sex-biased dominance in a sexually monomorphic electric fish: fight structure and submissive electric signalling. Ethology 118:398–410CrossRefGoogle Scholar
  3. Bergman TJ, Beehner JC (2008) A simple method for measuring colour in wild animals: validation and use on chest patch colour in geladas (Theropithecus gelada). Biol J Linn Soc 94:231–240CrossRefGoogle Scholar
  4. Bowmaker JK, Lowe ER, Ott M (2005) The cone photoreceptors and visual pigments of chameleons. J Comp Physiol A 191:925–932CrossRefGoogle Scholar
  5. Bradbury J, Vehrencamp S (1998) Principles of animal communication. Sinauer, MassachusettsGoogle Scholar
  6. Briffa M, Hardy ICW, Gammell MP, Jennings DJ, Clarke DD, Goubault M (2013) Analysis of animal contest data. In: Hardy ICW, Briffa M (eds) Animal contests. Cambridge University Press, New York, pp 47–85CrossRefGoogle Scholar
  7. Burrage BR (1973) Comparative ecology and behaviour of Chamaeleo pumilus (Gmelin) and C. namaquensis A. Smith (Sauria: Chamaeleonidae). Ann S Afr Mus 61:1–158Google Scholar
  8. Bustard HR (1965) Observations on the life history and behavior of Chamaeleo hohnelii (Steindachner). Copeia 1965:401–410CrossRefGoogle Scholar
  9. Bustard HR (1967) The comparative behavior of chameleons: fight behavior in Chameleo gracilis Hallowell. Herpetologica 23:44–50Google Scholar
  10. Cuadrado M (2000) Body colors indicate the reproductive status of female common chameleons: experimental evidence for the intersex communication function. Ethology 106:79–91CrossRefGoogle Scholar
  11. Cuadrado M (2001) Mate guarding and social mating system in male common chameleons (Chamaeleo chamaeleon). J Zool 255:425–435CrossRefGoogle Scholar
  12. Darwin C (1872) The expression of the emotions in man and the animals. Murray, LondonCrossRefGoogle Scholar
  13. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0,
  14. East ML, Hofer H, Wickler W (1993) The erect ‘penis’ is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behav Ecol Sociobiol 33:355–370CrossRefGoogle Scholar
  15. Eaton L, Sloman KA (2011) Subordinate brown trout exaggerate social signaling in turbid conditions. Anim Behav 81:603–608CrossRefGoogle Scholar
  16. Eberle AN (1988) The melanotropins: chemistry, physiology and mechanisms of action. Karger, SwitzerlandGoogle Scholar
  17. Enquist M, Leimar O (1990) The evolution of fatal fighting. Anim Behav 39:1–9CrossRefGoogle Scholar
  18. Fischer MS, Krause C, Lilje KE (2010) Evolution of chameleon locomotion, or how to become arboreal as a reptile. Zoology 113:67–74PubMedCrossRefGoogle Scholar
  19. Forster GL, Watt MJ, Korzan WJ, Renner KJ, Summers CH (2005) Opponent recognition in male green anoles, Anolis carolinensis. Anim Behav 69:733–740CrossRefGoogle Scholar
  20. Hannes RP, Franck D, Liemann F (1984) Effects of rank order fights on whole-body and blood concentrations of androgens and corticosteroids in the male swordtail (Xiphophorus helleri). Z Tierpsychol 65:53–65CrossRefGoogle Scholar
  21. Harkness L (1977) Chameleons use accommodation cues to judge distance. Nature 267:346–349PubMedCrossRefGoogle Scholar
  22. Hogben LT, Mirvish L (1928) The pigmentary effector system. V. The nervous control of excitement pallor in reptiles. J Exp Biol 5:295–308Google Scholar
  23. Höglund E, Balm PH, Winberg S (2000) Skin darkening, a potential social signal in subordinate artic charr (Salvelinus alpinus): the regulatory role of brain monoamines and pro-opiomelanocortin-derived peptides. J Exp Biol 203:1711–1721PubMedGoogle Scholar
  24. Huhman KL, Moore TO, Mougey EH, Meyerhoff JL (1992) Hormonal responses to fighting in hamsters: separation of physical and psychological causes. Physiol Behav 51:1083–1086PubMedCrossRefGoogle Scholar
  25. Huntingford FA, Taylor AC, Smith IP, Thorpe KE (1995) Behavioural and physiological studies of aggression in swimming crabs. J Exp Mar Biol Ecol 193:21–39CrossRefGoogle Scholar
  26. Hurd PL, Wachtmeister CA, Enquist M (1995) Darwin’s principle of antithesis revisited: a role for perceptual biases in the evolution of intraspecific signals. Proc R Soc Lond B 259:201–205CrossRefGoogle Scholar
  27. Issa FA, Edwards DH (2006) Ritualized submission and the reduction of aggression in an invertebrate. Curr Biol 16:2217–2221PubMedCrossRefGoogle Scholar
  28. Karsten KB, Andriamandimbiarisoa LN, Fox SF, Raxworthy CJ (2009) Social behavior of two species of chameleons in Madagascar: insights into sexual selection. Herpetologica 65:54–69CrossRefGoogle Scholar
  29. Kelso EC, Verrell PA (2002) Do male veiled chameleons, Chamaeleo calyptratus, adjust their courtship displays in response to female reproductive status? Ethology 108:495–512CrossRefGoogle Scholar
  30. Koutnik DL (1980) Submissive signalling in mule deer. Anim Behav 28:312–313CrossRefGoogle Scholar
  31. Ligon RA, McGraw KJ (2013) Chameleons communicate with complex colour changes during contests: different body regions convey different information. Biol Lett 9:20130892PubMedCrossRefGoogle Scholar
  32. Lorenz K (1966) On aggression. Methuen, London.Google Scholar
  33. Matsumura S, Hayden TJ (2006) When should signals of submission be given?—a game theory model. J Theor Biol 240:425–433PubMedCrossRefGoogle Scholar
  34. Molles LE, Vehrencamp SL (2001) Songbird cheaters pay a retaliation cost: evidence for auditory conventional signals. Proc R Soc Lond B 268:2013–2019CrossRefGoogle Scholar
  35. Nečas P (1999) Chameleons: Nature’s hidden jewels. Chimaira, FrankfurtGoogle Scholar
  36. O’Connor KI, Metcalfe NB, Taylor AC (1999) Does darkening signal submission in territorial contests between juvenile Atlantic salmon, Salmo salar? Anim Behav 58:1269–1276PubMedCrossRefGoogle Scholar
  37. O’Connor KI, Metcalfe NM, Taylor AC (2000) Familiarity influences body darkening in territorial disputes between juvenile salmon. Anim Behav 59:1095–1101PubMedCrossRefGoogle Scholar
  38. Okelo O (1986) Neuroendocrine control of physiological color change in Chameleo gracilis. Gen Comp Endocrinol 64:305–311PubMedCrossRefGoogle Scholar
  39. Ott M, Schaeffel F (1995) A negatively powered lens in the chameleon. Nature 373:692–694PubMedCrossRefGoogle Scholar
  40. Øverli Ø, Harris CA, Winberg S (1999) Short-term effects of fights for social dominance and the establishment of dominant-subordinate relationships on brain monoamines and cortisol in rainbow trout. Brain Behav Evol 54:263–275PubMedCrossRefGoogle Scholar
  41. Peterson JA (1984) The locomotion of Chamaeleo (Reptilia: Sauria) with particular reference to the forelimb. J Zool (202: 1-42Google Scholar
  42. Pike TW (2011) Using digital cameras to investigate animal colouration: estimating sensor sensitivity functions. Behav Ecol Sociobiol 65:849–858CrossRefGoogle Scholar
  43. Qvarnstrom A, Forsgren E (1998) Should females prefer dominant males? Trends Ecol Evol 13:498–501PubMedCrossRefGoogle Scholar
  44. Schuett GW, Harlow HJ, Rose JD, Van Kirk EA, Murdoch WJ (1996) Levels of plasma corticosterone and testosterone in male copperheads (Agkistrodon contortrix) following staged fights. Horm Behav 30:60–68PubMedCrossRefGoogle Scholar
  45. Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko TS (2007) Using digital photography to study animal coloration. Biol J Linn Soc 90:211–237CrossRefGoogle Scholar
  46. Stuart-Fox D (2006) Testing game theory models: fighting ability and decision rules in chameleon contests. Proc R Soc Lond B 273:1555–1561CrossRefGoogle Scholar
  47. Stuart-Fox DM, Johnston GR (2005) Experience overrides colour in lizard contests. Behaviour 142:329–350CrossRefGoogle Scholar
  48. Stuart-Fox DM, Moussalli A (2008) Selection for social signalling drives the evolution of chameleon colour change. PLoS Biol 6:e25PubMedCentralPubMedCrossRefGoogle Scholar
  49. Stuart-Fox DM, Firth D, Moussalli A, Whiting MJ (2006) Multiple signals in chameleon contests: designing and analysing animal contests as a tournament. Anim Behav 71:1263–1271CrossRefGoogle Scholar
  50. Summers CH, Korzan WJ, Lukkes JL, Watt MJ, Forster GL, Øverli O, Höglund E, Larson ET, Ronan PJ, Matter JM, Summers TR, Renner KJ, Greenberg N (2005) Does serotonin influence aggression? Comparing regional activity before and during social interaction. Physiol Biochem Zool 78:679–694PubMedCrossRefGoogle Scholar
  51. Van Dyk DA, Evans CS (2008) Opponent assessment in lizards: examining the effect of aggressive and submissive signals. Behav Ecol 19:895–901CrossRefGoogle Scholar
  52. Walton BM, Bennett AF (1993) Temperature-dependent color change in Kenyan chameleons. Physiol Zool 66:270–287Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Life SciencesArizona State UniversityTempeUSA

Personalised recommendations