Behavioral Ecology and Sociobiology

, Volume 70, Issue 1, pp 99–109 | Cite as

Metabolism, oxidative stress and territorial behaviour in a female colour polymorphic cichlid fish

  • Peter D. Dijkstra
  • Michele E.R. Pierotti
  • Ole Seehausen
  • Neil B. Metcalfe
Original Article


Intrasexual selection on body coloration is thought to play an important role in the evolution of colour polymorphism, but its physiological underpinnings have received limited attention. In the colour polymorphic cichlid Neochromis omnicaeruleus, three fully sympatric female colour morphs—a plain morph (P) and two conspicuously coloured blotched morphs, black-and-white blotched (WB) and orange blotched (OB)—differ in agonistic behaviour. We compared routine metabolic rate (when females were housed in social isolation), short-term energetic costs of interacting with a same-colour rival housed in an adjacent transparent chamber and oxidative stress between the three female colour morphs. WB females had a lower routine metabolic rate compared with the other colour morphs. WB females also had a lower active metabolic rate during inter-female interactions than OB females, while OB females used more oxygen per unit aggressive act than the other two colour morphs. However, there were no consistent differences in oxidative stress between the three morphs. Concerted divergence in colour, behaviour and metabolism might contribute to the evolution of these polymorphisms in sympatry.


Metabolic costs Oxidative stress Female-female competition Sexual selection Cichlid fish Lake Victoria 



Graham Law, John Laurie, Graham Adam and Alister Kirk helped maintain fish populations in Glasgow. We thank David Bailey for lending his respirometer equipment, technical assistance and discussions. We thank two anonymous reviewers for their useful comments on earlier versions of the manuscript. The research was supported by a postdoctoral fellowship from NWO (Rubicon-grant) and a Marie Curie Fellowship grant to PDD and NERC grant NE.K00400X/1 to NBM, who was also funded by ERC Advanced Grant 332784 during the writing of this paper.

Compliance with ethical standards

All experiments were carried out under UK Home Office Project License PPL 60/3625. from the University of Glasgow and complied with current laws in The UK.


  1. Baerends GP, Baerends-van Roon JM (1950) An introduction to the study of the ethology of cichlid fishes. Behav Suppl 1:233–366Google Scholar
  2. Bagni M, Civitareale C, Priori A, Ballerini A, Finoia M, Brambilla G, Marino G (2007) Pre-slaughter crowding stress and killing procedures affecting quality and welfare in sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata). Aquaculture 263:52–60CrossRefGoogle Scholar
  3. Beamonte-Barrientos R, Verhulst S (2013) Plasma reactive oxygen metabolites and non-enzymatic antioxidant capacity are not affected by an acute increase of metabolic rate in zebra finches. J Comp Physiol B 183:675–83PubMedCrossRefGoogle Scholar
  4. Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399CrossRefGoogle Scholar
  5. Bittner TD, King RB, Kerfin JM (2002) Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis). Copeia 2002:477–482CrossRefGoogle Scholar
  6. Borowsky R (1984) The evolutionary genetics of Xiphophorus. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum Press, New York, pp 235–310CrossRefGoogle Scholar
  7. Brambilla G, Civitareale C, Ballerini A et al (2002) Response to oxidative stress as a welfare parameter in swine. Redox Rep 7:159–163PubMedCrossRefGoogle Scholar
  8. Briffa M, Sneddon LU (2007) Physiological constraints on contest behaviour. Funct Ecol 21:627–637CrossRefGoogle Scholar
  9. Brooks R (2000) Negative genetic correlation between male sexual attractiveness and survival. Nature 406:67–70PubMedCrossRefGoogle Scholar
  10. Brown JH, Ross B, McCauley S, Dance S, Taylor AC, Huntingford FA (2003) Resting metabolic rate and social status in juvenile giant freshwater prawns, Macrobrachium rosenbergii. Mar Freshw Behav Physiol 36:31–40CrossRefGoogle Scholar
  11. Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc Lond B 278:3465–3473CrossRefGoogle Scholar
  12. Careau V, Thomas D, Humphries MM, Reale D (2008) Energy metabolism and animal personality. Oikos 117:641–653CrossRefGoogle Scholar
  13. Castro N, Ros RFH, Becker K, Oliveira RF (2006) Metabolic costs of aggressive behaviour in the Siamese fighting fish, Betta splendens. Aggress Behav 32:474–480CrossRefGoogle Scholar
  14. Chapman LJ, Nordlie FG, Seifert A (2002) Respiratory oxygen consumption among groups of Pseudocrenilabrus multicolor victoriae subjected to different oxygen concentrations during development. J Fish Biol 61:242–251CrossRefGoogle Scholar
  15. Cole GL, Endler JA (2015) Variable environmental effects on a multicomponent sexually selected Trait. Am Nat 185:452–468PubMedCrossRefGoogle Scholar
  16. Costantini D, Casagrande S, De Filippis S, Brambilla G, Fanfani A, Tagliavini J, Dell'Omo G (2006) Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176:329–337PubMedCrossRefGoogle Scholar
  17. Costantini D, Monaghan P, Metcalfe NB (2013) Loss of integration is associated with reduced resistance to oxidative stress. J Exp Biol 216:2213–2220PubMedCrossRefGoogle Scholar
  18. Cutts CJ, Metcalfe NB, Taylor AC (1998) Aggression and growth depression in juvenile Atlantic salmon: the consequences of individual variation in standard. J Fish Biol 44:1026–1037CrossRefGoogle Scholar
  19. Dijkstra PD, Groothuis TGG (2011) Male-male competition as a force in evolutionary diversification: evidence in haplochromine cichlid fish. Int J Evol Biol 2011:689254PubMedPubMedCentralCrossRefGoogle Scholar
  20. Dijkstra PD, Hekman R, Schulz RW, Groothuis TGG (2006) Social stimulation, nuptial colouration, androgens and immunocompetence in a sexual dimorphic cichlid fish. Behav Ecol Sociobiol 61:599–609CrossRefGoogle Scholar
  21. Dijkstra PD, Lindström J, Metcalfe NB, Hemelrijk CK, Brendel M, Seehausen O, Groothuis TGG (2010) Frequency-dependent social dominance in a color polymorphic cichlid fish. Evolution 64:2797–2807PubMedGoogle Scholar
  22. Dijkstra PD, Seehausen O, Groothuis TGG (2005) Direct male-male competition can facilitate invasion of new colour types in Lake Victoria cichlids. Behav Ecol Sociobiol 58:136–143CrossRefGoogle Scholar
  23. Dijkstra PD, Seehausen O, Groothuis TGG (2008) Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish. Proc R Soc Lond B 275:519–526CrossRefGoogle Scholar
  24. Dijkstra PD, Seehausen O, Metcalfe NB (2013) Metabolic divergence between sibling species of cichlids Pundamilia nyererei and Pundamilia pundamilia. J Fish Biol 82:1975–1989PubMedCrossRefGoogle Scholar
  25. Dijkstra PD, van Dijk S, Groothuis TGG, Pierotti MER, Seehausen O (2009) Behavioral dominance between female color morphs of a Lake Victoria cichlid fish. Behav Ecol 20:593–600CrossRefGoogle Scholar
  26. Dijkstra PD, Wiegertjes GF, Forlenza M, van der Sluijs I, Hofmann HA, Metcalfe NB, Groothuis TGG (2011) The role of physiology in the divergence of two incipient cichlid species. J Evol Biol 24:2639–2652PubMedCrossRefGoogle Scholar
  27. Ducrest A-L, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510PubMedCrossRefGoogle Scholar
  28. Emaresi G, Ducrest A-L, Bize P, Richter H, Simon C, Roulin A (2013) Pleiotropy in the melanocortin system: expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco). Mol Ecol 22:4915–4930PubMedCrossRefGoogle Scholar
  29. Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91CrossRefGoogle Scholar
  30. Fan S, Elmer KR, Meyer A (2012) Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and Neotropical lineages. Philos T Roy Soc B 367:385–394CrossRefGoogle Scholar
  31. Figueiredo-Silva AC, Saravanan S, Schrama JW, Panserat S, Kaushik S, Geurden I (2013) A comparative study of the metabolic response in rainbow trout and Nile tilapia to changes in dietary macronutrient composition. Br J Nutr 109:816–826PubMedCrossRefGoogle Scholar
  32. Finkel T, Holbrook NJ (2000) biology of ageing. Nature 408:239–247PubMedCrossRefGoogle Scholar
  33. Fletcher QE, Selman C, Boutin S et al (2013) Oxidative damage increases with reproductive energy expenditure and is reduced by food-supplementation. Evolution 67:1527–1536PubMedPubMedCentralGoogle Scholar
  34. Galván I, Gangoso L, Grande JM, Negro JJ, Rodríguez A, Figuerola J, Alonso-Alvarez C (2010) Antioxidant machinery differs between melanic and light nestlings of two polymorphic raptors. PLoS ONE 5, e13369PubMedPubMedCentralCrossRefGoogle Scholar
  35. Garratt M, Brooks RC (2012) Oxidative stress and condition-dependent sexual signals: more than just seeing red. Proc R Soc Lond B 279:3121–3130CrossRefGoogle Scholar
  36. Genner MJ, Turner GF (2005) The mbuna cichlids of Lake Malawi: a model for rapid speciation and adaptive radiation. Fish Fish 6:1–34CrossRefGoogle Scholar
  37. Grantner A, Taborsky M (1998) The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae). J Comp Physiol B 427–433Google Scholar
  38. Gray SM, Dill LM, Tantu FY et al (2008) Environment-contingent sexual selection in a colour polymorphic fish. Proc R Soc Lond B 275:1785–1791CrossRefGoogle Scholar
  39. Gray SM, McKinnon JS (2007) Linking color polymorphism maintenance and speciation. Trends Ecol Evol 22:71–79PubMedCrossRefGoogle Scholar
  40. Grether GF, Losin N, Anderson CN, Okamoto K (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev Camb Philos 84:617–635CrossRefGoogle Scholar
  41. Handelsman CA, Broder ED, Dalton CM, Ruell EW, Myrick CA, Reznick DN, Ghalambor CK (2013) Predator-induced phenotypic plasticity in metabolism and rate of growth: Rapid adaptation to a novel environment. Integr Comp Biol 53:975–988PubMedCrossRefGoogle Scholar
  42. Herskin J (1999) Effects of social and visual contact on the oxygen consumption of juvenile sea bass measured by computerized intermittent respirometry. J Fish Biol 55:1075–1085CrossRefGoogle Scholar
  43. Horth L (2003) Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki). Proc R Soc Lond B 270:1033–1040CrossRefGoogle Scholar
  44. Huffman LS, Mitchell MM, O’Connell LA, Hofmann HA (2012) Rising StARs: Behavioral, hormonal, and molecular responses to social challenge and opportunity. Horm Behav 61:631–641PubMedCrossRefGoogle Scholar
  45. Hughes KA, Houde AE, Price AC, Rodd FH (2013) Mating advantage for rare males in wild guppy populations. Nature 503:108–110PubMedCrossRefGoogle Scholar
  46. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5:288–298PubMedCrossRefGoogle Scholar
  47. Lahti K, Huuskonen H, Laurila A, Piironen J (2002) Metabolic rate and aggressiveness between Brown Trout. Funct Ecol 167–174Google Scholar
  48. Lande R, Seehausen O, van Alphen JJ (2001) Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112–113:435–443PubMedCrossRefGoogle Scholar
  49. Lehtonen TK (2014) Colour biases in territorial aggression in a Neotropical cichlid fish. Oecologia 175:85–93PubMedCrossRefGoogle Scholar
  50. Li Q, Clarke JA, Gao K-Q et al (2014) Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Nature 507:350–353PubMedCrossRefGoogle Scholar
  51. Maan ME, Eshuis B, Haesler MP et al (2008) Color polymorphism and predation in a Lake Victoria cichlid fish. Copeia 2008:621–629CrossRefGoogle Scholar
  52. Maan ME, Sefc KM (2013) Colour variation in cichlid fish: developmental mechanisms, selective pressures and evolutionary consequences. Semin Cell Dev Biol 24:516–528PubMedPubMedCentralCrossRefGoogle Scholar
  53. Magalhaes IS, Mwaiko S, Seehausen O (2010) Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria. Mol Ecol 19:3285–3300PubMedCrossRefGoogle Scholar
  54. Majerus MEN (1998) Melanism. Oxford University Press, Oxford, Evolution in actionGoogle Scholar
  55. Manceau M, Domingues VS, Mallarino R, Hoekstra HE (2011) The developmental role of Agouti in color pattern evolution. Science 331:1062–1065PubMedCrossRefGoogle Scholar
  56. Marras S, Claireaux G, McKenzie DJ, Nelson JA (2010) Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax. J Exp Biol 213:26–32PubMedCrossRefGoogle Scholar
  57. McCarthy I (2000) Temporal repeatability of relative standard metabolic rate in juvenile Atlantic salmon and its relation to life history variation. J Fish Biol 57:224–238CrossRefGoogle Scholar
  58. McKinnon JS, Pierotti MER (2010) Colour polymorphism and correlated characters: genetic mechanisms and evolution. Mol Ecol 19:5101–5125PubMedCrossRefGoogle Scholar
  59. McLean CA, Stuart-Fox D (2014) Geographic variation in animal colour polymorphisms and its role in speciation. Biol Rev Camb Philos 89:860–873CrossRefGoogle Scholar
  60. Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996CrossRefGoogle Scholar
  61. Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim Behav 49:431–436CrossRefGoogle Scholar
  62. Meyer CI, Kaufman R, Cech JJ (2006) Melanin pattern morphs do not differ in metabolic rate: implications for the evolutionary maintenance of a melanophore polymorphism in the green swordtail, Xiphophorus helleri. Naturwissenschaften 93:495–499PubMedCrossRefGoogle Scholar
  63. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92PubMedCrossRefGoogle Scholar
  64. Pierotti MER, Knight ME, Immler S et al (2008) Individual variation in male mating preferences for female coloration in a polymorphic cichlid fish. Behav Ecol 19:483–488CrossRefGoogle Scholar
  65. Pierotti MER, Martín-Fernández JA, Seehausen O (2009) Mapping individual variation in male mating preference space: multiple choice in a color polymorphic cichlid fish. Evolution 63:2372–2388PubMedCrossRefGoogle Scholar
  66. Pierotti MER, Seehausen O (2007) Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids. J Evol Biol 20:240–248PubMedCrossRefGoogle Scholar
  67. Pryke SR (2007) Fiery red heads: female dominance among head color morphs in the Gouldian finch. Behav Ecol 18:621–627CrossRefGoogle Scholar
  68. Roberts RB, Ser JR, Kocher TD (2009) Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326:998–1001PubMedPubMedCentralCrossRefGoogle Scholar
  69. Ros AFH, Becker K, Canário AVM, Oliveira RF (2004) Androgen levels and energy metabolism in Oreochromis mossambicus. J Fish Biol 65:895–905CrossRefGoogle Scholar
  70. Røskaft E, Järvi T, Bakken M et al (1986) The relationship between social status and resting metabolic rate in great tits (Parus major) and pied flycatchers (Ficedula hypoleuca). Anim Behav 34:838–842CrossRefGoogle Scholar
  71. Roulin A (2004) The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev Camb Philos 79:815–848CrossRefGoogle Scholar
  72. Saino N, Scatizzi L (1991) Selective aggressiveness and dominance among carrion crows, hooded crows and hybrids. B Zool 58:255–260CrossRefGoogle Scholar
  73. Salin K, Auer SK, Rey B, Selman C, Metcalfe NB (2015) Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance. Proc R Soc B 282:20151028Google Scholar
  74. Salin K, Luquet E, Rey B et al (2012) Alteration of mitochondrial efficiency affects oxidative balance, development and growth in frog (Rana temporaria) tadpoles. J Exp Biol 215:863–869PubMedCrossRefGoogle Scholar
  75. Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56PubMedCrossRefGoogle Scholar
  76. Seebacher F, Ward AJW, Wilson RS (2013) Increased aggression during pregnancy comes at a higher metabolic cost. J Exp Biol 216:771–776PubMedCrossRefGoogle Scholar
  77. Seehausen O (1996) Lake Victoria rock cichlids. Taxonomy, ecology and distribution. Cichlid Press, Zevenhuizen, NLGoogle Scholar
  78. Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. Proc R Soc Lond B 273:1987–1998CrossRefGoogle Scholar
  79. Seehausen O, Schluter D (2004) Male-male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc R Soc Lond B 271:1345–1353CrossRefGoogle Scholar
  80. Seehausen O, van Alphen JJM, Lande R (1999) Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection. Ecol Lett 2:367–378CrossRefGoogle Scholar
  81. Sinervo B, Calsbeek R (2006) The developmental, physiological, neural, and genetical causes and consequences of frequency-dependent selection in the wild. Annu Rev Ecol Evol Syst 37:581–610CrossRefGoogle Scholar
  82. Speakman JR, Selman C (2003) Physical activity and resting metabolic rate. Proc Nutr Soc 62:621–634PubMedCrossRefGoogle Scholar
  83. Steffensen JF, Johansen K, Bushnell PG (1984) An automated swimming respirometer. Comp Biochem Phys A 79:437–440CrossRefGoogle Scholar
  84. Watson P, Lighton JRB (1994) Sexual selection and the energetics of copulatory courtship in the Sierra dome spider, Linyphia litigiosa. Anim Behav 48:615–626CrossRefGoogle Scholar
  85. West-Eberhard MJ (1979) Sexual selection, social competition, and evolution. Proc Am Philos Soc 123:222–234Google Scholar
  86. Wong BBM, Candolin U (2005) How is female mate choice affected by male competition? Biol Rev Camb Philos 80:559–571CrossRefGoogle Scholar
  87. Yamamoto T, Ueda H, Higashi S (1998) Correlation among dominance status, metabolic rate and otolith size in masu salmon. J Fish Biol 52:281–290CrossRefGoogle Scholar
  88. Zhang C, Song Y, Thompson DA et al (2010) Pineal-specific agouti protein regulates teleost background adaptation. Proc Natl Acad Sci U S A 107:20164–20171PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Peter D. Dijkstra
    • 1
    • 2
  • Michele E.R. Pierotti
    • 3
    • 4
    • 5
  • Ole Seehausen
    • 3
    • 4
  • Neil B. Metcalfe
    • 1
  1. 1.Institute of Biodiversity, Animal Health and Comparative Medicine, Graham Kerr Building, College of Medical, Veterinary and Life SciencesUniversity of GlasgowGlasgowUK
  2. 2.Department of BiologyCentral Michigan UniversityMount PleasantUSA
  3. 3.Centre of Ecology, Evolution and BiogeochemistryEawag Swiss Federal Institute for Aquatic SciencesKastanienbaumSwitzerland
  4. 4.Institute of Ecology and Evolution, Division Aquatic Ecology and EvolutionUniversity of BernBernSwitzerland
  5. 5.Smithsonian Tropical Research InstitutePanamaRepublic of Panama

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