Coral Reefs

, Volume 32, Issue 3, pp 835–846 | Cite as

Morphology, sociality, and ecology: can morphology predict pairing behavior in coral reef fishes?

  • S. J. Brandl
  • D. R. Bellwood


Morphology can contain valuable information about the ecological performance of reef fishes, but it has rarely been used in combination with social traits. Social behavior is known to influence the ecological role of fishes; however, the ecological basis for pairing in reef fishes is not well understood. Field observations of 2,753 individuals, in 47 species in six families of biting reef fishes (Acanthuridae, Chaetodontidae, Kyphosidae, Labridae, Pomacanthidae, Siganidae), were used in combination with six morphological measurements, to examine the morphology of fishes in different social systems. A principal components analysis of morphological traits segregated species with high proportions of pairing individuals from non-pairing species along principal component 1, explaining 40.8 % of the variation. Pairing species were characterized by large eyes, concave foreheads, pointed snouts, deep bodies, and small maximum sizes. There was a significant positive relationship between these morphological traits (i.e., scores on PC1) and the prevalence of pairing within the Chaetodontidae (r 2 = 0.59; P = 0.026), Siganidae (r 2 = 0.72; P = 0.004), and Acanthuridae (r 2 = 0.82; P < 0.001). This was consistent when traits were corrected for phylogenetic effects. No pattern was evident in the scarine Labridae (r 2 = 0.15; P = 0.17). The morphological characteristics found among pairing species suggest that pairing species share common ecological traits, including foraging for small prey items in micro-topographically complex environments such as reef crevices. These ecological traits may have played a role in the evolution of pairing behavior and subsequently led to the development of reproductive patterns based on monogamy.


Pairing Ecomorphology Social system Reef fish Foraging ecology Functional morphology 



We wish to thank the staff of Lizard Island Research Station for field support; J. R. Hodge for statistical support; K. J. Nicolet, C. H. R. Goatley and J. Q. Welsh for field assistance; K. J. Nicolet, J. Q. Welsh, N. J. Marshall and four anonymous reviewers for helpful discussions and/or comments on earlier drafts of the manuscript. This work was supported by the Australian Research Council (DRB).

Supplementary material

338_2013_1042_MOESM1_ESM.docx (39 kb)
Supplementary material 1 (DOCX 38 kb)


  1. Alfaro ME, Janovetz J, Westneat MW (2001) Motor control across trophic strategies: muscle activity of biting and suction feeding fishes. Am Zool 41:1266–1279CrossRefGoogle Scholar
  2. Allen GR, Steene R, Allen M (1998) A guide to angelfishes and butterflyfishes. Odyssey Publishing, PerthGoogle Scholar
  3. Barlow GW (1987) Spawning, eggs and larvae of the longnose filefish Oxymonacanthus longirostris, a monogamous coralivore. Environ Biol Fish 20:183–194CrossRefGoogle Scholar
  4. Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fish 28:189–214CrossRefGoogle Scholar
  5. Bellwood DR, Wainwright PC (2001) Locomotion in labrid fishes: implications for habitat use and cross-shelf biogeography on the Great Barrier Reef. Coral Reefs 20:139–150CrossRefGoogle Scholar
  6. Berumen ML, Pratchett MS (2006) Effects of resource availability on the competitive behaviour of butterflyfishes (Chaetodontidae). Proc 10th Int Coral Reef Symp 644–650Google Scholar
  7. Berumen ML, Pratchett MS, McCormick MI (2005) Within-reef differences in diet and condition of butterflyfishes (Chaetodontidae). Mar Ecol Prog Ser 287:217–227CrossRefGoogle Scholar
  8. Beukers-Stewart BD, Jones GP (2004) The influence of prey abundance on the feeding ecology of two piscivorous species of coral reef fish. J Exp Mar Biol Ecol 299:155–184CrossRefGoogle Scholar
  9. Bonaldo RM, Bellwood DR (2011) Spatial variation in the effects of grazing on epilithic algal turfs on the Great Barrier Reef, Australia. Coral Reefs 30:381–390CrossRefGoogle Scholar
  10. Bonaldo RM, Krajewski JP, Sazima I (2005) Meals for two: foraging activity of the butterflyfish Chaetodon striatus (Perciformes) in southeast Brazil. Braz J Biol 65:211–215PubMedCrossRefGoogle Scholar
  11. Collar DC, Wainwright PC, Alfaro ME (2008) Integrated diversification of locomotion and feeding in labrid fishes. Biol Lett 4:84–86PubMedCrossRefGoogle Scholar
  12. DeMartini EE, Anderson TW, Friedlander AM, Beets JP (2011) Predator biomass, prey density, and species composition effects on group size in recruit coral reef fishes. Mar Biol 158:2437–2447CrossRefGoogle Scholar
  13. Dumay O, Tari PS, Tomasini JA, Mouillot D (2004) Functional groups of lagoon fish species in Languedoc Roussillon (South of France, Mediterranean Sea). J Fish Biol 64:970–983CrossRefGoogle Scholar
  14. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of the mating systems. Science 197:215–223PubMedCrossRefGoogle Scholar
  15. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 126:1–25CrossRefGoogle Scholar
  16. Fernald RD (1991) Teleost vision: seeing while growing. J Exp Zool S 5:167–180Google Scholar
  17. Ferry-Graham LA, Konow N (2010) The intramandibular joint in Girella: a mechanism for increased force production? J Morphol 271:271–279PubMedGoogle Scholar
  18. Ferry-Graham LA, Wainwright PC, Bellwood DR (2001a) Prey capture in long-jawed butterflyfishes (Chaetodontidae): the functional basis of novel feeding habits. J Exp Mar Biol Ecol 256:167–184PubMedCrossRefGoogle Scholar
  19. Ferry-Graham LA, Wainwright PC, Hulsey CD, Bellwood DR (2001b) Evolution and mechanics of long jaws in butterflyfishes (family Chaetodontidae). J Morphol 248:120–143PubMedCrossRefGoogle Scholar
  20. Ferry-Graham LA, Bolnick DI, Wainwright PC (2002a) Using functional morphology to examine the ecology and evolution of specialization. Integr Comp Biol 42:265–277PubMedCrossRefGoogle Scholar
  21. Ferry-Graham LA, Wainwright PC, Westneat MW, Bellwood DR (2002b) Mechanisms of benthic prey capture in wrasses (Labridae). Mar Biol 141:819–830CrossRefGoogle Scholar
  22. Ferry-Graham LA, Gibb AC, Hernandez LP (2008) Premaxillary movements in cyprinodontiform fishes: An unusual protrusion mechanism facilitates “picking” prey capture. Zoology 111:455–466PubMedCrossRefGoogle Scholar
  23. Fessler JL, Westneat MW (2007) Molecular phylogenetics of the butterflyfishes (Chaetodontidae): Taxonomy and biogeography of a global coral reef fish family. Mol Phylogenet Evol 45:50–68PubMedCrossRefGoogle Scholar
  24. Foster SA (1985) Group foraging by a coral reef fish: a mechanism for gaining access to defended resources. Anim Behav 33:782–792CrossRefGoogle Scholar
  25. Fouda MM, El-Sayed AM (1996) Distribution and feeding habits of two surgeonfish Zebrasoma xanthurum and Ctenochaetus striatus in the Gulf of Aqaba, Red Sea. J King Abdulaziz Univ Mar Sci 7:233–243CrossRefGoogle Scholar
  26. Fox RJ, Bellwood DR (2008) Remote video bioassays reveal the potential feeding impact of the rabbitfish Siganus canaliculatus (f: Siganidae) on an inner-shelf reef of the Great Barrier Reef. Coral Reefs 27:605–615CrossRefGoogle Scholar
  27. Fox RJ, Bellwood DR (2011) Unconstrained by the clock? Plasticity of diel activity rhythm in a tropical reef fish, Siganus lineatus. Funct Ecol 25:1096–1105CrossRefGoogle Scholar
  28. Fox RJ, Bellwood DR (2013) Niche partitioning of feeding microhabitats produces a unique function for herbivorous rabbitfishes (Perciformes, Siganidae) on coral reefs. Coral Reefs 32:13–23Google Scholar
  29. Fox RJ, Sunderland TL, Hoey AS, Bellwood DR (2009) Estimating ecosystem function: contrasting roles of closely related herbivorous rabbitfishes (Siganidae) on coral reefs. Mar Ecol Prog Ser 385:261–269CrossRefGoogle Scholar
  30. Froese R, Pauly D (eds) (2012) FishBase. World Wide Web electronic publication., version (08/2012)
  31. Fulton CJ (2007) Swimming speed performance in coral reef fishes: field validations reveal distinct functional groups. Coral Reefs 26:217–228CrossRefGoogle Scholar
  32. Fulton CJ, Bellwood DR (2002) Ontogenetic habitat use in labrid fishes: an ecomorphological perspective. Mar Ecol Prog Ser 236:255–262CrossRefGoogle Scholar
  33. Gardiner NM, Jones GP (2010) Synergistic effects of habitat preference and gregarious behaviour on habitat use in coral reef cardinalfish. Coral Reefs 29:845–856CrossRefGoogle Scholar
  34. Gerstner CL (1999) Maneuverabilty of four species of coral-reef fish that differ in body and pectoral-fin morphology. Can J Zool 77:1102–1110CrossRefGoogle Scholar
  35. Goatley CHR, Bellwood D (2009) Morphological structure in a reef fish assemblage. Coral Reefs 28:449–457CrossRefGoogle Scholar
  36. Gregson MA, Pratchett MS, Berumen ML, Goodman BA (2008) Relationships between butterflyfish (Chaetodontidae) feeding rates and coral consumption on the Great Barrier Reef. Coral Reefs 27:583–591CrossRefGoogle Scholar
  37. Guillemain M, Martin GR, Fritz H (2002) Feeding methods, visual fields and vigilance in dabbling ducks (Anatidae). Funct Ecol 16:522–529CrossRefGoogle Scholar
  38. Hernandez LP, Gibb AC, Ferry-Graham LA (2009) Trophic apparatus in Cyprinodontiform fishes: functional specializations for picking and scraping behaviors. J Morphol 270:645–661PubMedCrossRefGoogle Scholar
  39. Hourigan TF (1989) Environmental determinants of butterflyfish social-systems. Environ Biol Fish 25:61–78CrossRefGoogle Scholar
  40. Hutchinson GE (1957) Concluding remarks. Cold Spring Harbor Symposium on Quantitative Biology 22:415–427CrossRefGoogle Scholar
  41. Hutchinson GE (1959) Homage to Santa Rosalia, or why are there so many kinds of animals. Am Nat 93:145–159CrossRefGoogle Scholar
  42. Job SD, Bellwood DR (1996) Visual acuity and feeding in larval Premnas biaculeatus. J Fish Biol 48:952–963Google Scholar
  43. Johannes RE (1981) Words of the lagoon: Fishing and marine lore in the Palau district of Micronesia. University of California Press, Berkeley, CAGoogle Scholar
  44. Konow N, Bellwood DR (2005) Prey-capture in Pomacanthus semicirculatus (Teleostei, Pomacanthidae): functional implications of intramandibular joints in marine angelfishes. J Exp Biol 208:1421–1433PubMedCrossRefGoogle Scholar
  45. Konow N, Bellwood DR, Wainwright PG, Kerr AM (2008) Evolution of novel jaw joints promote trophic diversity in coral reef fishes. Biol J Linn Soc 93:545–555CrossRefGoogle Scholar
  46. Krause J, Godin JGJ (1996) Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey. Behav Ecol 7:264–271CrossRefGoogle Scholar
  47. Kuriiwa K, Naoto H, Tetsuo Y, Seishi K, Mutsumi N (2007) Phylogenetic relationships and natural hybridization in rabbitfishes (Teleostei: Siganidae) inferred from mitochondrial and nuclear DNA analyses. Mol Phylogenet Evol 45:69–80PubMedCrossRefGoogle Scholar
  48. Li KT, Wetterer JK, Hairston NG Jr (1985) Fish size, visual resolution and prey selectivity. Ecology 66:1729–1735CrossRefGoogle Scholar
  49. Madin EMP, Gaines SD, Warner RR (2010) Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology 91:3563–3571PubMedCrossRefGoogle Scholar
  50. Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS (2003) Visual biology of Hawaiian coral reef fishes: III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003:467–480CrossRefGoogle Scholar
  51. Martin GR, Katzir G (1999) Visual fields, foraging and binocularity in birds. In: Adams N, Slowtow R (eds) Proceedings of the 22nd International Ornithological Congress, Durban. Birdlife, Johannesburg, pp 2711–2728Google Scholar
  52. McComb DM, Kajiura SM (2008) Visual fields of four batoid fishes: a comparative study. J Exp Biol 211:482–490PubMedCrossRefGoogle Scholar
  53. Miller TJ, Crowder LB, Rice JA (1993) Ontogenetic changes in behavioural and histological measures of visual acuity in three species of fish. Environ Biol Fish 37:1–8CrossRefGoogle Scholar
  54. Mittelbach GG (1984) Predation and resource partitioning in two sunfishes (Centrarchidae). Ecology 65:499–513CrossRefGoogle Scholar
  55. Montgomery WL, Myrberg AA Jr, Fishelson L (1989) Feeding ecology of surgeonfishes (Acanthuridae) in the northern Red Sea, with particular reference to Acanthurus nigrofuscus (Forsskål). J Exp Mar Biol Ecol 132:179–207CrossRefGoogle Scholar
  56. Motta PJ (1988) Functional morphology of the feeding apparatus of ten species of Pacific butterflyfishes (Perciformes, Chaetodontidae): An ecomorphological approach. Environ Biol Fish 22:39–67CrossRefGoogle Scholar
  57. Motta PJ (1989) Dentition patterns among Pacific and Western Atlantic butterflyfishes (Perciformes, Chaetodontidae): relationship to feeding ecology and evolutionary history. Environ Biol Fish 25:159–170CrossRefGoogle Scholar
  58. Mouillot D, Dumay O, Tomasini JA (2007) Limiting similarity, niche filtering and functional diversity in coastal lagoon fish communities. Estuar Coast Shelf Sci 71:443–456CrossRefGoogle Scholar
  59. Osenberg CW, Mittelbach GG, Wainwright PC (1992) Two-stage life histories in fish — the interaction between juvenile competition and adult performance. Ecology 73:255–267CrossRefGoogle Scholar
  60. Overholtzer KL, Motta PL (2000) Effects of mixed-species foraging groups on the feeding and aggression of juvenile parrotfishes. Environ Biol Fish 58:345–354CrossRefGoogle Scholar
  61. Paul VJ, Nelson SG, Sanger HR (1990) Feeding preferences of adult and juvenile rabbitfish Siganus argenteus in relation to chemical defenses of tropical seaweeds. Mar Ecol Prog Ser 60:23–34CrossRefGoogle Scholar
  62. Persson A, Andersson J, Wahlstrom E, Eklov P (1996) Size specific interactions in lake systems: predator gape limitation and prey growth rate and mortality. Ecology 77:900–911CrossRefGoogle Scholar
  63. Pettigrew JD, Collin SP, Fritsches K (2000) Prey capture and accommodation in the sandlance, Limnichthytes fasciatus (Creediidae; Teleostei). J Comp Physiol 186:247–260CrossRefGoogle Scholar
  64. Popp JW (1988) Effects of food-handling time on scanning rates in American goldfinches. Auk 105:384–385CrossRefGoogle Scholar
  65. Pratchett MS (2005) Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar Biol 148:373–382CrossRefGoogle Scholar
  66. Pratchett MS, Pradjakusuma OA, Jones GP (2006) Is there a reproductive basis to solitary living versus pair-formation in coral reef fishes? Coral Reefs 25:85–92CrossRefGoogle Scholar
  67. Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. Crawford House Publishing Pty. Ltd., BathurstGoogle Scholar
  68. Reavis RH, Barlow GW (1998) Why is the coral-reef fish Valenciennea strigata (Gobiidae) monogamous? Behav Ecol Sociobiol 43:229–237CrossRefGoogle Scholar
  69. Reavis RH, Copus JM (2011) Monogamy in a feeding generalist, Chaetodon trichrous, the endemic Tahitian butterflyfish. Environ Biol Fish 92:167–179CrossRefGoogle Scholar
  70. Reese ES (1975) A comparative field study of the social behavior and related ecology of reef fishes of the family Chaetodontidae. Z Tierpsychol 37:37–61PubMedCrossRefGoogle Scholar
  71. Rice AN, Westneat MW (2005) Coordination of feeding, locomotor, and visual systems in parrotfishes (Teleostei: Labridae). J Exp Biol 208:3503–3518PubMedCrossRefGoogle Scholar
  72. Robertson DR (1983) On the spawning behavior and spawning cycle of eight surgeonfishes (Acanthuridae) from the Indo-Pacific. Environ Biol Fish 9:193–223CrossRefGoogle Scholar
  73. Robertson DR (1987) Responses of two coral reef toadfishes (Batrachoididae) to the demise of their primary prey, the sea urchin Diadema antillarum. Copeia 1987:637–642CrossRefGoogle Scholar
  74. Robertson DR, Gaines SD (1986) Interference competition structures habitat use in a local assemblage of coral reef surgeonfishes. Ecology 67:1372–1383CrossRefGoogle Scholar
  75. Robertson DR, Sweatman HPA, Fletcher EA, Cleland MG (1976) Schooling as a mechanism for circumventing the territoriality of competitors. Ecology 57:1208–1220CrossRefGoogle Scholar
  76. Robertson DR, Polunin NVC, Leighton K (1979) The behavioral ecology of three Indian Ocean surgeonfishes (Acanthurus lineatus, A. leucosternon, Zebrasoma scopas): their feeding strategies, and social and mating system. Environ Biol Fish 4:125–170CrossRefGoogle Scholar
  77. Robinson BW, Wilson DS, Margosian AS, Lotito PT (1993) Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evol Ecol 7:451–464CrossRefGoogle Scholar
  78. Russ G (1984) Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef. I. Levels of variability across the entire continental shelf. Mar Ecol Prog Ser 20:23–24CrossRefGoogle Scholar
  79. Ryer CH, Olla BL (1998) Shifting the balance between foraging and predator avoidance: the importance of food distribution for a schooling pelagic forager. Environ Biol Fish 52:467–475CrossRefGoogle Scholar
  80. Schmitz L, Wainwright PC (2011a) Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes. Coral Reefs 30:415–428CrossRefGoogle Scholar
  81. Schmitz L, Wainwright PC (2011b) Nocturnality constrains morphological and functional diversity in the eyes of reef fishes. BMC Evol Biol 11:338PubMedCrossRefGoogle Scholar
  82. Sogabe A, Matsumoto K, Yanagisawa Y (2007) Mate change reduces the reproductive rate of males in a monogamous pipefish Corythoichthys haematopterus: the benefit of long-term pair bonding. Ethology 113:764–771CrossRefGoogle Scholar
  83. Tamura T (1957) A study of visual perception in fish, especially on resolving power and accommodation. Bull Jap Soc Sci Fish 22:536–557CrossRefGoogle Scholar
  84. Wainwright PC (1988) Morphology and ecology: functional basis of feeding constraints in Caribbean labrid fishes. Ecology 69:635–645CrossRefGoogle Scholar
  85. Wainwright PC (1991) Ecomorphology: experimental functional anatomy for ecological problems. Am Zool 31:680–693Google Scholar
  86. Wainwright PC, Bellwood DR (2002) Ecomorphology of feeding in coral reef fishes. In: Sale PF (ed) Coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 33–55CrossRefGoogle Scholar
  87. Webb PW (1997) Swimming. In: Evans (ed) The physiology of fishes, 2nd edn. CRC Press, Marine Science Series, Boca Raton, pp 3–24Google Scholar
  88. Welsh JQ, Bellwood DR (2012) How far do schools of roving herbivores rove? A case study using Scarus rivulatus. Coral Reefs 31:991–1003CrossRefGoogle Scholar
  89. Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548CrossRefGoogle Scholar
  90. Wetterer JK (1989) Mechanisms of prey choice by planktivorous fish: perceptual constraints and rules of thumb. Anim Behav 37:955–967CrossRefGoogle Scholar
  91. White JW, Warner RR (2007a) Safety in numbers and the spatial scaling of density-dependent mortality in a coral reef fish. Ecology 88:3044–3054PubMedCrossRefGoogle Scholar
  92. White JW, Warner RR (2007b) Behavioral and energetic costs of group membership in a coral reef fish. Oecologia 154:423–433PubMedCrossRefGoogle Scholar
  93. Whiteman EA, Côté IM (2004) Monogamy in marine fishes. Biol Rev 79:351–375PubMedCrossRefGoogle Scholar
  94. Wickler W (1985) Coordination of vigilance in bird groups. The “Watchman’s song” hypothesis. Z Tierpsychol 69:250–253CrossRefGoogle Scholar
  95. Woodland DJ (1990) Revision of the fish family Siganidae with descriptions of two new species and comments on distribution and biology. Indo-Pacific Fishes 19. B.P. Bishop Museum, Honolulu, Hawaii, p 136Google Scholar
  96. Yabuta S (1997) Spawning migrations in the monogamous butterflyfish, Chaetodon trifasciatus. Ichthyol Res 44:177–182CrossRefGoogle Scholar
  97. Yabuta S (2007) Social groupings in 18 species of butterflyfish and pair bond weakening during the nonreproductive season. Ichthyol Res 54:207–210CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Australian Research Council Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia

Personalised recommendations