Coral Reefs

, Volume 36, Issue 2, pp 561–575 | Cite as

Relationships between structural complexity, coral traits, and reef fish assemblages

  • Emily S. Darling
  • Nicholas A. J. Graham
  • Fraser A. Januchowski-Hartley
  • Kirsty L. Nash
  • Morgan S. Pratchett
  • Shaun K. Wilson
Report

Abstract

With the ongoing loss of coral cover and the associated flattening of reef architecture, understanding the links between coral habitat and reef fishes is of critical importance. Here, we investigate whether considering coral traits and functional diversity provides new insights into the relationship between structural complexity and reef fish communities, and whether coral traits and community composition can predict structural complexity. Across 157 sites in Seychelles, Maldives, the Chagos Archipelago, and Australia’s Great Barrier Reef, we find that structural complexity and reef zone are the strongest and most consistent predictors of reef fish abundance, biomass, species richness, and trophic structure. However, coral traits, diversity, and life histories provided additional predictive power for models of reef fish assemblages, and were key drivers of structural complexity. Our findings highlight that reef complexity relies on living corals—with different traits and life histories—continuing to build carbonate skeletons, and that these nuanced relationships between coral assemblages and habitat complexity can affect the structure of reef fish assemblages. Seascape-level estimates of structural complexity are rapid and cost effective with important implications for the structure and function of fish assemblages, and should be incorporated into monitoring programs.

Keywords

Habitat diversity Species traits Functional ecology Reef architecture Scleractinian corals Coral reef fish 

Notes

Acknowledgements

We thank Sally Keith for providing species lists for Indo-Pacific provinces. ESD was supported by a David H. Smith Conservation Research Fellowship from the Cedar Tree Foundation, a Banting Fellowship from the Natural Sciences and Engineering Research Council of Canada, and the John D. and Catherine T. MacArthur Foundation. NAJG was supported by the Australian Research Council and a Royal Society University Research Fellowship. Field work in the Seychelles was supported by the Seychelles Fishing Authority, Seychelles National Parks Authority, Nature Seychelles, and Global Vision International. We thank the reviewers and Editor for suggestions that substantially improved earlier versions of this manuscript.

Supplementary material

338_2017_1539_MOESM1_ESM.docx (4.6 mb)
Supplementary material 1 (DOCX 4742 kb)

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723CrossRefGoogle Scholar
  2. Alvarez-Filip L, Carricart-Ganivet JP, Horta-Puga G, Iglesias-Prieto R (2013) Shifts in coral-assemblage composition do not ensure persistence of reef functionality. Sci Rep 3:3486CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alvarez-Filip L, Dulvy NK, Gill JA, Cote IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proc R Soc Lond B Biol Sci 276:3019–3025CrossRefGoogle Scholar
  4. Bartoń K (2016) MuMIn: multi-model inference. R package version 1(15):6Google Scholar
  5. Beets J, Hixon M (1989) Shelter characteristics and Caribbean fish assemblages: experiments with artificial reefs. Bull Mar Sci 44:666–680Google Scholar
  6. Bergman K, Ohman M, Svensson S (2000) Influence of habitat structure on Pomacentrus sulfureus, a western Indian Ocean reef fish. Environ Biol Fishes 59:243–252CrossRefGoogle Scholar
  7. Beukers JS, Jones GP (1997) Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia 114:50–59CrossRefGoogle Scholar
  8. Burnham KP, Anderson D (2002) Model selection and multimodel inference: a practical information-theoric approach. Springer, New York, NY, p 488Google Scholar
  9. Chabanet P, Ralambondrainy H, Amanieu M, Faure G, Galzin R (1997) Relationships between coral reef substrata and fish. Coral Reefs 16:93–102CrossRefGoogle Scholar
  10. Chong-Seng KM, Mannering TD, Pratchett MS, Bellwood DR, Graham NAJ (2012) The influence of coral reef benthic condition on associated fish assemblages. PLoS One 7:e42167CrossRefPubMedPubMedCentralGoogle Scholar
  11. Coker DJ, Wilson SK, Pratchett MS (2014) Importance of live coral habitat for reef fishes. Rev Fish Biol Fish 24:89–126CrossRefGoogle Scholar
  12. Collins DL, Langlois TJ, Bond T, Holmes TH, Harvey ES, Fisher R, McLean DL (2016) A novel stereo‐video method to investigate fish Holmes TH, Harvey ES, Fisher R, McLean DL (2016) A nove [DOI:  10.1111/2041-210X.12650]
  13. Darling ES, Alvarez-Filip L, Oliver TA, Mcclanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386CrossRefPubMedGoogle Scholar
  14. Darling ES, McClanahan TR, Côté IM (2013) Life histories predict coral community disassembly under multiple stressors. Glob Chang Biol 19:1930–1940CrossRefPubMedGoogle Scholar
  15. DeCarlo TM, Cohen AL, Barkley HC, Cobban Q, Young C, Shamberger KE, Brainard RE, Golbuu Y (2015) Coral macrobioerosion is accelerated by ocean acidification and nutrients. Geology 43:7–10CrossRefGoogle Scholar
  16. Facon M, Pinault M, Obura D, Pioch S, Pothin K, Bigot L, Garnier R, Quod J (2016) A comparative study of the accuracy and effectiveness of line and point intercept transect methods for coral reef monitoring in the southwestern Indian Ocean islands. Ecol Indic 60:1045–1055CrossRefGoogle Scholar
  17. Ferrari R, McKinnon D, He H, Smith R, Corke P, González-Rivero M, Mumby P, Upcroft B (2016) Quantifying multiscale habitat structural complexity: a cost-effective framework for underwater 3D modelling. Remote Sens (Basel) 8:113CrossRefGoogle Scholar
  18. Friedlander AM, Brown EK, Jokiel PL, Smith WR, Rodgers KS (2003) Effects of habitat, wave exposure, and marine protected area status on coral reef fish assemblages in the Hawaiian archipelago. Coral Reefs 22:291–305CrossRefGoogle Scholar
  19. Fulton CJ, Bellwood DR, Wainwright PC (2005) Wave energy and swimming performance shape coral reef fish assemblages. Proc R Soc Lond B Biol Sci 272:827–832CrossRefGoogle Scholar
  20. Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873CrossRefPubMedGoogle Scholar
  21. Graham NAJ, McClanahan TR (2013) The last call for marine wilderness? Bioscience 63:397–402CrossRefGoogle Scholar
  22. Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326CrossRefGoogle Scholar
  23. Graham NAJ, Chong-Seng KM, Huchery C, Januchowski-Hartley FA, Nash KL (2014) Coral reef community composition in the context of disturbance history on the Great Barrier Reef. Australia. PLoS One 9:e101204CrossRefPubMedGoogle Scholar
  24. Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97CrossRefPubMedGoogle Scholar
  25. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci U S A 103:8425–8429CrossRefPubMedPubMedCentralGoogle Scholar
  26. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Robinson J, Bijoux JP, Daw TM (2007) Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries, and ecosystems. Conserv Biol 21:1291–1300CrossRefPubMedGoogle Scholar
  27. Gratwicke B, Speight MR (2005) The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J Fish Biol 66:650–667CrossRefGoogle Scholar
  28. Harris A, Wilson S, Graham N, Sheppard C (2014) Scleractinian coral communities of the inner Seychelles 10 years after the 1998 mortality event. Aquat Conserv Mar Freshw Ecosyst 24:667–679CrossRefGoogle Scholar
  29. Hicks CC, Cinner JE (2014) Social, institutional, and knowledge mechanisms mediate diverse ecosystem service benefits from coral reefs. Proc Natl Acad Sci U S A 111:17791–17796CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hixon M, Beets J (1993) Predation, prey refuges, and the structure of coral reef fish assemblages. Ecol Monogr 63:77–101CrossRefGoogle Scholar
  31. Hoegh-Guldberg O, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefPubMedGoogle Scholar
  32. Holbrook SJ, Schmitt RJ, Brooks AJ (2008) Resistance and resilience of a coral reef fish community to changes in coral cover. Mar Ecol Prog Ser 371:263–271CrossRefGoogle Scholar
  33. Holbrook SJ, Schmitt RJ, Messmer V, Brooks AJ, Srinivasan M, Munday PL, Jones GP (2015) Reef fishes in biodiversity hotspots are at greatest risk from loss of coral species. PLoS One 10:e0124054CrossRefPubMedPubMedCentralGoogle Scholar
  34. Houk P, Musburger C (2013) Trophic interactions and ecological stability across coral reefs in the Marshall Islands. Mar Ecol Prog Ser 488:23–34CrossRefGoogle Scholar
  35. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642CrossRefPubMedGoogle Scholar
  36. Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145–159CrossRefGoogle Scholar
  37. Johansen JL, Bellwood DR, Fulton CJ (2008) Coral reef fishes exploit flow refuges in high-flow habitats. Mar Ecol Prog Ser 60:219–226CrossRefGoogle Scholar
  38. Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci U S A 101:8251–8253CrossRefPubMedPubMedCentralGoogle Scholar
  39. Keith SA, Baird AH, Hughes TP, Madin JS, Connolly SR (2013) Faunal breaks and species composition of Indo-Pacific corals: the role of plate tectonics, environment and habitat distribution. Proc R Soc Lond B Biol Sci 280:20130818CrossRefGoogle Scholar
  40. Kerry JT, Bellwood DR (2012) The effect of coral morphology on shelter selection by coral reef fishes. Coral Reefs 31:415–424CrossRefGoogle Scholar
  41. Kerry JT, Bellwood DR (2015) Do tabular corals constitute keystone structures for fishes on coral reefs? Coral Reefs 34:41–50CrossRefGoogle Scholar
  42. Kitahara MV, Fukami H, Benzoni F, Huang D (2016) The new systematics of Scleractinia: integrating molecular and morphological evidence. In: Goffredo S, Dubinsky Z (eds) The Cnidaria, Past, Present and Future. Springer, Netherlands, pp 41–59CrossRefGoogle Scholar
  43. Kleypas J, Buddemeier RW, Gattuso J-P (2001) The future of coral reefs in an age of global change. Int J Earth Sci 90:426–437CrossRefGoogle Scholar
  44. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305CrossRefPubMedGoogle Scholar
  45. Luckhurst E, Luckhurst K (1978) Analysis of the influence of substrate variables on coral reef fish communities. Mar Biol 323:317–323CrossRefGoogle Scholar
  46. MacNeil MA, Graham NAJ, Cinner JE, Wilson SK, Williams ID, Maina J, Newman S, Friedlander AM, Jupiter S, Polunin NVC, McClanahan TR (2015) Recovery potential of the world’s coral reef fishes. Nature 520:341–344CrossRefPubMedGoogle Scholar
  47. Madin EMP, Gaines SD, Madin JS, Warner RR (2010) Fishing indirectly structures macroalgal assemblages by altering herbivore behavior. Am Nat 176:785–801CrossRefPubMedGoogle Scholar
  48. Madin JS, Hoogenboom MO, Connolly SR, Darling ES, Falster D, Huang D, Keith SA, Mizerek T, Pandolfi JM, Putnam HM, Baird AH (2016a) A trait-based approach to advance coral reef science. Trends Ecol Evol 31:419–428CrossRefPubMedGoogle Scholar
  49. Madin JS, Anderson K, Andreason M, Bridge TCL, Cairns S, Connolly SR, Darling ES, Diaz M, Falster D, Franklin EC, Gates RD, Hoogenboom MO, Huang D, Keith SA, Kosnik M, Kuo C-Y, Lough JM, Lovelock CE, Luiz O, Martinelli J, Mizerek T, Pandolfi JM, Pochon X, Putnam HM, Pratchett MS, Roberts E, Stat M, Wallace CC, Widman E, Baird AH (2016b) The Coral Trait Database, a curated database of trait information for coral species from the global oceans. Sci Data 3:160012CrossRefGoogle Scholar
  50. Manzello DP, Kleypas JA, Budd DA, Eakin CM, Glynn PW, Langdon C (2008) Poorly cemented coral reefs of the eastern tropical Pacific: possible insights into reef development in a high-CO2 world. Proc Natl Acad Sci U S A 105:10450–10455CrossRefPubMedPubMedCentralGoogle Scholar
  51. McClanahan TR, Graham NAJ, MacNeil MA, Muthiga NA, Cinner JE, Bruggemann JH, Wilson SK (2011) Critical thresholds and tangible targets for ecosystem-based management of coral reef fisheries. Proc Natl Acad Sci U S A 108:17230–17233CrossRefPubMedPubMedCentralGoogle Scholar
  52. McCormick M (1994) Comparison of field methods for measuring surface topography and their associations with a tropical reef fish assemblage. Mar Ecol Prog Ser 112:87–96CrossRefGoogle Scholar
  53. Messmer V, Jones GP, Munday PL, Holbrook SJ, Schmitt RJ, Brooks AJ (2011) Habitat biodiversity as a determinant of fish community structure on coral reefs. Ecology 92:2285–2298CrossRefPubMedGoogle Scholar
  54. Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177CrossRefPubMedGoogle Scholar
  55. Nash KL, Graham NAJ, Wilson SK, Bellwood DR (2012) Cross-scale habitat structure drives fish body size distributions on coral reefs. Ecosystems 16:478–490CrossRefGoogle Scholar
  56. Newman SP, Meesters EH, Dryden CS, Williams SM, Sanchez C, Mumby PJ, Polunin NVC (2015) Reef flattening effects on total richness and species responses in the Caribbean. J Anim Ecol 84:1678–1689CrossRefPubMedGoogle Scholar
  57. Noonan SHC, Jones GP, Pratchett MS (2012) Coral size, health and structural complexity: effects on the ecology of a coral reef damselfish. Mar Ecol Prog Ser 456:127–137CrossRefGoogle Scholar
  58. Perry CT, Murphy GN, Graham NAJ, Wilson SK, Januchowski-Hartley FA, East HK (2015) Remote coral reefs can sustain high growth potential and may match future sea-level trends. Sci Rep 5:18289CrossRefPubMedPubMedCentralGoogle Scholar
  59. Pinheiro J, Bates D, DebRoy S, Sarkar D (2015) nlme: linear and nonlinear mixed effects models. R package version 3.1-120Google Scholar
  60. Pittman SJ, Costa BM, Battista TA (2009) Using lidar bathymetry and boosted regression trees to predict the diversity and abundance of fish and corals. J Coast Res 10053:27–38CrossRefGoogle Scholar
  61. Polunin NVC, Roberts CM (1993) Greater biomass and value of target coral-reef fishes in two small Caribbean marine reserves. Mar Ecol Prog Ser 100:167–176CrossRefGoogle Scholar
  62. Pratchett M, Anderson K, Hoogenboom M, Widman E, Baird A, Pandolfi J, Edmunds P, Lough J (2015) Spatial, temporal and taxonomic variation in coral growth—implications for the structure and function of coral reef ecosystems. Oceanogr Mar Biol Annu Rev 53:215–296CrossRefGoogle Scholar
  63. Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  64. Roberts CM, Ormond RFG (1987) Habitat complexity and coral reef fish diversity and abundance on Red Sea fringing reefs. Mar Ecol Prog Ser 41:1–8CrossRefGoogle Scholar
  65. Rogers A, Blanchard JL, Mumby PJ (2014) Vulnerability of coral reef fisheries to a loss of structural complexity. Curr Biol 24:1000–1005CrossRefPubMedGoogle Scholar
  66. Sommer B, Harrison PL, Beger M, Pandolfi JM (2014) Trait-mediated environmental filtering drives assembly at biogeographic transition zones. Ecology 95:1000–1009CrossRefPubMedGoogle Scholar
  67. Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011) Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanogr Mar Biol Annu Rev 49:43–104Google Scholar
  68. Syms C, Jones GP (2000) Disturbance, habitat structure, and the dynamics of a coral-reef fish community. Ecology 81:2714–2729CrossRefGoogle Scholar
  69. Trebilco R, Baum JK, Salomon AK, Dulvy NK (2013) Ecosystem ecology: size-based constraints on the pyramids of life. Trends Ecol Evol 28:423–431CrossRefPubMedGoogle Scholar
  70. Williams GJ, Gove JM, Eynaud Y, Zgliczynski BJ, Sandin SA (2015) Local human impacts decouple natural biophysical relationships on Pacific coral reefs. Ecography 38:751–761CrossRefGoogle Scholar
  71. Wilson SK, Graham NAJ, Polunin NVC (2007) Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Mar Biol 151:1069–1076CrossRefGoogle Scholar
  72. Wilson SK, Depczynski M, Fulton CJ, Holmes TH, Radford BT, Tinkler P (2016) Influence of nursery microhabitats on the future abundance of a coral reef fish. Proc R Soc Lond B Biol Sci 283:20160903CrossRefGoogle Scholar
  73. Wilson SK, Babcock RC, Fisher R, Holmes TH, Moore JY, Thomson DP (2012) Relative and combined effects of habitat and fishing on reef fish communities across a limited fishing gradient at Ningaloo. Mar Environ Res 81:1–11CrossRefPubMedGoogle Scholar
  74. Wilson SK, Dolman AM, Cheal AJ, Emslie M, Pratchett MS, Sweatman HPA (2009) Maintenance of fish diversity on disturbed coral reefs. Coral Reefs 28:3–14CrossRefGoogle Scholar
  75. Wilson SK, Fisher R, Pratchett MS, Graham NAJ, Dulvy NK, Turner RA, Cakacaka A, Polunin NVC (2010) Habitat degradation and fishing effects on the size structure of coral reef fish communities. Ecol Appl 20:442–451CrossRefPubMedGoogle Scholar
  76. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14CrossRefGoogle Scholar
  77. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed-effects models and extensions in ecology with R. Springer, New York, NYCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Emily S. Darling
    • 1
    • 2
  • Nicholas A. J. Graham
    • 3
    • 4
  • Fraser A. Januchowski-Hartley
    • 5
  • Kirsty L. Nash
    • 6
    • 7
  • Morgan S. Pratchett
    • 4
  • Shaun K. Wilson
    • 8
    • 9
  1. 1.Marine Program, Wildlife Conservation SocietyBronxUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada
  3. 3.Lancaster Environment CentreLancaster UniversityLancasterUK
  4. 4.ARC Centre for Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  5. 5.IRD UMR 9190 MARBEC, IRD-CNRS-IFREMER-UMUniversité de MontpellierMontpellierFrance
  6. 6.Centre for Marine SocioecologyHobartAustralia
  7. 7.Institute of Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia
  8. 8.Marine Science Program, Department of Parks and WildlifeKensingtonAustralia
  9. 9.Oceans InstituteUniversity of Western AustraliaCrawleyAustralia

Personalised recommendations