Marine Biology

, Volume 161, Issue 11, pp 2597–2607 | Cite as

Seasonal changes in habitat structure underpin shifts in macroalgae-associated tropical fish communities

  • S. K. WilsonEmail author
  • C. J. Fulton
  • M. Depczynski
  • T. H. Holmes
  • M. M. Noble
  • B. Radford
  • P. Tinkler
Original Paper


Habitat shifts play an important role in structuring faunal assemblages; however, research has focused on the influence of random disturbance events and information on how regular seasonal changes to habitat affect marine fauna remains largely unexplored, especially in the tropics. We recorded seasonal changes in the structure of tropical macroalgae fields within the Ningaloo lagoon (Western Australia) and related this to the density, biomass and species richness of fishes that represent key processes: juveniles, predators of juveniles and herbivores. The extent and direction of seasonal changes in macroalgae were inconsistent among sites, creating a highly dynamic habitat matrix across time and space. Species richness and density of fishes were largely maintained where density of holdfasts from canopy-forming macroalgae and/or cover was high across seasons, but shifted markedly in areas of macroalgae habitat loss: suggesting stable habitat structure is critical for the persistence of macroalgae-associated fishes. Our results demonstrate that macroalgae fields that maintain high structural complexity across different seasons are more likely to preserve key ecological processes and therefore warrant greater conservation attention within a spatial management framework.


Species Richness Macroalgae Fish Assemblage Canopy Height Juvenile Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank staff at the Department of Parks and Wildlife Exmouth for field support, AIMS 2013 Appropriation funding 3.3.5 and the Australian Research Council for financial support. Early versions of the manuscript were improved through comments and discussion with Alan Kendrick.

Supplementary material

227_2014_2531_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 17 kb)


  1. Aburto-Oropeza O, Sala E, Paredes G, Mendoza A, Ballesteros E (2007) Predictability of reef fish recruitment in a highly variable nursery habitat. Ecology 88:2220–2228CrossRefGoogle Scholar
  2. Afonso P, Fontes J, Holland KN, Santos RS (2008) Social status determines behaviour and habitat usage in a temperate parrotfish: implications for marine reserve design. Mar Ecol Prog Ser 359:215–227CrossRefGoogle Scholar
  3. Almany GR, Webster MS (2006) The predation gauntlet: early postsettlement mortality in coral-reef fishes. Coral Reefs 25:19–22CrossRefGoogle Scholar
  4. Anderson TW (1994) Role of macroalgal structure in the distribution and abundance of a temperate reef fish. Mar Ecol Prog Ser 113:279–290CrossRefGoogle Scholar
  5. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693CrossRefGoogle Scholar
  6. Arkema KK, Reed DC, Schroeter SC (2009) Direct and indirect effects of giant kelp determine benthic community structure and dynamics. Ecology 90:3126–3137CrossRefGoogle Scholar
  7. Bellwood DR, Hughes TP, Folke C, Nytrom M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefGoogle Scholar
  8. Bock CE, Jones ZF, Bock JH (2007) Relationships between species richness, evenness, and abundance in a south-western Savanna. Ecology 88:1322–1327CrossRefGoogle Scholar
  9. Bonaldo RM, Bellwood DR (2008) Size-dependent variation in the functional role of the parrotfish Scarus rivulatus on the Great Barrier Reef, Australia. Mar Ecol Prog Ser 360:237–244CrossRefGoogle Scholar
  10. Brown JH, Mehlman DW, Stevens GC (1995) Spatial variation in abundance. Ecology 76:2028–2043CrossRefGoogle Scholar
  11. Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci USA 105:16201–16206CrossRefGoogle Scholar
  12. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  13. Carr MH (1994) Effects of macroalgal dynamics on recruitment of a temperate reef fish. Ecology 75:1320–1333CrossRefGoogle Scholar
  14. Chaves LTC, Pereira PHC, Feitosa JLL (2013) Coral reef fish association with macroalgal beds on a tropical reef system in North-eastern Brazil. Mar Freshw Res 64:1101–1111CrossRefGoogle Scholar
  15. Choat JH (1991) The biology of herbivorous fishes on coral reefs. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, London, pp 120–155CrossRefGoogle Scholar
  16. Choat JH, Ayling AM (1987) The relationship between habitat structure and fish faunas on New Zealand reefs. J Exp Mar Biol Ecol 110:257–284CrossRefGoogle Scholar
  17. Choat JH, Robertson DR (2002) Age-based studies on coral reef fishes. In: Sale PF (ed) Coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, London, pp 57–80CrossRefGoogle Scholar
  18. Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs I: dietary analysis. Mar Biol 140:613–623CrossRefGoogle Scholar
  19. Commonwealth of Australia (2006) A guide to the integrated marine and coastal regionalisation of Australia Version 4.0. Department of the Environment and Heritage, Canberra, AustraliaGoogle Scholar
  20. Connell SD (1998) Patterns of piscivory by resident predatory reef fish at One Tree Reef, Great Barrier Reef. Mar Freshw Res 49:25–30CrossRefGoogle Scholar
  21. Development Core Team R (2013) R: a language and environment for statistical computing. R Project for Statistical Computing, ViennaGoogle Scholar
  22. Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117:507–514CrossRefGoogle Scholar
  23. Downie RA, Babcock RC, Thomson DP, Vanderklift MA (2013) Density of herbivorous fish and intensity of herbivory are influenced by proximity to coral reefs. Mar Ecol Prog Ser 482:217–225CrossRefGoogle Scholar
  24. Evans RD, Wilson SK, Field SN, Moore JAY (2014) Significance of fish recruitment to macroalgal fields for coral reef ecology and fisheries in north-west Australia. Mar Biol 161:599–607CrossRefGoogle Scholar
  25. Fisher R, Knowlton N, Brainard RE, Caley MJ (2011) Differences among major taxa in the extent of ecological knowledge across four major ecosystems. PLoS One 6(11):e26556CrossRefGoogle Scholar
  26. Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators. Mar Ecol Prog Ser 230:253–264CrossRefGoogle Scholar
  27. Froese R, Pauly D (2013) FishBase. World Wide Web Electronic Publication. Version (10/2013)
  28. Fulton CJ, Depczynski M, Holmes TH, Noble MM, Radford B, Wernberg T, Wilson SK (2014) Sea temperature shapes seasonal fluctuations in seaweed biomass within the Ningaloo coral reef ecosystem. Limnol Oceanogr 59:156–166CrossRefGoogle Scholar
  29. Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326CrossRefGoogle Scholar
  30. Graham NAJ, Evans RD, Russ GR (2003) The effects of marine reserve protection on the trophic relationships of reef fishes on the Great Barrier Reef. Environ Conserv 30:200–208CrossRefGoogle Scholar
  31. Green BC, Smith DJ, Grey J, Underwood GJC (2012) High site fidelity and low site connectivity in temperate salt marsh fish populations: a stable isotope approach. Oecologia 168:245–255CrossRefGoogle Scholar
  32. Hay ME (1981) Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. Am Nat 118:520–540CrossRefGoogle Scholar
  33. Hixon MA, Beets JP (1993) Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101CrossRefGoogle Scholar
  34. Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes density-dependent predation mortality in damselfishes. Ecology 83:2855–2868CrossRefGoogle Scholar
  35. Holmes TH, Wilson SK, Vanderklift M, Babcock R, Fraser M (2012) The role of Thalassoma lunare as a predator of juvenile fish on a sub-tropical coral reef. Coral Reefs 31:1113–1123CrossRefGoogle Scholar
  36. Horinouchi M, Mizuno N, Jo Y, Fujita M, Sano M, Suzuki Y (2009) Seagrass habitat complexity does not always decrease foraging efficiencies of piscivorous fishes. Mar Ecol Prog Ser 377:43–49CrossRefGoogle Scholar
  37. James PL, Heck KL Jr (1994) The effects of habitat complexity and light intensity on ambush predation within a simulated seagrass habitat. J Exp Mar Biol Ecol 176:187–200CrossRefGoogle Scholar
  38. Johansson CL, Bellwood DR, Depczynski M (2010) Sea urchins, macroalgae and coral reef decline: a functional evaluation of an intact reef system, Ningaloo, Western Australia. Mar Ecol Prog Ser 414:65–74CrossRefGoogle Scholar
  39. Johansson CL, Bellwood DR, Depczynski M (2012) The importance of live coral for small-sized herbivorous reef fishes in physically challenging environments. Mar Freshw Res 63:672–679CrossRefGoogle Scholar
  40. Jones GP, Andrew NL (1990) Herbivory and patch dynamics on rocky reefs in temperate Australasia: the roles of fish and sea urchins. Aust J Ecol 15:505–520CrossRefGoogle Scholar
  41. Kobryn HT, Wouters K, Beckley LE, Heege T (2013) Ningaloo Reef: shallow marine habitats mapped using a hyperspectral sensor. PLoS One 8:e70105CrossRefGoogle Scholar
  42. Lefevre CD, Bellwood DR (2010) Seasonality and dynamics in coral reef macroalgae: variation in condition and susceptibility to herbivory. Mar Biol 157:955–965CrossRefGoogle Scholar
  43. Levin PS (1993) Habitat structure, conspecific presence and spatial variation in the recruitment of a temperate reef fish. Oecologia 94:176–185CrossRefGoogle Scholar
  44. Levin P, Hay ME (1996) Responses of temperate reef fishes to alterations in algal structure and species composition. Mar Ecol Prog Ser 134:37–47CrossRefGoogle Scholar
  45. Lilley SA, Schiel DR (2006) Community effects following the deletion of a habitat-forming alga from rocky marine shores. Oecologia 148:672–681CrossRefGoogle Scholar
  46. Mackie MC (1998) Biology and ecology of the chinaman cod, Epinephelus rivulatus, at Ningaloo Reef, Western Australia. PhD dissertation, University of Western Australia, Perth, AustraliaGoogle Scholar
  47. McIlwain JL (2003) Fine-scale temporal and spatial patterns of larval supply to a fringing reef in Western Australia. Mar Ecol Prog Ser 252:207–222CrossRefGoogle Scholar
  48. Munday PL, Jones GP, Caley MJ (1997) Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar Ecol Prog Ser 152:227–239CrossRefGoogle Scholar
  49. Nash KL, Graham NAJ, Wilson SK, Bellwood DR (2013) Cross-scale habitat structure drives fish body size distributions on coral reefs. Ecosystems 16:478–490CrossRefGoogle Scholar
  50. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R Package version 3:1–106Google Scholar
  51. Pratchett MS, Munday PL, Wilson SK, Graham NAJ, Cinner JE, Bellwood DR, Jones GP, Polunin NVC, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes ecological and economical consequences. Oceanogr Mar Biol 46:251–296CrossRefGoogle Scholar
  52. Rossier O, Kulbicki M (2000) A comparison of fish assemblages from two types of algal beds and coral reefs in the south-west lagoon of New Caledonia. Cybium 24:3–26Google Scholar
  53. Savino JF, Stein RA (1989) Behavioural interactions between fish predators and their prey: effects of plant density. Anim Behav 37:311–321CrossRefGoogle Scholar
  54. Schiel DR, Foster MS (1986) The structure of subtidal algal stands in temperate waters. Oceanogr Mar Biol 24:265–307Google Scholar
  55. Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  56. Verges A, Vanderklift MA, Doropoulos C, Hyndes GA (2011) Spatial patterns in herbivory on a coral reef are influenced by structural complexity but not by algal traits. PLoS One 6:e17115CrossRefGoogle Scholar
  57. Warfe DM, Barmuta LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Oecologia 141:171–178CrossRefGoogle Scholar
  58. Welsh J, Bellwood DR (2012) Spatial ecology of the steephead parrotfish (Chlorurus microrhinos): an evaluation using acoustic telemetry. Coral Reefs 31:55–65CrossRefGoogle Scholar
  59. Wilson SK, Depczynski M, Fisher R, Holmes TH, O’Leary RA, Tinkler P (2010) Habitat associations of juvenile fish at Ningaloo reef, Western Australia: the importance of coral and algae. PLoS One 5:e15185CrossRefGoogle Scholar
  60. Wilson SK, Babcock RC, Fisher R, Holmes TH, Moore JAY, 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 81:1–11CrossRefGoogle Scholar
  61. Woo M, Pattiaratchi C, Schroeder W (2006) Summer surface circulation along the Gascoyne continental shelf, Western Australia. Cont Shelf Res 26:132–152CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • S. K. Wilson
    • 1
    • 2
    Email author
  • C. J. Fulton
    • 3
  • M. Depczynski
    • 2
    • 4
  • T. H. Holmes
    • 1
    • 2
  • M. M. Noble
    • 3
  • B. Radford
    • 2
    • 4
  • P. Tinkler
    • 4
  1. 1.Marine Science Program, Science DivisionDepartment of Parks and WildlifeKensingtonAustralia
  2. 2.Oceans InstituteUniversity of Western AustraliaCrawleyAustralia
  3. 3.Australian Research Council Centre of Excellence for Coral Reef Studies, Research School of BiologyAustralian National UniversityCanberraAustralia
  4. 4.Australian Institute of Marine ScienceCrawleyAustralia

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