Marine Biology

, Volume 158, Issue 8, pp 1757–1766 | Cite as

Community development on subtidal temperate reefs: the influences of wave energy and the stochastic recruitment of a dominant kelp

  • Dan A. SmaleEmail author
  • Thomas Wernberg
  • Thomas Vance
Original Paper


Patterns of community development on subtidal rocky reefs in Marmion Lagoon, southwest Australia, were investigated with a settlement panel experiment. We tested the hypothesis that community development would differ between outer and inner reefs lines, because exposure to swell and wave energy was significantly greater on outer reefs. Following a 14-month deployment, we recorded pronounced variability between panels and sites, but did not detect any effect of wave exposure on the structure of panel assemblages. Subsequent data exploration suggested the importance of the presence of kelp recruits (Ecklonia radiata) in structuring the overall assemblage. Panel assemblages with kelp recruits were significantly different in structure to those without, principally because of greater space coverage of encrusting coralline algae and less coverage of red turfing algae, spirorbids, and bryozoans. Mature E. radiata act as ecosystem engineers in subtidal rocky reefs in southwest Australia. Our results suggested the importance of young, recruiting kelps in determining patterns of early community development on newly available hard substrata.


Macroalgae Assemblage Structure Wave Exposure Limestone Reef Macroalgal Assemblage 
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 Thibaut de Bettignies, Renae Hovey, Samantha Childs, and Adam Gartner for assistance in the field, and Gary Kendrick and Tim Langlois for insightful discussion and comments on earlier drafts of the paper. DS is funded by the Western Australian Marine Science Institute (WAMSI). Fieldwork was supported by an ARC Discovery Project grant to TW.


  1. Anderson MJ, Gorley RN, Clarke KR (2007) Permanova+ for primer: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  2. Andrew NL, Jones GP (1990) Patch formation by herbivorous fish in a temperate Australian kelp forest. Oecologia 85:57–68CrossRefGoogle Scholar
  3. 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
  4. Bell JJ, Barnes DKA (2003) The importance of competitor identity, morphology and ranking methodology to outcomes in interference competition between sponges. Mar Biol 143:415–426CrossRefGoogle Scholar
  5. Bell EC, Denny MW (1994) Quantifying ‘wave exposure’: a simple device for recording maximum velocity and results of its use at several field sites. J Exp Mar Biol Ecol 181:9–29CrossRefGoogle Scholar
  6. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, PlymouthGoogle Scholar
  7. Connell SD (2003) The monopolization of understorey habitat by subtidal encrusting coralline algae: a test of the combined effects of canopy-mediated light and sedimentation. Mar Biol 142:1065–1071Google Scholar
  8. Connell SD (2005) Assembly and maintenance of subtidal habitat heterogeneity: synergistic effects of light penetration and sedimentation. Mar Ecol Prog Ser 289:53–61CrossRefGoogle Scholar
  9. Connell SD (2007) Subtidal temperate rocky habitats: habitat heterogeneity at local to continental scales. In: Connell SD, Gillanders BM (eds) Marine ecology. Oxford University Press, MelbourneGoogle Scholar
  10. Dayton PK (1985) Ecology of Kelp communities. Annu Rev Ecol Syst 16:215–245CrossRefGoogle Scholar
  11. Dayton PK, Tegner MJ, Parnell PE, Edwards PB (1992) Temporal and spatial patterns of disturbance and recovery in a Kelp forest community. Ecol Monogr 62:421–445CrossRefGoogle Scholar
  12. Dayton PK, Tegner MJ, Edwards PB, Riser KL (1999) Temporal and spatial scales of kelp deomography: the role of oceanographic climate. Ecol Monogr 69:219–250CrossRefGoogle Scholar
  13. Ebeling AW, Laur DR, Rowley RJ (1985) Severe storm disturbances and reversal of community structure in a southern California kelp forest. Mar Biol 84:287–294CrossRefGoogle Scholar
  14. England PR, Phillips J, Waring JR, Symonds G, Babcock R (2008) Modelling wave-induced disturbance in highly biodiverse marine macroalgal communities: support for the intermediate disturbance hypothesis. Mar Freshw Res 59:515–520CrossRefGoogle Scholar
  15. Fowler-Walker MJ, Connell SD (2007) Habitat heterogeneity as a consequence of substratum-orientation and kelp-canopy: relating interdependent responses to common patterns. J Exp Mar Biol Ecol 343:127–137CrossRefGoogle Scholar
  16. Fox NJ, Beckley LE (2005) Priority areas for conservation of Western Australian coastal fishes: a comparison of hotspot, biogeographical and complementarity approaches. Biol Conserv 125:399–410CrossRefGoogle Scholar
  17. Hatcher AI (1989) Variation in the components of benthic community structure in a coastal lagoon as a function of spatial scale. Mar Freshw Res 40:79–96CrossRefGoogle Scholar
  18. Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472CrossRefGoogle Scholar
  19. Hutchins JB (2001) Checklist of Western Australian fishes. Rec West Aust Mus Suppl 63:9–50Google Scholar
  20. Hyndes GA, Platell ME, Potter IC, Lenanton RCJ (1999) Does the composition of the demersal fish assemblages in temperate coastal waters change with depth and undergo consistent seasonal changes? Mar Biol 134:335–352CrossRefGoogle Scholar
  21. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  22. Kendrick GA (1994) Effects of propagule settlement density and adult canopy on survival of recruits on Sargassum spp. (Sargassaceae: Phaeophyta). Mar Ecol Prog Ser 103:129–140CrossRefGoogle Scholar
  23. Kendrick GA, Walker DI (1994) Role of recruitment in structuring beds of Sargassum spp. (Phaeophyta) at Rottnest Island, Western Australia. J Phycol 30:200–208CrossRefGoogle Scholar
  24. Kendrick GA, Lavery PS, Phillips JC (1999) Influence of Ecklonia radiata kelp canopy on structure of macro-algal assemblages in Marmion Lagoon, Western Australia. Hydrobiologia 398(399):275–283CrossRefGoogle Scholar
  25. Kendrick GA, Goldberg NA, Harvey ES, McDonald J (2009) Historical and contemporary influence of the Leeuwin Current to the marine biota of the Southern Western Australian Continental Shelf and the Recherche Archipelago. J R Soc West Aust 92:209–217Google Scholar
  26. Kennelly SJ (1987) Inhibition of kelp recruitment by turfing algae and consequences for an Australian kelp community. J Exp Mar Biol Ecol 112:49–60CrossRefGoogle Scholar
  27. Kerswell AP (2006) Biodiversity patterns of benthic marine algae. Ecology 87:2479–2488CrossRefGoogle Scholar
  28. Kirkman H (1984) Standing stock and production of Ecklonia radiata (C.Ag.). J Agardh J Exp Mar Biol Ecol 76:119–130CrossRefGoogle Scholar
  29. Lemm AJ, Hegge BJ, Masselink G (1999) Offshore wave climate, Perth (Western Australia), 1994–96. Mar Freshw Res 50:95–102CrossRefGoogle Scholar
  30. Lindegarth M, Gamfeldt L (2005) Comparing categorical and continuous ecological analyses: effects of ‘wave exposure’ on rocky shore. Ecology 86:1346–1357CrossRefGoogle Scholar
  31. McGowan JA, Cayan DR, Dorman LM (1998) Climate-ocean variability and ecosystem response in the Northeast Pacific. Science 281:210–217CrossRefGoogle Scholar
  32. Phillips JA (2001) Marine macroalgal biodiversity hotspots: why is there high species richness and endemism in southern Australian marine benthic flora? Biodivers Conserv 10:1555–1577CrossRefGoogle Scholar
  33. Phillips JC, Kendrick GA, Lavery PS (1997) A test of a functional group approach to detecting shifts in macroalgal communities along a disturbance gradient. Mar Ecol Prog Ser 153:125–138CrossRefGoogle Scholar
  34. Ruuskanen A, Back S, Reitalu T (1999) A comparison of two cartographic exposure methods using Fucus vesiculosus as an indicator. Mar Biol 134:139–145CrossRefGoogle Scholar
  35. Schiel DR, Foster MS (1986) The structure of subtidal algal stands in temperate waters. Oceanogr Mar Biol Ann Rev 24:265–307Google Scholar
  36. Searle DJ, Semeniuk V (1985) The natural sectors of the inner Rottnest Shelf coast adjoining the Swan Coastal Plain. J Roy Soc West Aus 67:116–136Google Scholar
  37. Shears NT, Babcock RC (2002) Marine reserves demonstrate top–down control of community structure on temperate reefs. Oecologia 132:131–142CrossRefGoogle Scholar
  38. Smale DA, Kendrick GA, Wernberg T (2010) Assemblage turnover and taxonomic sufficiency of subtidal macroalgae at multiple spatial scales. J Exp Mar Biol Ecol 384:76–86CrossRefGoogle Scholar
  39. Smale DA, Wernberg T, Kendrick GA (2011) Subtidal macroalgal richness, diversity and turnover, at multiple spatial scales, along the southwestern Australian coastline. Estuar Coastal Shelf Sci 91:224–231Google Scholar
  40. Somerfield PJ, Clarke KR, Olsgard F (2002) A comparison of the power of categorical and correlational tests applied to community ecology data from gradient studies. J Anim Ecol 71:581–593CrossRefGoogle Scholar
  41. 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
  42. Thomsen MS, Wernberg T, Kendrick GA (2004) The effect of thallus size, life stage, aggregation, wave exposure and substrate conditions on the forces required to break or dislodge the small kelp Ecklonia radiata. Bot Mar 47:454–460CrossRefGoogle Scholar
  43. Todd CD, Turner SJ (1986) Ecology of intertidal and sublittoral cryptic epifaunal assemblages. I. Experimental rationale and the analysis of larval settlement. J Exp Mar Biol Ecol 99:199–231CrossRefGoogle Scholar
  44. Toohey BD (2007) The relationship between physical variables on topographically simple and complex reefs and algal assemblage structure beneath an Ecklonia radiata canopy. Estuar Coastal Shelf Sci 71:232–240CrossRefGoogle Scholar
  45. Toohey B, Kendrick GA, Wernberg T, Phillips JA, Malkin S, Prince J (2004) The effects of light and thallus scour from Ecklonia radiata canopy on an associated foliose algal assemblages: the importance of photoacclimation. Mar Biol 144:1019–1027CrossRefGoogle Scholar
  46. Toohey BD, Kendrick GA, Harvey ES (2007) Disturbance and reef topography maintain high local diversity in Ecklonia radiata kelp forests. Oikos 116:1618–1630CrossRefGoogle Scholar
  47. Vanderklift MA, Kendrick GA (2004) Variations in abundances of herbivorous invertebrates in temperate subtidal rocky reef habitats. Mar Freshw Res 55:93–103CrossRefGoogle Scholar
  48. Vanderklift MA, Lavery PS, Waddington KI (2009) Intensity of herbivory on kelp by fish and sea urchins differs between inshore and offshore reefs. Mar Ecol Prog Ser 376:203–211CrossRefGoogle Scholar
  49. Wernberg T (2009) Spatial variation in juvenile and adult Ecklonia radiata (Laminariales) sporophytes. Aquat Bot 90:93–95CrossRefGoogle Scholar
  50. Wernberg T, Connell SD (2008) Physical disturbance and subtidal habitat structure on open rocky coasts: Effects of wave exposure, extent and intensity. J Sea Res 59:237–248CrossRefGoogle Scholar
  51. Wernberg T, Goldberg N (2008) Short-term temporal dynamics of algal species in a subtidal kelp bed in relation to changes in environmental conditions and canopy biomass. Estuar Coastal Shelf Sci 76:265–272CrossRefGoogle Scholar
  52. Wernberg T, Thomsen MS (2005) The effect of wave exposure on the morphology of Ecklonia radiata. Aquat Bot 83:61–70CrossRefGoogle Scholar
  53. Wernberg T, Vanderklift MA (2010) Contribution of temporal and spatial components to morphological variation in the kelp Ecklonia (Laminariales) J Phycol 46:153–161Google Scholar
  54. Wernberg T, Kendrick GA, Phillips JC (2003) Regional differences in kelp-associated algal assemblages on temperate limestone reefs in south-western Australia. Divers Distrib 9:427–441CrossRefGoogle Scholar
  55. Wernberg T, Kendrick GA, Toohey BD (2005) Modification of the physical environment by an Ecklonia radiata (Laminariales) canopy and its implications to associated foliose algae. Aquat Ecol 39:419–430CrossRefGoogle Scholar
  56. Wernberg T, Vanderklift MA, How J, Lavery PS (2006) Export of detached macroalgae from reefs to adjacent seagrass beds. Oecologia 147:692–701CrossRefGoogle Scholar
  57. Wernberg T, White M, Vanderklift MA (2008) Population structure of turbinid gastropods on wave-exposed subtidal reefs: effects of density, body size and algae on grazing behaviour. Mar Ecol Prog Ser 362:169–179CrossRefGoogle Scholar
  58. Wernberg T, Thomsen MS, Tuya F, Kendrick GA, Staehr PA, Toohey BD (2010) Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecol Lett 13:685–694CrossRefGoogle Scholar
  59. Wernberg T, Russell BD, Moore PJ, Ling SD, Smale DA, Coleman M, Steinberg PD, Kendrick GA, Connell SD (2011) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J Exp Mar Biol Ecol 400. doi: 10.1016/j.jembe.2011.02.021

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.School of Plant Biology, Oceans InstituteUniversity of Western AustraliaCrawleyAustralia
  2. 2.Australian Institute of Marine Science, Oceans InstituteUniversity of Western AustraliaCrawleyAustralia
  3. 3.Plymouth Marine LaboratoryPlymouthUK

Personalised recommendations