, Volume 156, Issue 4, pp 883–894 | Cite as

Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state

  • S. D. LingEmail author
Global Change Ecology - Original Paper


Global climate change is predicted to have major negative impacts on biodiversity, particularly if important habitat-modifying species undergo range shifts. The sea urchin Centrostephanus rodgersii (Diadematidae) has recently undergone poleward range expansion to relatively cool, macroalgal dominated rocky reefs of eastern Tasmania (southeast Australia). As in its historic environment, C. rodgersii in the extended range is now found in association with a simplified ‘barrens’ habitat grazed free of macroalgae. The new and important role of this habitat-modifier on reef structure and associated biodiversity was clearly demonstrated by completely removing C. rodgersii from incipient barrens patches at an eastern Tasmanian site and monitoring the macroalgal response relative to unmanipulated barrens patches. In barrens patches from which C. rodgersii was removed, there was a rapid proliferation of canopy-forming macroalgae (Ecklonia radiata and Phyllospora comosa), and within 24 months the algal community structure had converged with that of adjacent macroalgal beds where C. rodgersii grazing was absent. A notable scarcity of limpets on C. rodgersii barrens in eastern Tasmania (relative to the historic range) likely promotes rapid macroalgal recovery upon removal of the sea urchin. In the recovered macroalgal habitat, faunal composition redeveloped similar to that from adjacent intact macroalgal beds in terms of total numbers of taxa, total individuals and Shannon diversity. In contrast, the faunal community of the barrens habitat is overwhelmingly impoverished. Of 296 individual floral/faunal taxa recorded, only 72 were present within incipient barrens, 253 were present in the recovered patches, and 221 were present within intact macroalgal beds. Grazing activity of C. rodgersii results in an estimated minimum net loss of approximately 150 taxa typically associated with Tasmanian macroalgal beds in this region. Such a disproportionate effect by a single range-expanding species demonstrates that climate change may lead to unexpectedly large impacts on marine biodiversity as key habitat-modifying species undergo range modification.


Biodiversity Centrostephanus rodgersii Climate change Kelp beds Sea urchin barrens 



I thank many dive volunteers who assisted with the fieldwork, particularly Anthony Reid, Dave Stevenson, Adam Stephens and Ryan Downie. I am grateful for the assistance in faunal identification received from Graham Edgar. This work was supported by the School of Zoology and the Tasmanian Aquaculture and Fisheries Institute—University of Tasmania, plus the CSIRO-UTAS joint programme in Quantitative Marine Science. This manuscript was improved by comments received from Craig Johnson and Joseph Valentine.

Supplementary material

442_2008_1043_MOESM1_ESM.doc (390 kb)
Appendix (DOC 390 kb)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46CrossRefGoogle Scholar
  2. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  3. Andrew NL (1991) Changes in subtidal habitat following mass mortality of sea urchins in Botany Bay, New South Wales. Aust J Ecol 16:353–362CrossRefGoogle Scholar
  4. Andrew NL (1993) Spatial heterogeneity, sea urchin grazing, and habitat structure on reefs in temperate Australia. Ecology 74:292–302CrossRefGoogle Scholar
  5. Andrew NL, Byrne M (2001) The ecology of Centrostephanus rodgersii. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 149–160CrossRefGoogle Scholar
  6. Andrew NL, O’Neill AL (2000) Large-scale patterns in habitat structure on subtidal rocky reefs in New South Wales. Mar Freshw Res 51:255–263CrossRefGoogle Scholar
  7. Andrew NL, Underwood AJ (1992) Associations and abundance of sea urchins and abalone on shallow subtidal reefs in southern New South Wales. Aust J Mar Freshw Res 43:1547–1559CrossRefGoogle Scholar
  8. Andrew NL, Underwood AJ (1993) Density-dependent foraging in the sea urchin Centrostephanus rodgersii on shallow subtidal reefs in New South Wales, Australia. Mar Ecol Prog Ser 99:89–98CrossRefGoogle Scholar
  9. Andrew NL, Worthington DG, Brett PA, Bentley N, Chick RC, Blount C (1998) Interactions between the abalone fishery and sea urchins in New South Wales. FRDC Final Report, Project No. 93/102. Fisheries Research and Development Corporation, Deakin West, ACT, AustraliaGoogle Scholar
  10. Babcock RC, Kelly S, Shears NT, Walker JW, Willis TJ (1999) Changes in community structure in temperate marine reserves. Mar Ecol Prog Ser 189:125–134CrossRefGoogle Scholar
  11. Barrett NS (1995) Short and long-term movement patterns of six temperate reef fishes (Families: Labridae and Monacanthidae). Mar Freshw Res 46:853–860CrossRefGoogle Scholar
  12. Bodkin JL (1988) Effects of kelp forest removal on associated fish assemblages in central California. J Exp Mar Biol Ecol 117:227–238CrossRefGoogle Scholar
  13. Cai WJ, Shi G, Cowan T, Bi D, Ribbe J (2005) The response of southern annular mode, the East Australian Current, and the southern midlatitude ocean circulation to global warming. Geophys Res Lett 32:L23706Google Scholar
  14. Chapman ARO (1981) Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St. Margaret’s Bay, Eastern Canada. Mar Biol 62:307–311CrossRefGoogle Scholar
  15. Dayton PK (1985) Ecology of kelp communities. Annu Rev Ecol Evol Syst 16:215–245CrossRefGoogle Scholar
  16. Draper N, Smith H (1981) Applied regression analysis. Wiley, New YorkGoogle Scholar
  17. Duggins DO (1980) Kelp beds and sea otters: an experimental approach. Ecology 61:447–453CrossRefGoogle Scholar
  18. Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173PubMedCrossRefGoogle Scholar
  19. Edgar GJ (1997) Australian marine life. Reed, KewGoogle Scholar
  20. Edgar GJ, Shaw C (1995) The production and trophic ecology of shallow-water fish assemblages in southern Australia. II. Diets of fishes and trophic relationships between fishes and benthos at Western Port. Victoria. J Exp Mar Biol Ecol 194:83–106CrossRefGoogle Scholar
  21. Edgar GJ, Barrett NS, Morton AJ, Samson CR (2004) Effects of algal canopy clearance on plant, fish and macroinvertebrate communities on eastern Tasmanian reefs. J Exp Mar Biol Ecol 312:67–87CrossRefGoogle Scholar
  22. Edgar GJ, Samson CR, Barrett NS (2005) Species extinction in the marine environment: Tasmania as a regional example of overlooked losses in biodiversity. Conserv Biol 19:1294–1300CrossRefGoogle Scholar
  23. Elmqvist T, Folke C, Nystrom M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity and ecosystem resilience. Front Ecol Environ 1:488–94Google Scholar
  24. Fletcher WJ (1987) Interactions among subtidal Australian sea urchins, gastropods and algae: effects of experimental removals. Ecol Monogr 57:89–109CrossRefGoogle Scholar
  25. Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Evol Syst 35:557–81CrossRefGoogle Scholar
  26. Graham MH (2004) Effects of local deforestation on the diversity and structure of southern California giant kelp forest food webs. Ecosystems 7:341–357CrossRefGoogle Scholar
  27. Harley CDG, Hughes RA, Hultgren KM, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impact of climate change in coastal marine systems. Ecol Lett 9:228–241PubMedCrossRefGoogle Scholar
  28. Hijmans RJ, Graham CH (2006) The ability of climate envelope models to predict the effect of climate change on species distributions. Glob Chang Biol 12:2272–2281CrossRefGoogle Scholar
  29. Hill NA, Blount C, Poore AGB, Worthington D, Steinberg P (2003) Grazing effects of the sea urchin Centrostephanus rodgersii in two contrasting rocky reef habitats: effects of urchin density and its implications for the fishery. Mar Freshw Res 54:691–700CrossRefGoogle Scholar
  30. Himmelman JH, Cardinal A, Bourget E (1983) Community development following removal of urchins, Strongylocentrotus droebachiensis, from the rocky subtidal zone of the St. Lawrence Estuary, Eastern Canada. Oecologia 59:27–39CrossRefGoogle Scholar
  31. Hughes L (2000) Biological consequences of global warming: is the signal already apparent across natural systems? TREE 15:56–61PubMedGoogle Scholar
  32. Hughes TP, Bellwood DR, Folke C, Steneck RS, Wilson J (2005) New paradigms for supporting the resilience of marine ecosystems. TREE 20:380–386PubMedGoogle Scholar
  33. Johnson CR, Mann KH (1993) Rapid succession in subtidal understorey seaweeds during recovery from overgrazing by sea urchins in eastern Canada. Bot Mar 36:63–77CrossRefGoogle Scholar
  34. Johnson CR, Ling SD, Ross J, Shepherd S, Miller K (2005) Establishment of the long-spined sea urchin (Centrostephanus rodgersii) in Tasmania: first assessment of potential threats to fisheries. FRDC Final Report, Project No. 2001/044. Fisheries Research and Development Corporation, Deakin West, ACT, AustraliaGoogle Scholar
  35. Keats DW, South GR, Steele DH (1990) Effects of an experimental reduction in grazing green sea urchins on a benthic macroalgal community in eastern Newfoundland. Mar Ecol Prog Ser 68:181–193CrossRefGoogle Scholar
  36. Leinass HP, Christie H (1996) Effects of removing sea urchins (Strongylocentrotus droebachiensis): stability of the barren state and succession of kelp forest recovery in the east Atlantic. Oecologia 105:524–536CrossRefGoogle Scholar
  37. Ling SD, Johnson CR, Frusher S, King CK (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Glob Chang Biol 14:907–915CrossRefGoogle Scholar
  38. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  39. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change. Nature 421:37–42PubMedCrossRefGoogle Scholar
  40. Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien ML, Hereu B, Milazzo M, Zabala M, D’Anna G, Pipitone C (2000) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200CrossRefGoogle Scholar
  41. Poloczanska ES, Babcock RC, Butler A, Hobday AJ, Hoegh-Guldberg O, Kunz TJ, Matear R, Milton DA, Okey TA, Richardson AJ (2007) Climate change and Australian marine life. Oceanogr Mar Biol Annu Rev 45:409–480Google Scholar
  42. Ridgway KR (2007) Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophys Res Lett 34:L13613. doi: 10.1029/2007GL030393 CrossRefGoogle Scholar
  43. Rosenzweig C, Casassa G, Karoly DJ, Imeson A, Liu C, Menzel A, Rawlins S, Root TL, Seguin B, Tryjanowski P (2007) Assessment of observed changes and responses in natural and managed systems. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 79–131Google Scholar
  44. Sanderson JC (1997) Subtidal macroalgal assemblages in temperate Australian coastal waters. State of the Environment Technical Paper Series (Estuaries and the Sea). Department of the Environment, CanberraGoogle Scholar
  45. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596PubMedCrossRefGoogle Scholar
  46. Taylor RB (1998) Density, biomass and productivity of animals in four subtidal rocky reef habitats: the importance of small mobile invertebrates. Mar Ecol Prog Ser 172:37–51CrossRefGoogle Scholar
  47. Valentine JP, Johnson CR (2004) Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania, Australia. Mar Freshw Res 55:223–230CrossRefGoogle Scholar
  48. Vance RR (1979) Effects of grazing by the sea urchin, Centrostephanus coronatus, on prey community composition. Ecology 60:537–546CrossRefGoogle Scholar
  49. Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design, 3rd edn edn. McGraw Hill, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.School of ZoologyUniversity of TasmaniaHobartAustralia

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