Reconstructing Historical Marine Populations Reveals Major Decline of a Kelp Forest Ecosystem in Australia

Abstract

Managing changing ecosystems requires an understanding both of how the system is currently performing and of how current performance relates to long-term, often variable, natural dynamics. However, making such assessments usually relies on having long-term ecological datasets, leaving managers often reliant on assumptions because such information is relatively rare. This is particularly an issue in kelp forests, as these ecosystems are difficult to survey, and many monitoring programs are relatively recent (last 10–20 years). A historical time series was constructed of kelp (Ecklonia radiata) and sea urchin (Heliocidaris erythrogramma) populations using various field-collected datasets, beginning in the 1960s, for the large shallow embayment of Port Phillip Bay, Australia. Additionally, aerial photographs were sourced to calculate the extent of these algal beds, going back to the 1930s. Both surveys and aerial images confirm that between the 1930s and the 1980s, kelp once occurred as dense (21–58% cover) beds over large sections of reef at all surveyed sites. However, by the early 2000s, kelp cover had declined by between 59 and 98%. From 2005 to 2012, sea urchins became 250–420% more abundant and were observed to be directly consuming large areas of macroalgae, creating the so-called sea urchin barrens. Analysis of reef algal cover between the 1930s and 2014 indicates that increases in temperature and declines in rainfall—which, in Port Phillip Bay, influences salinity, nutrient inputs and algal productivity—are correlated with the declines in kelp abundance. While it is difficult to tease apart all possible drivers, the years 1997–2009 coincided with a 1 °C increase in average air temperature and the longest drought period (137 mm less rainfall than the annual long-term average) in this region in recent record.

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References

  1. Abramoff, M.D., P.J. Magelhaes, and S.J. Ram. 2004. Image processing with ImageJ. Journal of Biophotonics 11: 36–42.

    Google Scholar 

  2. Alleway, H.K., and S.D. Connell. 2015. Loss of an ecological baseline through the eradication of oyster reefs from coastal ecosystems and human memory. Conservation Biology 29 (3): 795–804. https://doi.org/10.1111/COBI.12452.

    Article  Google Scholar 

  3. Andrew, N.L., and A.J. Underwood. 1993. Density dependent foraging in the sea urchin Centrostephanus rodgersii on shallow subtidal reefs in New South Wales, Australia. Marine Ecology Progress Series 99: 89–98.

    Article  Google Scholar 

  4. Bjorkman, A.D., and M. Vellend. 2010. Defining historical baselines for conservation: Ecological changes since european settlement on Vancouver Island, Canada. Conservation Biology 24 (6): 1559–1568.

    Article  Google Scholar 

  5. Bulleri, F., B.D. Russell, and S.D. Connell. 2012. Context-dependency in the effects of nutrient loading and consumers on the availability of space in marine rocky environments. PLoS One 7 (3): e33825.

    Article  CAS  Google Scholar 

  6. Campbell, A.H., E.M. Marzinelli, A. Verges, M.A. Coleman, and P.D. Steinberg. 2014. Towards restoration of missing underwater forests. PLoS One 9 (1): e84106.

    Article  CAS  Google Scholar 

  7. Carnell, P.E. 2014. Resilience of kelp dominated reefs of south-eastern Australia. PhD dissertation. In The University of Melbourne. Melbourne: VIC.

    Google Scholar 

  8. Carnell, P.E., and M.J. Keough. 2014. Spatially variable synergistic effects of disturbance and additional nutrients on kelp recruitment and recovery. Oecologia 175 (1): 409–416.

    Article  Google Scholar 

  9. Carnell, P.E., and M.J. Keough. 2016. The influence of herbivores on primary producers can vary spatially and interact with disturbance. Oikos 125 (9): 1273–1283.

    Article  Google Scholar 

  10. Connell, J.H., T.P. Hughes, and C.C. Wallace. 1997. A 30-year study of coral abundance, recruitment and disturbance at several scales in space and time. Ecological Monographs 67 (4): 461–488.

    Article  Google Scholar 

  11. Connell, S.D., and A.D. Irving. 2008. Integrating ecology with biogeography using landscape characteristics: A case study of subtidal habitat across continental Australia. Journal of Biogeography 5: 1608–1621.

    Article  Google Scholar 

  12. Connell, S.D., B.D. Russell, D.J. Turner, S.A. Shepherd, T. Kildea, D. Miller, L. Airoldi, and A. Cheshire. 2008. Recovering a lost baseline: Missing kelp forests from a metropolitan coast. Marine Ecology Progress Series 360: 63–72.

    Article  Google Scholar 

  13. Constable, A.J. 1990. An investigation of resource allocation in the sea urchin Heliocidaris erythrogramma (Valenciennes). PhD dissertation. In The University of Melbourne. Melbourne: VIC.

    Google Scholar 

  14. Crain, C.M., K. Kroeker, and B.S. Halpern. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters 11 (12): 1304–1315.

    Article  Google Scholar 

  15. Dayton, P.K., and M.J. Tegner. 1984. Catastrophic storms, El Niño and patch stability in a Southern California kelp community. Science 224 (4646): 283–285.

    Article  CAS  Google Scholar 

  16. Dayton, P.K., M.J. Tegner, P.B. Edwards, and K.L. Riser. 1998. Sliding baselines, ghosts, and reduced expectations in kelp forest communities. Ecological Applications 8 (2): 309–322.

    Article  Google Scholar 

  17. Dayton, P.J., M.J. Tegner, P.B. Edwards, and K.L. Riser. 1999. Temporal and spatial scales of kelp demography: The role of oceanographic climate. Ecological Monographs 69 (2): 219–250.

    Article  Google Scholar 

  18. De'ath, G., K.E. Fabricius, H. Sweatman, and M. Puotinen. 2012. The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences USA 109 (44): 17995–17999.

    Article  Google Scholar 

  19. Eckman, J.E., D.O. Duggins, and A.T. Sewell. 1989. Ecology of understory kelp environments I. Effects of kelps on flow and particle transport near the bottom. Journal of Experimental Marine Biology and Ecology 129 (2): 173–188.

    Article  Google Scholar 

  20. Edmunds, M., K. Stewart, and K. Pritchard (2009) Victorian subtidal reef monitoring program: the reef biota in the Port Phillip Bay Marine Sanctuaries. Parks Victoria Technical Series No. 67, Parks Victoria, Melbourne.

  21. Edwards, M.S. 2004. Estimating scale-dependency in disturbance impacts: El Niños and giant kelp forests in the northeast Pacific. Oecologia 138 (3): 436–447.

    Article  Google Scholar 

  22. EPA Victoria (2012) Baywide water quality monitoring program: milestone report No. 9. EPA Victoria, Melbourne, Australia. http://www.oem.vic.gov.au/WaterQuality (accessed June 2014).

  23. Estes, J.A., J. Terborgh, J.S. Brashares, M.E. Power, J. Berger, W.J. Bond, S.R. Carpenter, T.E. Essington, R.D. Holt, J.B.C. Jackson, R.J. Marquis, L. Oksanen, T. Oksanen, R.T. Paine, E.K. Pikitch, W.J. Ripple, S.A. Sandin, M. Scheffer, T.W. Schoener, J.B. Shurin, A.R.E. Sinclair, M.E. Soule, R. Virtanen, and D.A. Wardle. 2011. Trophic downgrading of planet Earth. Science 333 (6040): 301–306.

    Article  CAS  Google Scholar 

  24. Falkenberg, L.J., B.D. Russell, and S.D. Connell. 2013. Disrupting the effects of synergies between stressors: Improved water quality dampens the effects of future CO2 on a marine habitat. Journal of Applied Ecology 50 (1): 51–58.

    Article  CAS  Google Scholar 

  25. Foster, M.S., and D.R. Schiel. 2010. Loss of predators and the collapse of southern California kelp forests (?): Alternatives explanations and generalizations. Journal of Experimental Marine Biology and Ecology 393 (1-2): 59–70.

    Article  Google Scholar 

  26. Fulton, B. and T. Smith (2002) Ecosim case study: Port Phillip Bay, Australia. Fisheries Centre Research Reports 10, 83–93. Fisheries Centre, University of British Columbia, Vancouver, Canada.

  27. Harrold, C., and D.C. Reed. 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66 (4): 1160–1169.

    Article  Google Scholar 

  28. Jackson, J.B.C., M.X. Kirby, W.H. Berger, K.A. Bjorndal, L.W. Botsford, B.J. Bourque, R.H. Bradbury, R. Cooke, J. Erlandson, J.E. Estes, T.P. Hughes, S. Kidwell, C.B. Lange, H.S. Lenihan, J.M. Pandolfi, C.H. Peterson, R.S. Steneck, M.J. Tegner, and R.R. Warner. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293 (5530): 629–638.

    Article  CAS  Google Scholar 

  29. Johnson, C.R., and K.H. Mann. 1988. Diversity, patterns of adaptation, and stability of Nova Scotian kelp beds. Ecological Monographs 58 (2): 129–154.

    Article  Google Scholar 

  30. Johnson, C.R., S.C. Banks, N.S. Barrett, F. Cazassus, P.K. Dunstan, G.J. Edgar, S.D. Frusher, C. Gardner, M. Haddon, F. Helidoniotis, K.L. Hill, N.J. Holbrook, G.W. Hosie, P.R. Last, S.D. Ling, J. Melbourne-Thomas, K. Miller, G.T. Pecl, A.J. Richardson, K.R. Ridgway, S.R. Rintoul, D.A. Ritz, D.J. Ross, J.C. Sanderson, S.A. Shepherd, A. Slotwinski, K.M. Swadling, and N. Taw. 2011. Climate change cascades: Shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. Journal of Experimental Marine Biology and Ecology 400 (1-2): 17–32

    Article  Google Scholar 

  31. Jones, C.G., J.H. Lawton, and M. Shachak. 1994. Organisms as Ecosystem engineers. Oikos 69 (3): 373–386.

    Article  Google Scholar 

  32. Jung, C.A., P.D. Dwyer, M. Minnegal, and S.E. Swearer. 2011. Perceptions of environmental change over more than six decades in two groups of people interacting with the environment of Port Phillip Bay, Australia. Ocean and Coastal Management 54 (1): 93–99.

    Article  Google Scholar 

  33. Lee, R.S., K.P. Black, C. Bosserel, and D. Greer. 2012. Present and future prolonged drought impacts on a large temperate embayment: Port Phillip Bay Australia. Ocean Dynamics 62 (6): 907–922.

    Article  Google Scholar 

  34. Lester, S.E., B.S. Halpern, K. Grorud-Colvert, J. Lubchenco, B.I. Ruttenberg, S.D. Gaines, S. Airame, and R.R. Warner. 2009. Biological effects within no-take marine reserves: A global synthesis. Marine Ecology Progress Series 384: 33–46.

    Article  Google Scholar 

  35. Lindenmayer, D.B., G.E. Likens, A. Andersen, B. Bowman, C.M. Bull, E. Burns, C.R. Dickman, A.A. Hoffman, D.A. Keith, M.J. Liddell, A.J. Lowe, D.J. Metcalfe, S.R. Phinn, J. Russell-Smith, N. Thurgate, and G.M. Wardle. 2012. Value of long-term ecological studies. Austral Ecology 37 (7): 745–757.

    Article  Google Scholar 

  36. Ling, S.D. 2008. Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: A new and impoverished reef state. Oecologia 156 (4): 883–894.

    Article  CAS  Google Scholar 

  37. Ling, S.D., C.R. Johnson, S.D. Frusher, and K.R. Ridgway. 2009. Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proceedings of the National Academy of Sciences 106 (52): 22341–22345.

    Article  Google Scholar 

  38. Ling, S.D., S. Ibbott, and J.C. Sanderson. 2010. Recovery of canopy-forming macroalgae following removal of the enigmatic grazing sea urchin Heliocidaris erythrogramma. Journal of Experimental Marine Biology and Ecology 395 (1-2): 135–146.

    Article  Google Scholar 

  39. Livore, J.P., and S.D. Connell. 2012. Reducing per capita food supply alters urchin condition and habitat. Marine Biology 159 (5): 967–973.

    Article  Google Scholar 

  40. Longmore A. (2014). Port Phillip Bay Environmental Management Plan. Monitoring the State of Bay Nutrient Cycling 2013–2014. CAPIM Technical Report No. 49, Centre for Aquatic Pollution Identification and Management, University of Melbourne, Victoria, Australia.

  41. Lotze, H.K., H.S. Lenihan, B.J. Bourque, R.H. Bradbury, R.G. Cooke, M.C. Kay, S.M. Kidwell, M.X. Kirby, C.H. Peterson, and J.B.C. Jackson. 2006. Depletion, degradation and recovery potential of estuaries and coastal seas. Science 312 (5781): 1806–1809.

    Article  CAS  Google Scholar 

  42. Magurran, A.E., S.R. Baillie, S.T. Buckland, J.M. Dick, D.A. Elston, E.M. Scott, R.I. Smith, P.J. Somerfield, and A.D. Watt. 2010. Long-term datasets in biodiversity research and monitoring: Assessing change in ecological communities through time. Trends in Ecology and Evolution 25 (10): 574–582.

    Article  Google Scholar 

  43. Martin, T.G., M.A. Burgman, F. Fidler, P.M. Kuhnert, S. Low-Choy, M. McBride, and K. Mengersen. 2012. Eliciting expert knowledge in conservation science. Conservation Biology 26 (1): 29–38.

    Article  Google Scholar 

  44. McClenachan, L. 2009. Documenting loss of large trophy fish from the Florida keys with historical photographs. Conservation Biology 23 (3): 636–643.

    Article  Google Scholar 

  45. McClenachan, L., F. Ferretti, and J.K. Baum. 2012. From archives to conservation: Why historical data are needed to set baselines for marine animals and ecosystems. Conservation Letters 5 (5): 349–359.

    Article  Google Scholar 

  46. O’Brien, C.E. 1981. The subtidal ecology of the Gloucester Reserve Reef, Northern Port Phillip Bay. MSc thesis. In School of botany. Australia: University of Melbourne.

    Google Scholar 

  47. Osenberg, C.W., B.M. Bolker, J.S. White, C.M.St. Mary, and J.S. Shima. 2006. Statistical issues and study design in ecological restorations: Lessons learned from Marine Reserves. In Foundations of restoration ecology. Society for ecological restoration international, ed. D.A. Falk, M.A. Palmer, and J.B. Zedler, 280–302.

    Google Scholar 

  48. Pauly, D. 1995. Anecdotes and the shifting baseline syndrome of fisheries. Trends in Ecology and Evolution 10 (10): 430.

    Article  CAS  Google Scholar 

  49. Reed, D.C., A. Rassweiler, M.H. Carr, K.C. Cavanaugh, D.P. Malone, and D.R. Siegel. 2011. Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests. Ecology 92 (11): 2108–2116.

    Article  Google Scholar 

  50. Russell, B.D., and S.D. Connell. 2005. A novel interaction between nutrients and grazers alters relative dominance of marine habitats. Marine Ecology Progress Series 289: 5–11.

    Article  CAS  Google Scholar 

  51. Spencer, R.D. 1970. An ecological study of the sub-tidal macrophytic vegetation of three selected areas of Port Phillip Bay: Werribee, Altona and Carrum. MSc Thesis. In The University of Melbourne. Melbourne: VIC.

    Google Scholar 

  52. Tait, L.W., and D.R. Schiel. 2011. Legacy effects of canopy disturbance on ecosystem functioning in macroalgal assemblages. PLoS One 6 (10): e26986.

    Article  CAS  Google Scholar 

  53. Tegner, M.J., and P.K. Dayton. 1991. Sea urchins, El Niños, and the long-term stability of Southern California kelp forests. Marine Ecology Progress Series 77: 49–63.

    Article  Google Scholar 

  54. Tegner, M.J., P.K. Dayton, P.B. Edwards, and K.L. Riser. 1996. Is there evidence for long-term climatic change in southern California kelp forests? California Cooperative Oceanic Fisheries Investigations 37: 111–126.

    Google Scholar 

  55. Tegner, M.J., P.K. Dayton, P.B. Edwards, and K.L. Riser. 1997. Large-scale, low-frequency oceanographic effects on kelp forest succession: A tale of two cohorts. Marine Ecology Progress Series 146: 117–134.

    Article  Google Scholar 

  56. Thurstan, R.H., L. McClenachan, L.B. Crowder, J.A. Drew, J.N. Kittinger, P.S. Levin, C.M. Roberts, and J.M. Pandolfi. 2015. Filling historical data gaps to foster solutions in marine conservation. Ocean and Coastal Management 115: 31–40.

    Article  Google Scholar 

  57. Valentine, J.P., and C.R. Johnson. 2005. Persistence of sea urchin (Heliocidaris erythrogramma) barrens on the east coast of Tasmania: Inhibition of macroalgal recovery in the absence of high densities of sea urchins. Botanica Marina 48: 106–115.

    Article  Google Scholar 

  58. Wernberg, T., G.A. Kendrick, and B.D. Toohey. 2005. Modification of physical environment by an Ecklonia radiata (Laminariales) canopy and its implications for associated foliose algae. Aquatic Ecology 39 (4): 419–430.

    Article  Google Scholar 

  59. Wernberg, T., D.A. Smale, F. Tuya, M.S. Thomsen, T.J. Langlois, T. de Bettignies, S. Bennett, and C.S. Rousseaux (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nature Climate Change 3 (1): 78–82.

    Article  Google Scholar 

  60. Worm, B., E.B. Barbier, N. Beaumont, J.E. Duffy, C. Folke, B.S. Halpern, J.B.C. Jackson, H.K. Lotze, F. Micheli, S.R. Palumbi, E. Sala, K.A. Selcoe, J.J. Stachowicz, and R. Watson. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314 (5800): 787–790.

    Article  CAS  Google Scholar 

  61. Worthington, D.G. and C. Blount (2003) Research to develop and manage the sea urchin fisheries of NSW and eastern Victoria. Final report to the Fisheries Research and Development Corporation for Project 1999/128.

  62. Wright, J.T., S.A. Dworjanyn, C.N. Rogers, P.D. Steinberg, J.E. Williamson, and A.G.B. Poore. 2005. Density-dependent sea urchin grazing: Differential removal of species changes in community composition and alternative community states. Marine Ecology Progress Series 298: 143–156.

    Article  Google Scholar 

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Acknowledgements

We thank P. Crockett, J. Ford, D. Chamberlain and C. Taylor for their field assistance. SRMP data used with the permission of Parks Victoria and Department of Environment, Land, Water and Planning. Water quality data were supplied by A. Longmore from the Port Phillip Bay Environmental Monitoring Plan Nitrogen Monitoring Program. We also thank K. Mossop, J. Ford, P. Addison and the anonymous reviewers for the comments that greatly improved the manuscript. This study was funded by an Australian Research Council grant to M.J.K, a Holsworth Wildlife Research Endowment to P.E.C, the Jasper Loftus-Hills award to P.E.C and an Australian Postgraduate Award to P.E.C.

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Correspondence to Paul E. Carnell.

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Carnell, P.E., Keough, M.J. Reconstructing Historical Marine Populations Reveals Major Decline of a Kelp Forest Ecosystem in Australia. Estuaries and Coasts 42, 765–778 (2019). https://doi.org/10.1007/s12237-019-00525-1

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Keywords

  • Shifting baselines
  • Habitat loss
  • Historical ecology
  • Ecosystem shift