Environmental Monitoring and Assessment

, Volume 175, Issue 1–4, pp 685–697 | Cite as

The influence of estuarine water quality on cover of barnacles and Enteromorpha spp.

  • Glenn Courtenay
  • William Gladstone
  • Marcus Scammell
  • Renée Kidson
  • Julie Wood


The influence of ambient water quality on the settlement of barnacles and the green alga Enteromorpha spp. to an artificial substratum in the estuaries of Sydney, Australia, was investigated to test the efficacy of both groups of organisms as indicators of changes in water quality due to urban stormwater runoff and/or sewage overflows. Wooden settlement panels were immersed for 4 months on 17 occasions between 1996 and 2005 at 11 locations known to vary in water-quality parameters (conductivity, total uncombined ammonia, oxidised nitrogen, total nitrogen, filterable phosphorus, total phosphorus, faecal coliforms and chlorophyll-a) and ambient meteorological conditions (total rainfall, maximum rainfall). Water-quality data were collected during the time that the settlement panels were deployed. Cover of barnacles was highly variable among locations (range 1.2–55.2%). Hierarchical partitioning found that chlorophyll-a, total phosphorus and total nitrogen had significant independent positive effects on barnacle cover. Together, these variables explained 26% of the variation in barnacle cover. Mean cover of Enteromorpha spp., however, did not vary significantly among locations suggesting that other potentially more important factors are influencing its settlement and growth. The results of this study suggest that barnacle cover is likely to be a useful indicator of some components of water quality.


Estuary Indicator Settlement Urbanised catchments Water quality 


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  1. Anderson, M. J. & Underwood, A. J (1994). Effects of substratum on the recruitment and development of an intertidal estuarine fouling assemblage. Journal of Experimental Marine Biology and Ecology, 184, 217–236.CrossRefGoogle Scholar
  2. APHA [American Public Health Association, American Water Works Association and Water Pollution Control Federation] (1998). Standard methods for the examination of water and wastewater, 20th Edition. Washington DC: American Public Health Association.Google Scholar
  3. AWT - Ensight (1996). Biological Indicators Pilot Studies—May 1994 to December 1995. Prepared for Clean Waterways Programme, Sydney Water Corporation.Google Scholar
  4. Atilla, N. (2000). Meiofaunal colonization of artificial substrates in an estuarine embayment. Marine Ecology, 21, 69–83.CrossRefGoogle Scholar
  5. Barr, N. G., & Rees, T. A. V. (2003). Nitrogen status and metabolism in the green seaweed Enteromorpha intestinalis: An examination of three natural populations. Marine Ecology Progress Series, 249, 133–144.CrossRefGoogle Scholar
  6. Bellgrove, A., Clayton, M. N., & Quinn, G. P. (1997). Effects of secondarily treated sewage effluent on intertidal macroalgal recruitment processes. Marine and Freshwater Research, 48, 137–46.CrossRefGoogle Scholar
  7. Bertness, M. D., Gaines, S. D., Bermudez, D., & Sanford, E. (1991). Extreme spatial variation in the growth and reproductive output of the acorn barnacle Semibalanus balanoides. Marine Ecology Progress Series, 75, 91–100.CrossRefGoogle Scholar
  8. Browne, K. A., & Zimmer, R. K. (2001). Controlled field release of a waterborne chemical signal stimulates planktonic larvae to settle. The Biological Bulletin, 200, 87–91.CrossRefGoogle Scholar
  9. Bulleri, F., & Chapman, M. G. (2004). Intertidal assemblages on artificial and natural habitats in marinas on the north-west coast of Italy. Marine Biology, 145, 381–391.CrossRefGoogle Scholar
  10. Bulleri, F., Chapman, M. G., & Underwood, A. J. (2005). Intertidal assemblages on seawalls and vertical rocky shores in Sydney Harbour, Australia. Austral Ecology, 30, 655–667.CrossRefGoogle Scholar
  11. Cadotte, M. W., & Fukami, T. (2005). Dispersal, spatial scale, and species diversity in a hierarchically structured experimental landscape. Ecology Letters, 8, 548–557.CrossRefGoogle Scholar
  12. Cadotte, M. W., Drake, J. A., & Fukami, T. (2005). Constructing nature: Laboratory models as necessary tools for investigating complex ecological communities. Advanced Ecological Research, 37, 333–353.CrossRefGoogle Scholar
  13. Caffey, H. M. (1985). Spatial and temporal variation in settlement and recruitment of intertidal barnacles. Ecological Monographs, 55, 313–332.CrossRefGoogle Scholar
  14. Calcagno, J. A., López Gappa, J., & Tablado, A. (1998). Population dynamics of the barnacle Balanus amphitrite in an intertidal area affected by sewage pollution. Journal of Crustacean Biology, 18, 128–137.CrossRefGoogle Scholar
  15. Chevan, A., & Sutherland, M. (1991). Hierarchical Partitioning. American Statistician, 45, 90–96.CrossRefGoogle Scholar
  16. Cohen, R. A., & Fong, P. (2004). Nitrogen uptake and assimilation in Enteromorpha intestinalis (L.) Link (Chlorophyta): Using 15N to determine preference during simultaneous pulses of nitrate and ammonium. Journal of Experimental Marine Biology and Ecology, 309, 67–77.CrossRefGoogle Scholar
  17. Cohen, R. A., & Fong, P. (2005). Experimental evidence supports the use of δ 15N content of the opportunistic green macroalga Enteromorpha intestinalis (Chlorophyta) to determine nitrogen sources to estuaries. Journal of Phycology, 41, 287–293.CrossRefGoogle Scholar
  18. Cohen, R. A., & Fong, P. (2006). Using opportunistic green macroalgae as indicators of nitrogen supply as sources to estuaries. Ecological Applications, 16, 1405–1420.CrossRefGoogle Scholar
  19. Courtenay, G., Gladstone, W., & Schreider, M. (2005). Assessing the response of estuarine intertidal assemblages to urbanised catchment discharge. Environmental Monitoring and Assessment, 107, 375–398.CrossRefGoogle Scholar
  20. Das, P., Marchesiello, P., & Middleton, J. H. (2000). Numerical modelling of tide-induced residual circulation in Sydney Harbour. Marine and Freshwater Research, 51, 97–112.CrossRefGoogle Scholar
  21. Day, J. W., Hall, C. A. S., & Kemp, W. M. (1989). Estuarine ecology. New Jersey: Wiley.Google Scholar
  22. Dean, T. A., & Hurd, L. E. (1980). Development in an estuarine fouling community: The influence of early colonists on later animals. Oecologia, 46, 295–301.Google Scholar
  23. Desai, D. V., Anil, A. C., & Venkat, K. (2006). Reproduction in Balanus amphitrite Darwin (Cirripedia: Thoracica): Influence of temperature and food concentration. Marine Biology, 149, 1431–1441.CrossRefGoogle Scholar
  24. DiDonato, G. T., Stewart, J. R., Sanger, D. M., Robinson, B. J., Thompson, B. C., Frederick Holland, A. et al. (2009). Effects of changing land use on the microbial water quality of tidal creeks. Marine Pollution Bulletin, 58, 97–106.CrossRefGoogle Scholar
  25. Egan, E. A., & Anderson, D. T. (1986). Larval development of Balanus amphitrite Darwin and Balanus variegates Darwin (Cirripedia, Balanidae) from New South Wales, Australia. Crustaceana, 51, 188–207.CrossRefGoogle Scholar
  26. Ellien, C., Thiébaut, E., Dumas, F., Salomon, J., & Nival, P. (2004). A modelling study of the respective role of hydrodynamic processes and larval mortality on larval dispersal and recruitment of benthic invertebrates: Example of Pectinaria koreni (Annelida: Polychaeta) in the Bay of Seine (English Channel). Journal of Plankton Research, 26, 117–132.CrossRefGoogle Scholar
  27. Fairfull, S. J. L., & Harriott, V. J. (1999). Succession, space and coral recruitment in a subtropical fouling community. Marine and Freshwater Research, 50, 235–240.CrossRefGoogle Scholar
  28. Fairweather, P. G. (1991). Implications of “supply-side” ecology for environmental assessment and management. Trends in Ecology and Evolution, 6, 60–63.CrossRefGoogle Scholar
  29. Fairweather, P. G. (1999). Determining the ‘health’ of estuaries: Priorities for ecological research. Australian Journal of Ecology, 24, 441–451.CrossRefGoogle Scholar
  30. Fletcher, R. L., & Callow, M. E. (1992). The settlement, attachment and establishment of marine algal spores. British Phycology Journal, 27, 303–329.CrossRefGoogle Scholar
  31. Fong, P., Boyer, K. E., & Zedler, J. B. (1998). Developing an indicator of nutrient enrichment in coastal estuaries and lagoons using tissue nitrogen content of the opportunistic alga, Enteromorpha intestinalis (L. Link). Journal of Experimental Marine Biology and Ecology, 231, 63–79.CrossRefGoogle Scholar
  32. Fong, P., Fong, J. J., & Fong, C. R. (2004). Growth, nutrient storage, and release of dissolved organic nitrogen by Enteromorpha intestinalis in response to pulses of nitrogen and phosphorus. Aquatic Botany, 78, 83–95.CrossRefGoogle Scholar
  33. Fry, B., Gace, A., & McClelland, J. W. (2003). Chemical indicators of anthropogenic nitrogen loading in four Pacific estuaries. Pacific Science, 57, 77–101.CrossRefGoogle Scholar
  34. Gombach, M., Bressan, G., & Seriani, M. (1992). Microfouling Seasonality in a locality of the Gulf of Trieste (1986–1988). In R. A. Vollenweider, R. Marchetti, & R. Viviani (Eds.), Marine Coastal Eutrophication (pp. 441–443). Oxford: Elsevier.Google Scholar
  35. Hargrave, B. T. (1991). Impacts of man’s activities on aquatic systems. In R. S. K. Barnes, & K. H. Mann (Eds.), Fundamentals of aquatic ecology (pp. 245–264). Oxford: Blackwell.Google Scholar
  36. Hentschel, B. T., & Emlet, R. B. (2000). Metamorphosis of barnacle nauplii: Effects of food variability and a comparison with amphibian models. Ecology, 81, 3495–3508.CrossRefGoogle Scholar
  37. Hindell, J. S., & Quinn, G. P. (2000). Effects of sewage effluent on the population structure of Brachidontes rostratus (Mytilidae) on a temperate intertidal rocky shore. Marine and Freshwater Research, 51, 543–51.CrossRefGoogle Scholar
  38. Hunter, P. R. (2002). Does calculation of the 95th percentile of microbiological results offer any advantage over percentage exceedence in determining compliance with bathing water quality standards. Letters in Applied Microbiology, 34, 283–286.CrossRefGoogle Scholar
  39. Jarrett, J. N., & Pechenik, J. A. (1997). Temporal variation in cyprid quality and juvenile growth capacity for an intertidal barnacle. Ecology, 78, 1262–1265.CrossRefGoogle Scholar
  40. Jones, A. B., O’Donohue, M. J., Udy, J., & Dennison, W. C. (2001). Assessing ecological impacts of shrimp and sewage effluent: Biological indicators with standard water quality analyses. Estuarine and Coastal Shelf Science, 52, 91–109.CrossRefGoogle Scholar
  41. Kamer, K., & Fong, P. (2001). Nitrogen enrichment ameliorates the negative effects of reduced salinity on the green macroalga Enteromorpha intestinalis. Marine Ecology Progress Series, 218, 87–93.CrossRefGoogle Scholar
  42. Kennish, M. J. (1992). Ecology of estuaries: Anthropogenic effects. Boca Raton: CRC.Google Scholar
  43. Kennish, M. J. (2002). Environmental threats and environmental future of estuaries. Environmental Conservation, 29, 78–107.CrossRefGoogle Scholar
  44. Keough, M. J. (1998). Responses of settling invertebrate larvae to the presence of established recruits. Journal of Experimental Marine Biology and Ecology, 231, 1–19.CrossRefGoogle Scholar
  45. Loeb, S. L. (1994). An ecological context for biological monitoring. In S. L. Loeb, & A. Spacie (Eds.), Biological monitoring of aquatic systems (pp. 3–7). Boca Raton: Lewis.Google Scholar
  46. Lopez, C., & Dates, G. (1998). The efforts of community volunteers in assessing watershed ecosystem health. In D. Rapport, R. Costanza, P. R. Epstein, C. Gaudet, & R. Levins (Eds.), Ecosystem health (pp. 103–128). Oxford: Blackwell.Google Scholar
  47. Lotze, H. K., Worm, B., & Sommer, U. (2000). Propagule banks, herbivory and nutrient supply control population development and dominance patterns in macroalgal blooms. Oikos, 89, 46–58.CrossRefGoogle Scholar
  48. MacNally, R. (2000). Regression and model building in conservation biology, biogeography and ecology: The distinction between—and the reconciliation of—‘predictive’ and ‘explanatory’ models. Biodiversity and Conservation, 9, 655–671.CrossRefGoogle Scholar
  49. MacNally, R. (2002). Multiple regression and inference in ecology and conservation biology: Further comments on identifying important predictor variables. Biodiversity and Conservation, 11, 1397–1401.CrossRefGoogle Scholar
  50. Mann, K. H. (2000). Ecology of coastal waters. Oxford: Blackwell.Google Scholar
  51. Martins, I., Oliveira, J. M., Flindt, M. R., & Marques, J. C. (1999). The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal). Acta Oecologica, 20, 259–265.CrossRefGoogle Scholar
  52. McGuiness, K. A. (1989). Effects of some natural and artificial substrata on sessile marine organisms at Galeta Reef, Panama. Marine Ecology Progress Series, 52, 201–208.CrossRefGoogle Scholar
  53. Moreira, J. (2006). Patterns of occurrence of grazing molluscs on sandstone and concrete seawalls in Sydney Harbour (Australia). Molluscan Research, 26, 51–60.Google Scholar
  54. Nordby, C. S., & Zedler, J. B. (1991). Responses of Fish and Macrobenthic Assemblages to Hydrologic Disturbances in Tijuana Estuary and Los Peňasquitos lagoon, California. Estuaries, 14, 80–93.CrossRefGoogle Scholar
  55. Olivier, F., Tremblay, R., Bourget, E., & Rittschof, D. (2000). Barnacle settlement: Field experiments on the influence of larval supply, tidal level, biofilm quality and age on Balanus amphitrite cyprids. Marine Ecology Progress Series, 199, 185–204.CrossRefGoogle Scholar
  56. Paerl, H. W., Pinckney, J. L., Fear, J. M., & Peierls, B. L. (1998). Ecosystem responses to internal and watershed organic matter loading: Consequences for hypoxia in the eutrophying Neuse River Estuary, North Carolina, USA. Marine Ecology Progress Series, 166, 17–25.CrossRefGoogle Scholar
  57. Pech, D., Ardisson, P. L., & Bourget, E. (2002). Settlement of a tropical marine epibenthic assemblage on artificial panels: Influence of substratum heterogeneity and complexity scales. Estuarine and Coastal Shelf Science, 55, 743–750.CrossRefGoogle Scholar
  58. Pierson, W. L., Bishop, K., Van Senden, D., Horton, P. R., & Adamantidis, C. A. (2002). Environmental Flows Initiative Technical Report: Environmental Water Requirements to Maintain Estuarine Processes. Canberra: Environment Australia.Google Scholar
  59. Quinn, G. P., & Keough, M. J. (2002). Experimental design and data analysis for biologists. Cambridge: Cambridge University Press.Google Scholar
  60. Ross, P. M. (2001). Larval supply, settlement and survival of barnacles in a temperate mangrove forest. Marine Ecology Progress Series, 215, 237–249.CrossRefGoogle Scholar
  61. Saiz-Salinas, J. I., & González-Oreja, J. A. (2000). Stress in estuarine communities: Lessons from the highly-impacted Bilbao estuary (Spain). Journal of Aquatic Ecosystem Stress and Recovery, 7, 43–55.CrossRefGoogle Scholar
  62. Sanford, E., & Menge, B. A. (2001). Spatial and temporal variation in barnacle growth in a coastal upwelling system. Marine Ecology Progress Series, 209, 143–157.CrossRefGoogle Scholar
  63. Satumanatpan, S., Keough, M. J., & Watson, G. F. (1999). Role of settlement in determining the distribution and abundance of barnacles in a temperate mangrove forest. Journal of Experimental Marine Biology and Ecology, 241, 45–66.CrossRefGoogle Scholar
  64. Scammell, M., & Besley, C. (1995). Biological indicators pilot study: Intertidal settlement - June 1995, Prepared for Clean Waterways Programme, Sydney Water Corporation, Report No. 95/79.Google Scholar
  65. Sousa, A. I., Martins, I., Lillebø, A. I., Flindt, M. R., & Pardal, M. A. (2007). Influence of salinity, nutrients and light on the germination and growth of Enteromorpha sp. spores. Journal of Experimental Marine Biology and Ecology, 341, 142–150.CrossRefGoogle Scholar
  66. Starr, M., Himmelman, J. H., & Therriault, J. (1991). Coupling of nauplii release in barnacles with phytoplankton blooms: A parallel strategy to that of spawning in urchins and mussels. Journal of Plankton Research, 13, 561–571.CrossRefGoogle Scholar
  67. Tamburri, M. N., Finelli, C. M., Wethey, D. S., & Zimmer-Faust, R. K. (1996). Chemical Induction of Larval Settlement Behavior in Flow. The Biological Bulletin, 191, 367–373.CrossRefGoogle Scholar
  68. Thiyagarajan, V., Hung, O. S., Chiu, J. M. Y., Wu, R. S. S., & Qian, P. Y. (2005). Growth and survival of juvenile barnacle Balanus amphitrite: Interactive effects of cyprid energy reserve and habitat. Marine Ecology Progress Series, 299, 229–237.CrossRefGoogle Scholar
  69. Thrush, S. F., Hewitt, J. E., Cummings, V. J., Green, M. O., Funnell, G. A., & Wilkinson, M. R. (2000). The generality of field experiments: Interactions between local and broad-scale processes. Ecology, 81, 399–415.CrossRefGoogle Scholar
  70. Tremblay, R., Olivier, F., Bourget, E., and Rittschof, D. (2007). Physiological condition of Balanus amphitrite cyprid larvae determines habitat selection success. Marine Ecology Progress Series, 340, 1–8.CrossRefGoogle Scholar
  71. Underwood, A. J. (1997). Experiments in ecology: Their logical design and interpretation using analysis of variance. Cambridge: Cambridge University Press.Google Scholar
  72. UNESCO (1980). UNESCO Technical Papers in Marine Science 1978. Journal of Oceanographic Engineering, Vol.OE-5, No.1, January 1980.Google Scholar
  73. Valiela, I. (1991). Ecology of coastal ecosystems. In R. S. K. Barnes, & K. H. Mann (Eds.), Fundamentals of aquatic ecology (pp. 57–76). Oxford: Blackwell.CrossRefGoogle Scholar
  74. Van Dolah, R. F., Riekerk, G. H. M., Bergquist, D. C., Felber, J., Chestnut, D. E., & Fredrick Holland, A. (2008). Estuarine habitat quality reflects urbanization at large spatial scales in South Carolina’s coastal zone. Science of The Total Environment, 390, 142–154.CrossRefGoogle Scholar
  75. Walsh, C., & MacNally R. (2004). The hier.part package’ available at Accessed 6 August 2008.
  76. Wisely, B., & Blick, R. A. P. (1964). Seasonal abundance of first stage nauplii in 10 species of barnacles at Sydney. Australian Journal of Marine and Freshwater Research, 15, 162–171.CrossRefGoogle Scholar
  77. Worm, B., & Lotze, H. K. (2006). Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnology and Oceanography, 51, 569–579.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Glenn Courtenay
    • 1
  • William Gladstone
    • 2
  • Marcus Scammell
    • 3
  • Renée Kidson
    • 3
  • Julie Wood
    • 3
  1. 1.coEcoTerrigalAustralia
  2. 2.School of Environmental and Life SciencesUniversity of NewcastleOurimbahAustralia
  3. 3.Sydney Water CorporationParramattaAustralia

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