Abstract
Resistance to heavy metals is a potentially important trait for introduced marine organisms, facilitating their successful invasion into disturbed natural communities. We conducted laboratory and field experiments to examine differential resistance to copper (Cu) between two source populations of the introduced bryozoan Bugula neritina, originating from a polluted (Port Kembla Harbour, NSW, Australia) and an unpolluted (Botany Bay, NSW, Australia) environment. A laboratory toxicity test was conducted to test the relative resistance of B. neritina recruits from the two sources, by measuring the attachment success, survival and growth of individuals exposed to a range of Cu concentrations (0, 25, 50 and 100 μg l−1 Cu). Upon completion, reciprocal transplantation of the colonies to the original polluted and unpolluted locations was carried out to assess ongoing survival and growth of colonies in the field. B. neritina colonies originating from the polluted Port Kembla Harbour had increased resistance to Cu relative to populations from an unpolluted part of Botany Bay. There appeared to be a cost associated with increased metal tolerance. In the laboratory, Botany Bay recruits displayed significantly higher growth in control treatments and significantly poorer growth at 100 μg l−1 Cu with respect to Port Kembla Harbour individuals, which showed unusually uniform and low growth irrespective of Cu concentration. No difference in attachment success or post-metamorphic survival was observed between populations. Field transplantation showed copper resistance in Port Kembla Harbour colonies constituted an advantage in polluted but not benign environments. The findings of this study provide evidence of the benefits to invasive species of pollution tolerance and suggest that human disturbance can facilitate the establishment and spread of invasive species in marine systems.
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References
Apte SC, Day GM (1998) Dissolved metal concentrations in the Torres Strait and Gulf of Papua. Mar Pollut Bull 36:298–304
ASTM (1999) Annual book of ASTM standards, 11.05. American Society for Testing and Materials. West Conshocken, PA
Brown BE (1976) Observations on the tolerance of the isopod Asellus meridianus Rac to copper and lead. Water Res 10:555–559
Brusca RC, Brusca GJ (1990) The lophophorate phyla: phoronids, ectoprocts and branchiopods. In: Brusca RC, Brusca GJ (eds) Invertebrates. Sinauer Associates, Sunderland MA, pp 788
Bryan GW, Hummerstone LG (1971) Adaptations of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of heavy metals. J Mar Biolog Assoc UK 51:845–863
Bryan GW, Hummerstone LG (1973) Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of zinc and cadmium. J Mar Biolog Assoc UK 53:839–857
Buss LW (1986) Competition and community organization on hard surfaces in the sea. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York NY, pp 517–536
Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82
Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–557
Connell JH (1985) The consequences of variation in intertidal settlement vs post-settlement mortality in rocky intertidal communities. J Exp Mar Biol Ecol 93:11–45
Daka ER, Hawkins SJ (2004) Tolerance to heavy metals in Littorina saxatilis from a metal contaminated estuary in the Isle of Man. J Mar Biolog Assoc UK 84:393–400
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Floerl O, Pool TK, Inglis GJ (2004) Positive interactions between nonindigenous species facilitate transport by human vectors. Ecol Appl 14:1724–1736
Fox MD, Fox BJ (1986) The susceptibility of natural communities to invasion. In: Groves RH, Burdon JJ (eds) Ecology of biological invasions: an Australian perspective. Australian Academy of Science, Canberra, pp 57–66
Gordon DP, Mawatari SF (1992) Atlas of marine-fouling Bryozoa of New Zealand ports and harbours. Misc Publ NZ Oceanogr Inst 107:1–52
Grant A, Hateley JG, Jones NV (1989) Mapping the ecological impact of heavy metals on the estuarine polychaete Nereis diversicolor using inherited metal tolerance. Mar Pollut Bull 20:235–238
Hall LW Jr, Scott MC, Killen WD (1998) Ecological risk assessment of copper and cadmium in surface waters of Chesapeake Bay watershed. Environ Toxicol Chem 17:1172–1189
Harper FA, Smith SE, Macnair MR (1997) Can an increased copper requirement in copper-tolerant Mimulus guttatus explain the cost of tolerance? 1 Vegetative growth. New Phytol 136:455–467
Hayes K, Sliwa C, Migus S, McEnnulty F, Dunstan P (2004) National priority pests—part II: ranking of Australian marine pests. CSIRO Marine Research for the Australian Department of Environment and Heritage, Parkes, Australia
He Z, Morrison RJ (2001) Changes in the marine environment of Port Kembla Harbour, NSW, Australia, 1975–1995: a review. Mar Pollut Bull 42:193–201
Hewitt CL, Campbell ML, Thresher RE, Martin RB, Boyd S, Cohen BF, Currie DR, Gomom MF, Keough MJ, Lewis JA, Lockett MM, Mays N, McArthur MA, O’Hara TD, Poore GCB, Ross DJ, Storey MJ, Watson JE, Wilson RS (2004) Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar Biol 144:183–202
Hoare K, Beaumont AR, Davenport J (1995) Variation among populations in the resistance of Mytilus edulis embryos to copper: adaptations to pollution?. Mar Ecol Prog Ser 120:155–161
I.M.O (2001) International conference on the control of harmful anti-fouling systems for ships, adoption of the final act of the conference and any instruments, recommendations and resolutions resulting from the work of the conference. International Maritime Organisation, IMO Headquarters, London, UK, 15 pp
Johnston EL, Keough MJ (2002) Direct and indirect effects of repeated pollution events of marine hard-substrate assemblages. Ecol Appl 12:1212–1228
Johnston EL, Webb J (2000) Novel techniques for field assessment of copper toxicity of fouling assemblages. Biofouling 15:165–173
Kägi JHR, Kojima Y (1987) Chemistry and biochemistry of metallothionein. Experimentia Suppl (Basel) 25:25–61
Keough MJ, Chernoff H (1987) Dispersal and population variation in the bryozoan Bugula neritina. Ecology 68:199–210
Kim S-J, Rodriguez-Lanetty M, Suh J-H, Song J-I (2003) Emergent effects of heavy metal pollution at a population level: Littorina brevicula a study case. Mar Pollut Bull 46:74–80
Klerks PL, Bartholomew PR (1991) Cadmium accumulation and detoxification in a Cd-resistant population of the oligochaete Limnodrilus hoffmeisteri. Aquat Toxicol 19:97–112
Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176:135–141
Klerks PL, Weis JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Pollut 45:173–205
Lam PKS (1996) Interpopulation differences in acute response of Brotia hainanensis (Gastropoda, Prosobranchia) to cadmium: genetic or environmental variance?. Environ Pollut 94:1–7
Lange BW, Langley CH, Stephan W (1990) Molecular evolution of Drosophila metallothionein genes. Genetics 126:921–932
Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15–26
Levinton JS, Suatoni E, Wallace W, Junkins R, Kelaher B, Allen BJ (2003) Rapid loss of genetically based resistance to metals after the cleanup of a Superfund site. Proc Natl Acad Sci USA 100:9889–9891
Long A, Wang W-X (2005) Metallothionein induction and bioaccumulation kinetics of Cd and Ag in the marine fish Terapon jarbua challenged with dietary or waterborne Ag and Cu. Mar Ecol Prog Ser 291:215–226
Luoma SN (1996) The developing framework of marine ecotoxicology: pollutants as a variable in marine ecosystems?. J Exp Mar Biol Ecol 200:29–55
Luoma SN, Phillips DJH (1988) Distribution, variability and impacts of trace elements in San Francisco Bay. Mar Pollut Bull 19:413–425
Macnair MR, Watkins AD (1983) The fitness of the copper tolerance gene of Mimulus guttatus in uncontaminated soil. New Phytol 95:133–137
Marshall DJ (2005) Geographical variation in offspring size effects across generations. Oikos 108:602–608
Minchin D, Gollasch S (2003) Fouling and ships’ hulls: how changing circumstances and spawning events may result in the spread of exotic species. Biofouling 19:111–122
Mokdad R, Debec A, Wegnez M (1987) Metallothionein genes in Drosophila melanogaster constitute a dual system. Proc Natl Acad Sci USA 84:2658–2662
Moran PJ, Grant TR (1989) The effects of industrial pollution on the development and succession of marine fouling communities. Mar Ecol 10:231–246
Odum EP (1985) Trends expected in stressed ecosystems. Bioscience 35:419–422
Ohtake H, Suyemitsu T, Koga M (1983) Sea urchin (Anthocidaris crassispina) egg zinc-binding protein: cellular localization, purification and characterization. Biochem J 211:109–118
Paulson AJ, Curl HCJ, Feely RA (1989) Estimates of trace metal inputs from non-point sources discharged into estuaries. Mar Pollut Bull 20:549–555
Pitt RE (1995) Effects of urban runoff on aquatic biota. In: Hoffman DJ, Rattner BA, Burton GAJ, Cairns JJ (eds) Handbook of ecotoxicology. Lewis Publishers, Boca Raton, FL
Pollard DA, Pethebridge RL (2002) Report on Port of Botany Bay Introduced Marine Pest Species Survey. New South Wales Fisheries Office of Conservation, 40, Cronulla, Australia
Preston BL, Shackelford J (2002) Multiple stressor effects on benthic biodiversity of Chesapeake Bay: implications for ecological risk assessment. Ecotoxicology 11:85–99
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Roesijadi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114
Roesijadi G, Fellingham GW (1987) Influence of Cu, Cd and Zn pre-exposure on Hg toxicity in the mussel Mytilus edulis. Can J Fish Aquat Sci 44:680–684
Roesijadi G, Calabrese A, Nelson DA (1982) Mercury-binding proteins of Mytilus edulis. In: Vernberg WB, Calabrese A, Thurberg FP, Vernberg FJ (eds) Physiological mechanisms of marine pollutant toxicology. Academic, New York NY, pp 75–87
Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632
Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531
Russ GR (1982) Overgrowth in a marine epifaunal community: competitive hierarchies and competitive networks. Oecologia 53:12–19
Rygg B (1985) Effect of sediment copper on benthic fauna. Mar Ecol Prog Ser 25:83–89
Scanes P (1996) ‘Oyster watch’: monitoring trace metal and organochlorine concentrations in Sydney’s coastal waters. Mar Pollut Bull 33:226–238
Schiff K, Diehl D, Valkirs AO (2004) Copper emissions from antifouling paint on recreational vessels. Mar Pollut Bull 48:371–377
Shirley MDF, Sibly RM (1999) Genetic basis of a between-environment trade-off involving resistance to cadmium in Drosophila melanogaster. Evolution 53:826–836
Sibly RM, Calow P (1989) A life-cycle theory of responses to stress. Biol J Linn Soc 37:101–116
Stauber JL, Benning RJ, Hales LT, Eriksen R, Nowak B (2000) Copper bioavailability and amelioration of toxicity in Macquarie Harbour, Tasmania, Australia. Mar Freshw Res 51:1–10
Underwood AJ, Keough MJ (1986) Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York NY, pp 183–200
Viarengo A (1989) Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. Crit Rev Aquat Sci 1:295–317
Weis JS, Weis P (1992) Construction materials in estuaries: reduction in the epibiotic community on chromated copper arsenate (CCA) treated wood. Mar Ecol Prog Ser 83:45–53
Weis JS, Weis P (1996) Reduction in toxicity of chromated copper arsenate (CCA)- treated wood as assessed by community study. Mar Environ Res 41:15–25
Wisely B (1958) The settling and some experimental reactions of a bryozoan larva, Watersipora cucullata (Busk). Aust J Mar Freshw Res 9:362–371
Wright DA (1986) Trace metal uptake and sodium regulation in Gammarus marinus from metal polluted estuaries in England. J Mar Biolog Assoc UK 66:83–92
Wyatt ASJ, Hewitt CL, Walker DI, Ward TJ (2005) Marine introductions in the Shark Bay World Heritage Property, Western Australia: a preliminary assessment. Divers Distrib 11:33–44
Acknowledgements
We are grateful to G. Clark, T. Nelson and K. Lee for their assistance with field and laboratory work. We than K. Gotham, G. Wicks and all the staff of the Caltex Refinery for providing access to Kurnell Pier. We also thank C. Doyle and all the staff of the Port Kembla Ports Authority for access to Port Kembla Harbour. We are indebted to B. Kelaher, G. Clark and K. Wright for their helpful and insightful comments on the original manuscript. R.F.P. was supported throughout this study by an Australian Government Postgraduate Award (APA). This study was partially funded by an Australian Research Council (ARC) Discovery Grant awarded to E.L.J and a PADI Project AWARE grant awarded to R.F.P.
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Piola, R.F., Johnston, E.L. Differential tolerance to metals among populations of the introduced bryozoan Bugula neritina . Marine Biology 148, 997–1010 (2006). https://doi.org/10.1007/s00227-005-0156-5
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DOI: https://doi.org/10.1007/s00227-005-0156-5