Skip to main content
SpringerLink
Log in

Indicators of environmental stress: cellular biomarkers and reproductive responses in the Sydney rock oyster (Saccostrea glomerata)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

We measured a suite of common biomarker responses for the first time in the Sydney rock oyster Saccostrea glomerata to evaluate their utility as biological effects measures for pollution monitoring. To examine the relationship between biomarker responses and population level effects, fertilisation and embryo development assays were also conducted. Adult oysters were deployed in two contaminated estuaries and a reference estuary in Sydney, Australia. The concentrations of various contaminants (metals and polycyclic aromatic hydrocarbon, PAHs) were quantified in oyster’s tissue from each site and both metals and total PAHs were significantly elevated in contaminated estuaries relative to the reference estuary. Lysosomal membrane destabilisation, lipid peroxidation levels and glutathione (GSH) concentrations were measured in the digestive gland of oysters. Of all biomarkers measured, lysosomal membrane destabilisation proved to be the most useful indicator of oysters facing anthropogenic stress and we suggest this may be an especially useful biomarker for incorporation into local environmental monitoring programs. Moreover, lysosomal membrane destabilisation showed good correlations with fertilisation, normal embryo development and estuary status. GSH and lipid peroxidation were not as valuable for distinguishing between estuaries exposed to differing levels of anthropogenic stress, but did provide additional valuable information regarding overall health status of the oysters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmad I, Oliveira M, Pacheco M, Santos MA (2005) Anguilla anguilla L. oxidative stress biomarkers responses to copper exposure with or without beta-naphthoflavone pre-exposure. Chemosphere 61:267–275

    Article  CAS  Google Scholar 

  • Allen JI, Moore MN (2004) Environmental prognostics: is the current use of biomarkers appropriate for environmental risk evaluation? Mar Environ Res 58:227–232

    Article  Google Scholar 

  • Almroth BC, Albertsson E, Sturve J, Forlin L (2008) Oxidative stress, evident in antioxidant defences and damage products, in rainbow trout caged outside a sewage treatment plant. Ecotoxicol Environ Saf 70:370–378

    Article  Google Scholar 

  • Anderson ME (1985) Determination of glutathione and glutathione disulfide in biological samples. In: Alton M (ed) Methods in enzymology. Academic Press, New York, pp 548–555

    Google Scholar 

  • Andrew MN, O’Connor WA, Dunstan RH, MacFarlane GR (2010) Exposure to 17 alpha-ethynylestradiol causes dose and temporally dependent changes in intersex, females and vitellogenin production in the Sydney rock oyster. Ecotoxicology 19:1440–1451

    Article  CAS  Google Scholar 

  • Auffret M, Rousseau S, Boutet I, Tanguy A, Baron J, Moraga D, Duchemin M (2006) A multiparametric approach for monitoring immunotoxic responses in mussels from contaminated sites in Western Mediterranea. Ecotoxicol Environ Saf 63:393–405

    Article  CAS  Google Scholar 

  • Bebianno MJ, Geret F, Hoarau P, Serafim MA, Coelho MR, Gnassia-Barelli M, Romeo M (2004) Biomarkers in Ruditapes decussatus: a potential bioindicator species. Biomarkers 9:305–330

    Article  CAS  Google Scholar 

  • Bergayou H, Mouneyrac C, Pellerin J, Moukrim A (2009) Oxidative stress responses in bivalves (Scrobicularia plana, Cerastoderma edule) from the Oued Souss estuary (Morocco). Ecotoxicol Environ Saf 72:765–769

    Article  CAS  Google Scholar 

  • Birch GF, Harrington C, Symons RK, Hunt JW (2007) The source and distribution of polychlorinated dibenzo-p-dioxin and polychlorinated dibenzofurans in sediments of Port Jackson, Australia. Mar Pollut Bull 54:295–308

    Article  CAS  Google Scholar 

  • Box A, Sureda A, Galgani F, Pons A, Deudero S (2007) Assessment of environmental pollution at Balearic Islands applying oxidative stress biomarkers in the mussel Mytilus galloprovincialis. Comp Biochem Physiol C Toxicol Pharmacol 146:531–539

    Article  CAS  Google Scholar 

  • Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, Viarengo A (2000) The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247:295–311

    Article  CAS  Google Scholar 

  • Cheung CCC, Siu WHL, Richardson B, De Luca-Abbott SB, Lam PKS (2004) Antioxidant responses to benzo a pyrene and Aroclor 1254 exposure in the green-lipped mussel, Perna viridis. Environ Pollut 128:393–403

    Article  CAS  Google Scholar 

  • Coen LD, Brumbaugh RD, Bushek D, Grizzle R, Luckenbach MW, Posey MH, Powers SP, Tolley SG (2007) Ecosystem services related to oyster restoration. Mar Ecol Prog Ser 341:303–307

    Article  Google Scholar 

  • Company R, Serafim A, Cosson RP, Fiala-Médioni A, Camus L, Colaço A, Serrão-Santos R, Bebianno MJ (2008) Antioxidant biochemical responses to long-term copper exposure in Bathymodiolus azoricus from Menez-Gwen hydrothermal vent. Sci Total Environ 389:407–417

    Article  CAS  Google Scholar 

  • Conners DE, Ringwood AH (2000) Effects of glutathione depletion on copper cytotoxicity in oysters (Crassostrea virginica). Aquat Toxicol 50:341–349

    Article  CAS  Google Scholar 

  • Cossu C, Doyotte A, Babut M, Exinger A, Vasseur P (2000) Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicol Environ Saf 45:106–121

    Article  CAS  Google Scholar 

  • Dafforn KA, Simpson SL, Kelaher BP, Clark GF, Komyakova V, Wong CKC, Johnston EL (2012) The challenge of choosing environmental indicators of anthropogenic impacts in estuaries. Environ Pollut 163:207–217

    Article  CAS  Google Scholar 

  • Devier MH, Augagneur S, Budzinski H, Mora P, Narbonne JF, Garrigues P (2003) Microcosm tributyltin bioaccumulation and multibiomarker assessment in the blue mussel Mytilus edulis. Environ Toxicol Chem 22:2679–2687

    Article  CAS  Google Scholar 

  • Devier MH, Augagneur S, Budzinski H, Le Menach K, Mora P, Narbonne JF, Garrigues P (2005) One-year monitoring survey of organic compounds (PAHs, PCBs, TBT), heavy metals and biomarkers in blue mussels from the Arcachon Bay, France. J Environ Monit 7:224–240

    Article  CAS  Google Scholar 

  • Dondero F, Dagnino A, Jonsson H, Capri F, Gastaldi L, Viarengo A (2006) Assessing the occurrence of a stress syndrome in mussels (Mytilus edulis) using a combined biomarker/gene expression approach. Aquat Toxicol 78:S13–S24

    Article  CAS  Google Scholar 

  • Faria M, Huertas D, Soto DX, Grimalt JO, Catalan J, Riva MC, Barata C (2010) Contaminant accumulation and multi-biomarker responses in field collected zebra mussels (Dreissena polymorpha) and crayfish (Procambarus clarkii), to evaluate toxicological effects of industrial hazardous dumps in the Ebro river (NE Spain). Chemosphere 78:232–240

    Article  CAS  Google Scholar 

  • Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25:272–280

    Article  CAS  Google Scholar 

  • Guimaraes L, Gravato C, Santos J, Monteiro LS, Guilhermino L (2009) Yellow eel (Anguilla anguilla) development in NW Portuguese estuaries with different contamination levels. Ecotoxicology 18:385–402

    Article  CAS  Google Scholar 

  • Gutteridge JMC, Halliwell B (1990) The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci 15:129–135

    Article  CAS  Google Scholar 

  • He ZJ, Morrison RJ (2001) Changes in the marine environment of Port Kembla Harbour, NSW, Australia, 1975–1995: a review. Mar Pollut Bull 42:193–201

    Article  CAS  Google Scholar 

  • Hollows CF, Johnston EL, Marshall DJ (2007) Copper reduces fertilisation success and exacerbates Allee effects in the field. Mar Ecol Prog Ser 333:51–60

    Article  CAS  Google Scholar 

  • Lehtonen KK, Leinio S, Schneider R, Leivuori M (2006) Biomarkers of pollution effects in the bivalves Mytilus edulis and Macoma balthica collected from the southern coast of Finland (Baltic Sea). Mar Ecol Prog Ser 322:155–168

    Article  CAS  Google Scholar 

  • Lewis C, Galloway T (2009) Reproductive consequences of paternal genotoxin exposure in marine invertebrates. Environ Sci Technol 43:928–933

    Article  CAS  Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    Article  CAS  Google Scholar 

  • Livingstone DR, Chipman JK, Lowe DM, Minier C, Mitchelmore CL, Moore MN, Peters LD, Pipe RK (2000) Development of biomarkers to detect the effects of organic pollution on aquatic invertebrates: recent molecular, genotoxic, cellular and immunological studies on the common mussel (Mytilus edulis L.) and other mytilids. Int J Environ Pollut 13:56–91

    Article  CAS  Google Scholar 

  • Lobo J, Costa PM, Caeiro S, Martins M, Ferreira AM, Caetano M, Cesario R, Vale C, Costa MH (2010) Evaluation of the potential of the common cockle (Cerastoderma edule L.) for the ecological risk assessment of estuarine sediments: bioaccumulation and biomarkers. Ecotoxicology 19:1496–1512

    Article  CAS  Google Scholar 

  • Losada S, Roach A, Roosens L, Santos FJ, Galceran MT, Vetter W, Neels H, Covaci A (2009) Biomagnification of anthropogenic and naturally-produced organobrominated compounds in a marine food web from Sydney Harbour, Australia. Environ Int 35:1142–1149

    Article  CAS  Google Scholar 

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30

    Article  CAS  Google Scholar 

  • Lyons BP, Thain JE, Stentiford GD, Hylland K, Davies IM, Vethaak AD (2010) Using biological effects tools to define Good Environmental Status under the European Union Marine Strategy Framework Directive. Mar Pollut Bull 60:1647–1651

    Article  CAS  Google Scholar 

  • Maria VL, Santos MA, Bebianno MJ (2009) Biomarkers of damage and protection in Mytilus galloprovincialis cross transplanted in Ria Formosa Lagoon (Portugal). Ecotoxicology 18:1018–1028

    Article  CAS  Google Scholar 

  • Martins LKP, Nascimento IA, Fillmann G, King R, Evangelista AJA, Readman JW, Depledge MH (2005) Lysosomal responses as a diagnostic tool for the detection of chronic petroleum pollution at Todos os Santos Bay, Brazil. Environ Res 99:387–396

    Article  CAS  Google Scholar 

  • Monserrat JM, Martinez PE, Geracitano LA, Amado LL, Martins CMG, Pinho GLL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C Toxicol Pharmacol 146:221–234

    Article  Google Scholar 

  • Moore MN, Allen JI, McVeigh A (2006) Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 61:278–304

    Article  CAS  Google Scholar 

  • Nicholson S (2001) Ecocytological and toxicological responses to copper in Perna viridis (L.) (Bivalvia: Mytilidae) haemocyte lysosomal membranes. Chemosphere 45:399–407

    Article  CAS  Google Scholar 

  • Niyogi S, Biswas S, Sarker S, Datta AG (2001) Antioxidant enzymes in brackishwater oyster, Saccostrea cucullata as potential biomarkers of polyaromatic hydrocarbon pollution in Hooghly Estuary (India): seasonality and its consequences. Sci Total Environ 281:237–246

    Article  CAS  Google Scholar 

  • Pena-Llopis S, Ferrando MD, Pena JB (2002) Impaired glutathione redox status is associated with decreased survival in two organophosphate-poisoned marine bivalves. Chemosphere 47:485–497

    Article  CAS  Google Scholar 

  • Picado A, Bebianno MJ, Costa MH, Ferreira A, Vale C (2007) Biomarkers: a strategic tool in the assessment of environmental quality of coastal waters. Hydrobiologia 587:79–87

    Article  CAS  Google Scholar 

  • Pinsino A, Turturici G, Sconzo G, Geraci F (2011) Rapid changes in heat-shock cognate 70 levels, heat-shock cognate phosphorylation state, heat-shock transcription factor, and metal transcription factor activity levels in response to heavy metal exposure during sea urchin embryonic development. Ecotoxicology 20:246–254

    Article  CAS  Google Scholar 

  • Regoli F, Frenzilli G, Bocchetti R, Annarumma F, Scarcelli V, Fattorini D, Nigro M (2004) Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment. Aquat Toxicol 68:167–178

    Article  CAS  Google Scholar 

  • Ringwood AH (1992) Comparative sensitivity of gametes and early developmental stages of a sea-urchin species (Ecinometra mathaei) and a bivalve species (Isognomon californicum) during metal exposures. Arch Environ Contam Toxicol 22:288–295

    Article  CAS  Google Scholar 

  • Ringwood AH, Conners DE, Hoguet J (1998) Effects of natural and anthropogenic stressors on lysosomal destabilization in oysters Crassostrea virginica. Mar Ecol Prog Ser 166:163–171

    Article  Google Scholar 

  • Ringwood AH, Conners DE, Keppler CJ, DiNovo AA (1999) Biomarker studies with juvenile oysters (Crassostrea virginica) deployed in situ. Biomarkers 4:400–415

    Article  CAS  Google Scholar 

  • Ringwood AH, Hoguet J, Keppler C, Gielazyn M (2004) Linkages between cellular biomarker responses and reproductive success in oysters—Crassostrea virginica. Mar Environ Res 58:151–155

    Article  CAS  Google Scholar 

  • Ringwood AH, Conners DE, Hoguet J, Ringwood LA (2005) Lysosomal destabilisation assays in estuarine organisms. In: Ostrander GK (ed) Techniques in aquatic toxicology. CRC Press, Taylor and Francis, Boca Raton, pp 287–300

    Google Scholar 

  • Roach AC, Runcie J (1998) Levels of selected chlorinated hydrocarbons in edible fish tissues from polluted areas in the Georges/Cooks Rivers and Sydney Harbour, New South Wales, Australia. Mar Pollut Bull 36:323–344

    Article  CAS  Google Scholar 

  • Roach AC, Muller R, Komarova T, Symons R, Stevenson GJ, Mueller JF (2009) Using SPMDs to monitor water column concentrations of PCDDs, PCDFs and dioxin-like PCBs in Port Jackson (Sydney Harbour), Australia. Chemosphere 75:1243–1251

    Article  CAS  Google Scholar 

  • Romeo M, Hoarau P, Garello G, Gnassia-Barelli M, Girard JP (2003) Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environ Pollut 122:369–378

    Article  CAS  Google Scholar 

  • Scanes PR, Roach AC (1999) Determining natural ‘background’ concentrations of trace metals in oysters from New South Wales, Australia. Environ Pollut 105:437–446

    Article  CAS  Google Scholar 

  • USEPA (1996) Method 3540C Soxlet extraction. US Environmental Protection Agency, Washington

    Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189

    Article  CAS  Google Scholar 

  • Valdez Domingos FX, Azevedo M, Silva MD, Randi MAF, Freire CA, Silva de Assis HC, Oliveira Ribeiro CA (2007) Multibiomarker assessment of three Brazilian estuaries using oysters as bioindicators. Environ Res 105:350–363

    Article  CAS  Google Scholar 

  • van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Viarengo A, Dondero F, Pampanin DM, Fabbri R, Poggi E, Malizia M, Bolognesi C, Perrone E, Gollo E, Cossa GP (2007) A biomonitoring study assessing the residual biological effects of pollution caused by the HAVEN wreck on marine organisms in the Ligurian sea (Italy). Arch Environ Contam Toxicol 53:607–616

    Article  CAS  Google Scholar 

  • Wedderburn J, McFadzen I, Sanger RC, Beesley A, Heath C, Hornsby M, Lowe D (2000) The field application of cellular and physiological biomarkers, in the mussel Mytilus edulis, in conjunction with early life stage bioassays and adult histopathology. Mar Pollut Bull 40:257–267

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was primarily supported by the Australian Research Council through an Australian Research Fellowship awarded to Emma Johnston and the NSW government through an Environmental Trust grant awarded to Anthony Roach. We would like to thank Dr. Katherine Dafforn for her help with this project. We would also like to thank Dr. Stuart Simpson and Chad Jarolimek at the CSIRO Centre for Environmental Contaminants Research for their help with the tissue metals analysis.

Author information

Authors and Affiliations

  1. Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 2052, Australia

    Katelyn J. Edge & Emma L. Johnston

  2. Centre for Ecotoxicology, NSW Office of Environment and Heritage, Lidcombe, NSW, Australia

    Katelyn J. Edge & Anthony C. Roach

  3. Department of Biology, University of North Carolina at Charlotte, 9201 University City Boulevard, Charlotte, NC, 28223, USA

    Amy H. Ringwood

Authors
  1. Katelyn J. Edge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emma L. Johnston
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anthony C. Roach
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amy H. Ringwood
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katelyn J. Edge.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Edge, K.J., Johnston, E.L., Roach, A.C. et al. Indicators of environmental stress: cellular biomarkers and reproductive responses in the Sydney rock oyster (Saccostrea glomerata). Ecotoxicology 21, 1415–1425 (2012). https://doi.org/10.1007/s10646-012-0895-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-012-0895-2

Keywords

Search

Navigation