Skip to main content

Advertisement

SpringerLink
Log in

Multiple approaches to assess the safety of artisanal marine food in a tropical estuary

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

In this study, metal and metalloid concentrations and pathogens were measured in shellfish at different locations in a tropical estuary, including sites impacted by sewage and industry. Oyster, mangrove snails and mud snails did not exceed Australian and New Zealand Food Standards maximum levels for copper, lead or estimated inorganic arsenic at any site although copper concentrations in oysters and mud snails exceeded generally expected levels at some locations. Bacterial community composition in shellfish was species-specific regardless of location and different to the surrounding water and sediment. In the snails Telescopium telescopium, Terebralia palustris and Nerita balteata, some bacterial taxa differed between sites, but not in Saccostrea cucullata oysters. The abundance of potential human pathogens was very low and pathogen abundance or diversity was not associated with site classification, i.e. sewage impact, industry impact and reference.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • ANZECC. (2000). Australian and New Zealand guidelines for fresh and marine water quality (Vol. 1). Canberra: Australian and New Zealand Environment and Conservation Council and Agriculture Resources Management Council of Australia and New Zealand.

    Google Scholar 

  • Bibby, K., Viau, E., & Peccia, J. (2010). Pyrosequencing of the 16S rRNA gene to reveal bacterial pathogen diversity in biosolids. Water Research, 44(14), 4252–4260. doi:10.1016/j.watres.2010.05.039.

    Article  CAS  Google Scholar 

  • Bigoraj, E., Kwit, E., Chrobocińska, M., & Rzeżutka, A. (2014). Occurrence of norovirus and hepatitis a virus in wild mussels collected from the Baltic Sea. Food and Environmental Virology, 6(3), 207–212. doi:10.1007/s12560-014-9153-5.

    Article  CAS  Google Scholar 

  • Birch, G. F. (2003). A test of normalization methods for marine sediment, including a new post-extraction normalization (PEN) technique. Hydrobiologia, 492(1–3), 5–13.

    Article  CAS  Google Scholar 

  • Bryan, G. W. (1971). The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proceedings of the Royal Society of London. Series B, Biological Sciences, 177(1048), 389–410.

    Article  CAS  Google Scholar 

  • Bryan, G. W. (1979). Bioaccumulation of marine pollutants. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 286(1015), 483–505.

    Article  CAS  Google Scholar 

  • Buchet, J. P., Pauwels, J., & Lauwerys, R. (1994). Assessment of exposure to inorganic arsenic following ingestion of marine organisms by volunteers. Environmental Research, 66(1), 44–51. doi:10.1006/enrs.1994.1043.

    Article  CAS  Google Scholar 

  • Cañigral, I., Moreno, Y., Alonso, J. L., González, A., & Ferrús, M. A. (2010). Detection of Vibrio vulnificus in seafood, seawater and wastewater samples from a Mediterranean coastal area. Microbiological Research, 165(8), 657–664. doi:10.1016/j.micres.2009.11.012.

    Article  Google Scholar 

  • Capone, K. A., Dowd, S. E., Stamatas, G. N., & Nikolovski, J. (2011). Diversity of the human skin microbiome early in life. The Journal of Investigative Dermatology, 131(10), 2026–2032. doi:10.1038/jid.2011.168.

    Article  CAS  Google Scholar 

  • Clements, K., Quilliam, R. S., Jones, D. L., Wilson, J., & Malham, S. K. (2015). Spatial and temporal heterogeneity of bacteria across an intertidal shellfish bed: implications for regulatory monitoring of faecal indicator organisms. Science of the Total Environment, 506-507(C), 1–9. doi:10.1016/j.scitotenv.2014.10.100.

    Article  CAS  Google Scholar 

  • DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., & Andersen, G. L. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72(7), 5069–5072. doi:10.1128/AEM.03006-05.

    Article  CAS  Google Scholar 

  • Dettrick, D., & Schlusser, K. (2006). Report on microbiological results of water, fish and crab sampling in the vicinity of Larrakeyah outfall, Darwin Harbour. Department of Natural Resources, Environment and the Arts, Department of Primary Industries, Fisheries and Mines and Department of Health and Community Services, 1–17.

  • Dowd, S. E., Callaway, T. R., Wolcott, R. D., Sun, Y., McKeehan, T., Hagevoort, R. G., & Edrington, T. S. (2008a). Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiology, 8, 125. doi:10.1186/1471-2180-8-125.

    Article  Google Scholar 

  • Dowd, S. E., Delton Hanson, J., Rees, E., Wolcott, R. D., Zischau, A. M., Sun, Y., White, J., Smith, D. M., Kennedy, J., & Jones, C. E. (2011). Survey of fungi and yeast in polymicrobial infections in chronic wounds. Journal of Wound Care, 20(1), 40–47.

    Article  CAS  Google Scholar 

  • Dowd, S. E., Sun, Y., Wolcott, R. D., Domingo, A., & Carroll, J. A. (2008b). Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned salmonella-infected pigs. Foodborne Pathogens and Disease, 5(4), 459–472. doi:10.1089/fpd.2008.0107.

    Article  CAS  Google Scholar 

  • Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19), 2460–2461. doi:10.1093/bioinformatics/btq461.

    Article  CAS  Google Scholar 

  • Eren, A. M., Zozaya, M., Taylor, C. M., Dowd, S. E., Martin, D. H., & Ferris, M. J. (2011). Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PloS One, 6(10), e26732. doi:10.1371/journal.pone.0026732.

    Article  CAS  Google Scholar 

  • Fortune, J., & Drewry, J. (2011). Darwin harbour region report cards 2011. Department of Natural Resources, Environment, the Arts and Sport. Report Number, 18(2011D), 1–44.

    Google Scholar 

  • French, V. (2013). An investigation of microcontaminant impacts in Darwin Harbour using the tropical marine snail Telescopium telescopium. PhD thesis, Charles Darwin University.

  • FSANZ. (2001). Australia New Zealand Food Standards Code—generally expected levels (GELs) for metal contaminants. Additional guidelines to maximum levels in standard 1.4.1—contaminants and natural toxicants July 2001.

  • FSANZ. (2011). Australia New Zealand Food Standards Code—standard 1.4.1—contaminants and natural toxicants (F2015C00052).

  • Harris, J. M. (1993). The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microbial Ecology, 25(3), 195–231.

    Article  CAS  Google Scholar 

  • Keller, R., Justino, J. F., & Cassini, S. T. (2013). Assessment of water and seafood microbiology quality in a mangrove region in Vitória, Brazil. Journal of Water and Health, 11(3), 573. doi:10.2166/wh.2013.245.

    Article  CAS  Google Scholar 

  • Li, X., Harwood, V. J., Nayak, B., Staley, C., Sadowsky, M. J., & Weidhaas, J. (2015). A novel microbial source tracking microarray for pathogen detection and fecal source identification in environmental systems. Environmental Science & Technology, 49(12), 150527061731002. doi:10.1021/acs.est.5b00980.

    Google Scholar 

  • Loring, D. H., & Rantala, R. T. T. (1992). Manual for the geochemical analyses of marine sediments and suspended particulate matter. Earth-Science Reviews, 32(4), 235–283. doi:10.1016/0012-8252(92)90001-A.

    Article  CAS  Google Scholar 

  • Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

    Article  Google Scholar 

  • Luna, R. A., Fasciano, L. R., Jones, S. C., Boyanton, B. L., Ton, T. T., & Versalovic, J. (2007). DNA pyrosequencing-based bacterial pathogen identification in a pediatric hospital setting. Journal of Clinical Microbiology, 45(9), 2985–2992. doi:10.1128/JCM.00630-07.

    Article  CAS  Google Scholar 

  • Marino, A., Lombardo, L., & Fiorentino, C. (2005). Uptake of Escherichia coli, Vibrio cholerae non-O1 and Enterococcus durans by, and depuration of mussels (Mytilus galloprovincialis). International Journal of Food Microbiology, 99, 281–286.

    Article  Google Scholar 

  • Martinez-Urtaza, J., Saco, M., Hernandez-Cordova, G., Lozano, A., Garcia-Martin, O., & Espinosa, J. (2003). Identification of Salmonella serovars isolated from live molluscan shellfish and their significance in the marine environment. Journal of Food Protection, 66(2), 226–232.

    Article  Google Scholar 

  • Metcalf, T. G., Mullin, B., Eckerson, D., Moulton, E., & Larkin, E. P. (1979). Bioaccumulation and depuration of enteroviruses by the soft-shelled clam, Mya arenaria. Applied and Environmental Microbiology, 38(2), 275–282.

    CAS  Google Scholar 

  • McMurdie, P. J., & Holmes, S. (2014). Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Computational Biology, 1–12. doi:10.1371/journal.pcbi.1003531.

  • Miller, W. A., Miller, M. A., Gardner, I. A., Atwill, E. R., Byrne, B. A., Jang, S., Harris, M., Ames, J., Jessup, D., Paradies, D., Worcester, K., Melli, A., & Conrad, P. A. (2006). Salmonella spp., Vibrio spp., Clostridium perfringens, and Plesiomonas shigelloides in marine and freshwater invertebrates from coastal California ecosystems. Microbial Ecology, 52(2), 198–206. doi:10.1007/s00248-006-9080-6.

    Article  CAS  Google Scholar 

  • Muniain-Mujika, I., Girones, R., Tofino-Quesada, G., Calvo, M., & Lucena, F. (2002). Depuration dynamics of viruses in shellfish. International Journal of Food Microbiology, 77(1–2), 125–133.

    Article  CAS  Google Scholar 

  • Munksgaard, N. C., & Livingstone Parry, D. (2002). Metals, arsenic and lead isotopes in near-pristine estuarine and marine coastal sediments from northern Australia. Marine and Freshwater Research, 53(3), 719. doi:10.1071/MF01060.

    Article  CAS  Google Scholar 

  • Muñoz, O., Devesa, V., Suñer, M. A., & Vélez, D. (2000). Total and inorganic arsenic in fresh and processed fish products. Journal of Agricultural and Food Chemistry, 48, 4369–4376.

    Article  Google Scholar 

  • National Health Medical Research Council (NHMRC). (2008). Guidelines for Managing Risks in Recreational Water, 1–216. Australian Government.

  • Neave, M., Luter, H., Padovan, A., Townsend, S., Schobben, X., & Gibb, K. (2014). Multiple approaches to microbial source tracking in tropical northern Australia. Microbiology Open. doi:10.1002/mbo3.209.

    Google Scholar 

  • Peerzada, N., Eastbrook, C., & Guinea, M. (1990). Heavy metal concentration in Telescopium from Darwin Harbour, N. T., Australia. Marine Pollution Bulletin, 21(6), 307–308.

    Article  CAS  Google Scholar 

  • Peerzada, N., Padovan, A., & Guinea, M. (1993). Concentrations of heavy metals in oysters from the coastline of the northern territory, Australia. Environmental Monitoring and Assessment, 28(2), 101–107. doi:10.1007/bf00547028.

    Article  CAS  Google Scholar 

  • Reid, D. G., Dyal, P., Lozouet, P., Glaubrecht, M., & Williams, S. T. (2008). Mudwhelks and mangroves: the evolutionary history of an ecological association (Gastropoda: Potamididae). Molecular Phylogenetics and Evolution, 47(2), 680–699. doi:10.1016/j.ympev.2008.01.003.

    Article  CAS  Google Scholar 

  • Rippey, S. R. (1994). Infectious diseases associated with molluscan shellfish consumption. Clinical Microbiology Reviews, 7(4), 419–425. doi:10.1128/CMR.7.4.419.

    Article  CAS  Google Scholar 

  • Rojas de Astudillo, L., Chang Yen, I., & Bekele, I. (2005). Heavy metals in sediments, mussels and oysters from Trinidad and Venezuela. Revista de Biología Tropical, 53, 41–51.

    Google Scholar 

  • Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., & Weber, C. F. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23), 7537–7541. doi:10.1128/AEM.01541-09.

    Article  CAS  Google Scholar 

  • Sirot, V., Guérin, T., Volatier, J.-L., & Leblanc, J.-C. (2009). Dietary exposure and biomarkers of arsenic in consumers of fish and shellfish from France. The Science of the Total Environment, 407(6), 1875–1885. doi:10.1016/j.scitotenv.2008.11.050.

    Article  CAS  Google Scholar 

  • Smith, K. F., Schmidt, V., Rosen, G. E., & Amaral-Zettler, L. (2012). Microbial diversity and potential pathogens in ornamental fish aquarium water. PloS One, 7(9), e39971. doi:10.1371/journal.pone.0039971.t002.

    Article  CAS  Google Scholar 

  • Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. -L., & Ideker, T. (2011). Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics, 27(3), 431–432. doi:10.1093/bioinformatics/btq675.

  • Swanson, K. S., Dowd, S. E., Suchodolski, J. S., Middelbos, I. S., Vester, B. M., Barry, K. A., Nelson, K. E., Torralba, M., Henrissat, B., Coutinho, P. M., Cann, I. K. O., White, B. A., & Fahey, G. C. (2011). Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice. The ISME Journal, 5(4), 639–649. doi:10.1038/ismej.2010.162.

    Article  CAS  Google Scholar 

  • Thompson, J. R., Marcelino, L. A., & Polz, M. F. (2005). Diversity, sources, and detection of human bacterial pathogens in the marine environment. In: Belkin & Colwell (Eds.), Oceans and health: pathogens in the marine environment (pp. 29–68). New York: Springer.

  • Wegner, K. M., Volkenborn, N., Peter, H., & Eiler, A. (2013). Disturbance induced decoupling between host genetics and composition of the associated microbiome. BMC Microbiology, 13, 252. doi:10.1186/1471-2180-13-252.

    Article  Google Scholar 

  • Wickham, H. (2009). ggplot2: elegant graphics for data analysis. New York: Springer.

    Book  Google Scholar 

  • Ye, L., & Zhang, T. (2011). Pathogenic bacteria in sewage treatment plants as revealed by 454 pyrosequencing. Environmental Science & Technology, 45(17), 7173–7179. doi:10.1021/es201045e.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Australian Government for ‘Caring for our Country’ funding, administered through Territory Natural Resource Management. We thank Larrakia elders Lorraine Williams, Annie Risk and family, and Leslie Gordon for sharing their traditional knowledge and shellfish sampling and processing.

Author information

Authors and Affiliations

  1. Research Institute of the Environment and Livelihoods, Charles Darwin University, Ellengowan Drive, Darwin, NT, 0810, Australia

    A. C Padovan, N. C. Munksgaard & K. S. Gibb

  2. CSIRO Health and Biosecurity, Australian Animal Health Laboratory, Geelong, Vic, 3220, Australia

    M. J. Neave

Authors
  1. A. C Padovan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. J. Neave
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. C. Munksgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. S. Gibb
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. C Padovan.

Electronic supplementary material

ESM 1

(DOCX 91 kb)

ESM 2

(DOCX 81 kb)

ESM 3

Supplement 3 Rarefaction curves of biota, seawater and sediment samples. (EPS 1622 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Padovan, A.C., Neave, M.J., Munksgaard, N.C. et al. Multiple approaches to assess the safety of artisanal marine food in a tropical estuary. Environ Monit Assess 189, 125 (2017). https://doi.org/10.1007/s10661-017-5842-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-017-5842-5

Keywords

Search

Navigation