Skip to main content

Advertisement

SpringerLink
Log in

Integrated early warning systems in marine bivalves reveal detrimental alterations of coastal habitats

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Several biological levels are considered as signals of environmental perturbations so that integrative biological responses have been proposed in environmental monitoring activities. We evaluated the use of markers in Mytilus galloprovincialis at two different levels (protein nitration and S-nitrosylation, and geometric morphometrics) to investigate the sea coastal environmental status. We studied adductor muscle, digestive gland and valves of mussels collected from 3 sampling sites (2 disturbed + 1 control) in eastern Tyrrhenian Sea, and 2 (1 + 1) in western Ionian Sea. Molecular and morphometric markers showed significant variations in relation to environmental conditions, but the most interesting result was evidenced by the analysis of covariation between both protein post-translational modifications and geometric morphometric descriptors. The main interesting finding regards the relationship between protein nitration values (an irreversible molecular marker) of both adductor muscle and digestive gland, and geometric morphometric descriptors (that are Procrustes’ distances) of valve shapes. Molecular and morphometric markers revealed useful warning systems in detecting environmental changes, even if causes and mechanisms altering both cellular metabolism and shape morphology are still unclear. Our findings suggested that pollutants affected the normal cellular metabolic pathways altering the correct functionality at higher biological levels and producing developmental detrimental noise visible on the shell.

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

Similar content being viewed by others

References

  • Aarab, N., B. F. Godal & R. K. Bechmann, 2011. Seasonal variation of histopathological and histochemical markers of PAH exposure in blue mussel (Mytilus edulis L.). Marine Environmental Research 71: 213–217.

    CAS  PubMed  Google Scholar 

  • Akritas, M. G. & D. N. Politis, 2003. Recent Advances and Trends in Nonparametric Statistics. Elsevier, Amsterdam.

    Google Scholar 

  • Albanese, S., B. De Vivo, A. Lima, D. Cicchella, D. Civitillo & A. Cosenza, 2010. Geochemical baselines and risk assessment of the Bagnoli brownfield site coastal sea sediments (Naples, Italy). Journal of Geochemical Exploration 105: 19–33.

    CAS  Google Scholar 

  • Arndt, U., W. Nobel & B. Schweizer. 1987. Bioindikatoren. Möglichkeiten, Grenzen und neue Erkenntnisse. Verlag, Stuttgart, Germany.

    Google Scholar 

  • Arndt, U., A. Fomin & S. Lorenz. 1996. Bio-Indikation. Neue Entwicklungen, Nomenklatur, synökologische Aspekte. Verlag, Ostfildern, Germany.

    Google Scholar 

  • Baker, L. F., R. S. King, J. M. Unrine, B. T. Castellon, G. V. Lowry & C. W. Matson, 2016. Press or pulse exposures determine the environmental fate of Cerium nanoparticles in stream mesocosms. Environmental Toxicology and Chemistry 35: 1213–1223.

    CAS  PubMed  Google Scholar 

  • Baudrimont, M., J. Schafer, V. Marie, R. Maury-Brachet, C. Bossy, A. Boudou & G. Balnc, 2005. Geochemical survey and metal bioaccumulation of three bivalve species (Crassostrea gigas, Cerastoderma edule and Ruditapes philippinarum) in the Nord Medoc salt marshes (Gironde estuary, France). Science of the Total Environment 337: 265–280.

    CAS  PubMed  Google Scholar 

  • Begliomini, F. N., D. C. Maciel, S. M. de Almeida, D. M. Abessa, L. A. Maranho, C. S. Pereira, G. T. Yogui, E. Zanardi-Lamardo & I. B. Castro, 2017. Shell alterations in limpets as putative biomarkers for multi-impacted coastal areas. Environmental Pollution 226: 494–503.

    CAS  PubMed  Google Scholar 

  • Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248–254.

    CAS  PubMed  Google Scholar 

  • Brenner, M., K. Broeg, S. Frickenhaus, B. H. Buck & A. Koehler, 2014. Multi-biomarker approach using the blue mussel (Mytilus edulis L.) to assess the quality of marine environments: season and habitat-related impacts. Marine Environmental Research 95: 13–27.

    CAS  PubMed  Google Scholar 

  • Cajaraville, M. P., I. Cancio, A. Orbea, X. Lekube & I. Marigómez, 1998. Detection, control and monitoring of pollution using early warning cellular biomarkers: conventional and innovative approaches based on biotechnology. Cuadernos de Investigacion Biologica 20: 545–548.

    Google Scholar 

  • Casadei, M., T. Persichini, F. Polticelli, G. Musci & M. Colasanti, 2008. S-Glutathionylation of metallothioneins by nitrosative/oxidative stress. Experimental Gerontology 43: 415–422.

    CAS  PubMed  Google Scholar 

  • Castro, I. B. & G. Fillmann, 2012. High tributyltin and imposex levels in the commercial muricid Thais chocolata from two peruvian harbor areas. Environmental Toxicology abd Chemestry 31: 955–960.

    CAS  Google Scholar 

  • Castro, I. B., C. A. Rocha-Barreira, M. A. Fernandez & G. Bigatti, 2012. Transplant bioassay induces different imposex responses in two species of the genus Stramonita. Marine Biology Research 8: 397–404.

    Google Scholar 

  • Cheggour, M., A. Chafik, W. J. Langston, G. R. Burt, S. Benbrahim & H. Texier, 2001. Metals in sediments and the edible cockle Cerastoderma edule from two Moroccan Atlantic lagoons: Moulay Bou Selham and Sidi Moussa. Environmental Pollution 115: 149–160.

    CAS  PubMed  Google Scholar 

  • D’Agata, A., S. Fasulo, L. J. Dallas, A. S. Fisher, M. Maisano, J. W. Readman & A. N. Jha, 2014. Enhanced toxicity of ‘bulk’ titanium dioxide compared to ‘fresh’ and ‘aged’ nano-TiO2 in marine mussels (Mytilus galloprovincialis). Nanotoxicology 8: 5549–5558.

    Google Scholar 

  • Di Leonardo, R., A. Mazzola, C. D. Tramati, A. Vaccaro & S. Vizzini, 2014. Highly contaminated areas as sources of pollution for adjoining ecosystems: the case of Augusta Bay (Central Mediterranean). Marine Pollution Bulletin 89: 417–426.

    PubMed  Google Scholar 

  • Dowling, V., B. McDonagh, E. M. Cotter, N. O’Brien, F. van Pelt, J. O’Halloran & D. Sheehan, 2006. Two-dimensional electrophoresis analysis of glutathione affinity-selected proteins from the clam Tapes semidecussatus: evidence for tissue-specific expression of redox proteins. Comparative Biochemestry and Physiology Part D 1: 267–272.

    CAS  Google Scholar 

  • Fasulo, S., G. Guerriero, S. Cappello, M. Colasanti, T. Schettino, C. Leonzio, G. Mancini & R. Gornati, 2015. The “SYSTEMS BIOLOGY” in the study of xenobiotic effects on marine organisms for evaluation of the environmental health status: biotechnological applications for potential recovery strategies. Review on Environmental Sciences and Bio/Technology 14: 339–345.

    CAS  Google Scholar 

  • Figueira, E., A. Lima, D. Branco, V. Quintino, A. M. Rodrigues & R. Freitas, 2011. Health concerns of consuming cockles (Cerastoderma edule L.) from a low contaminated coastal system. Environment International 37: 965–972.

    CAS  PubMed  Google Scholar 

  • Goldberg, E. D. & K. K. Bertine, 2000. Beyond the Mussel Watch – new directions for monitoring marine pollution. Science of the Total Environment 247: 165–174.

    CAS  PubMed  Google Scholar 

  • Gouveia, N., C. R. M. Oliveira, C. P. Martins, L. A. Maranho, C. Dias Seabra Pereira, M. R. de Orte, C. A. Y. Harayashiki, S. M. Almeida & I. B. Castro, 2019. Can shell alterations in limpets be used as alternative biomarkers of coastal contamination? Chemosphere 224: 9–19.

    CAS  PubMed  Google Scholar 

  • Griscom, S. B., S. N. Fisher & S. N. Luoma, 2002. Kinetic modeling of Ag, Cd and Co bioaccumulation in the clam Macoma balthica: quantifying dietary and dissolved sources. Marine Ecology Progression Series 240: 127–141.

    CAS  Google Scholar 

  • Hagger, J. A., M. B. Jones, D. Lowe, D. R. Leonard, R. Owen & T. S. Galloway, 2008. Application of biomarkers for improving risk assessments of chemicals under the Water Framework Directive: a case study. Marine Pollution Bulletin 56: 1111–1118.

    CAS  PubMed  Google Scholar 

  • Hamza-Chaffai, A., 2014. Usefulness of bioindicators and biomarkers in pollution biomonitoring. International Journal of Biotechnology and Wellness, India 3: 19–26.

    Google Scholar 

  • Jordaan, M. S., S. A. Reinecke & A. J. Reinecke, 2013. Biomarker responses and morphological effects in juvenile tilapia Oreochromis mossambicus following sequential exposure to the organophosphate azinphos-methyl. Aquatic Toxicology 144: 133–140.

    PubMed  Google Scholar 

  • Lagadic, L., T. Caquet, J. C. Amiard & T. F. Ramade, 2000. Use of Biomarkers in Monitoring Environmental Health. Science Publishers Inc., Enfield, NH.

    Google Scholar 

  • Langston, W. J., N. D. Pope, P. J. C. Jonas, C. Nikitic, M. D. R. Field, B. Dowell, N. Shillabeer, R. H. Swarbrick & A. R. Brown, 2010. Contaminants in fine sediments and their consequences for biota of the Severn Estuary. Marine Pollution Bulletin 61: 68–82.

    CAS  PubMed  Google Scholar 

  • Lawson, A., 1983. Rank analysis of covariance: alternative approaches. Statistician 32: 331–337.

    Google Scholar 

  • Lecoeur, S., B. Videmann & P. Berny, 2004. Evaluation of metallothionein as a biomarker of single and combined Cd/Cu exposure in Dreissena polymorpha. Environment Research 94: 184–191.

    CAS  Google Scholar 

  • Machreki-Ajmi, M. & A. Hamza-Chaffai, 2008. Assessment of sediment/water contamination by in vivo transplantation of the cockles Cerastoderma glaucum from a non contaminated to a contaminated area by cadmium. Ecotoxicology 17: 802–810.

    CAS  PubMed  Google Scholar 

  • Maisano, M., T. Cappello, A. Natalotto, V. Vitale, V. Parrino, A. Giannetto, S. Oliva, G. Mancini, S. Cappello, A. Mauceri & S. Fasulo, 2016. Effects of petrochemical contamination on caged marine mussels using a multi-biomarker approach: histological changes, neurotoxicity and hypoxic stress. Marine Environmental Research 16: 114–123.

    Google Scholar 

  • Manfrin, A., S. Wuertz, S. Larsen, M. Scalici & M. T. Monaghan, 2018. Stress response of Chironomus riparius to changes in water temperature and oxygen concentrations in a lowland stream. Ecological Indicators 95: 720–725.

    CAS  Google Scholar 

  • Marigómez, I. & L. Baybay-Villacorta, 2003. Pollutant-specific and general lysosomal responses in digestive cells of mussels exposed to model organic chemicals. Aquatic Toxicology 64: 235–257.

    PubMed  Google Scholar 

  • Márquez, F., R. González-José & G. Bigatti, 2011. Combined methods to detect pollution effects on shell shape and structure in Neogastropods. Ecological Indicators 11: 248–254.

    Google Scholar 

  • McCarty, L. S., M. Power & K. R. Munkittrick, 2002. Bioindicators versus biomarkers in ecological risk assessment. Human Ecology Risk and Assessment 8: 159–164.

    Google Scholar 

  • McDonagh, B. & D. Sheehan, 2008. Effects of oxidative stress on protein thiols and disulphides in Mytilus edulis revealed by proteomics: actin and protein disulphide isomerase are redox targets. Marine Environment Research 66: 193–195.

    CAS  Google Scholar 

  • McDonagh, B., R. Tyther & D. Sheehan, 2005. Carbonylation and glutathionylation of proteins in the blue mussel Mytilus edulis detected by proteomic analysis and Western blotting: actin as a target for oxidative stress. Aquatic Toxicology 73: 315–326.

    CAS  PubMed  Google Scholar 

  • McDonagh, B., R. Tyther & D. Sheehan, 2006. Redox proteomics in the mussel, Mytilus edulis. Marine Environment Research 62: 101–104.

    Google Scholar 

  • Mc Geoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181–201.

    Google Scholar 

  • Mercogliano, R., S. Santonicola, A. De Felice, A. Anastasio, N. Murru, M. C. Ferrante & M. L. Cortesi, 2016. Occurrence and distribution of polycyclic aromatic hydrocarbons in mussels from the gulf of Naples Tyrrhenian Sea, Italy. Marine Pollution Bulletin 104: 386–390.

    CAS  PubMed  Google Scholar 

  • Metian, M., L. Charbonnier, F. Oberhaensli, P. Bustamante, R. Jeffree, J. C. Amiard & M. Warnau, 2009. Assessment of metal, metalloid, and radionuclide bioaccessibility from mussels to human consumers, using centrifugation and simulated digestion methods coupled with radiotracer techniques. Ecotoxicology and Environmental Safety 72: 1499–1502.

    CAS  PubMed  Google Scholar 

  • Monnet, C., C. Zollikofer, H. Bucher & N. Goudemand, 2009. Three-dimensional morphometric ontogeny of mollusc shells by micro-computed tomography and geometric analysis. Palaeontology Electronica 12: 13p.

    Google Scholar 

  • Moore, M. N., M. H. Depledge, J. W. Readman & D. R. P. Leonard, 2004. An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutagenesis Research 552: 247–268.

    CAS  Google Scholar 

  • Nuñez, J. D., M. V. Laitano & M. Cledón, 2012. An intertidal limpet species as a bioindicator: pollution effects reflected by shell characteristics. Ecological Indicators 14: 178–183.

    Google Scholar 

  • Peakall, D. B. & C. H. Walker, 1996. Commentary. Ecotoxicology 5: 22.

    Google Scholar 

  • Phelps, H., J. Hardy, W. Pearson & C. Apts, 1983. Clam burrowing behaviour: inhibition by copper-enriched sediment. Marine Pollution Bulletin 14: 452–455.

    CAS  Google Scholar 

  • Ramos-Gomez, J., A. Coz, J. R. Viguri, A. Luque, M. L. Martin-Diaz & T. A. Del Valls, 2011. Biomarker responsiveness in different tissues of caged Ruditapes philippinarum and its use within an integrated sediment quality assessment. Environmental Pollution 159: 1914–1922.

    CAS  PubMed  Google Scholar 

  • Romano, E., L. Bergamin, M. G. Finoia, M. G. Carboni, S. Ausili & M. Gabellini, 2008. Industrial pollution at Bagnoli (Naples, Italy): benthic foraminifera as a tool in integrated programs of environmental characterisation. Marine Pollution Bulletin 56: 439–457.

    CAS  PubMed  Google Scholar 

  • Roméo, M. & M. Gnassia-Barelli, 1997. Effect of heavy metals on lipid peroxidation in the Mediterranean clam Ruditapes decussatus. Comparative Biochemistry and Physiology 118C: 33–37.

    Google Scholar 

  • Rossi, F., S. Palombella, C. Pirrone, G. Mancini, G. Bernardini & R. Gornati, 2016. Evaluation of tissue morphology and gene expression as biomarkers of pollution in mussel Mytilus galloprovincialis caging experiment. Aquatic Toxicology 181: 57–66.

    CAS  PubMed  Google Scholar 

  • Scalici, M., L. Traversetti, V. Malafoglia, T. Persichini & M. Colasanti, 2015. Concepts and tools for exploiting sessile bio-filters as early warning elements: introductory applications for marine ecosystem preservation. Invertebrate Survival Journal 12: 278–286.

    Google Scholar 

  • Scalici, M., L. Traversetti, F. Spani, R. Bravi, V. Malafoglia, T. Persichini & M. Colasanti, 2016. Using 3D virtual surfaces to investigate molluscan shell shape. Aquatic Living Research 29: 207.

    Google Scholar 

  • Scalici, M., L. Traversetti, F. Spani, V. Malafoglia, M. Colamartino, T. Persichini, S. Cappello, G. Mancini, G. Guerriero & M. Colasanti, 2017. Shell fluctuating asymmetry in sea-dwelling benthic bivalves as morphological markers to detect environmental chemical contamination. Ecotoxicology 26: 396–404.

    CAS  PubMed  Google Scholar 

  • Serafim, A. & M. J. Bebiano, 2010. Effect of a polymetallic mixture on metal accumulation and metallothionein response in the clam Ruditapes decussatus. Aquatic Toxicology 99: 370–378.

    CAS  PubMed  Google Scholar 

  • Shugart, L. R., J. F. McCarthy, S. J. D’Surney, M. S. Greeley & C. G. Hull, 1990. Molecular and cellular markers of toxicity in the Japanese medaka (Oryzias latipes). In Gardner Jr., H.S. (ed), Compendium of the FY 1990 & FY 1992 Research Reviews for the Research Method Branch. Report/MD-21702-5010. U.S. Army Biomedical Research & development Laboratory Fort Detrick Frederick: 34–51.

  • Shugart, L. R., J. F. McCarthy & R. S. Halbrook, 1992. Biological markers of environmental and ecological contamination: an overview. Risk Analysis 12: 353–360.

    CAS  PubMed  Google Scholar 

  • Smaoui-Damak, W., B. Berthet & A. Hamza-Chaffai, 2009. In situ potential use of metallothionein as a biomarker of cadmium contamination in Ruditapes decussatus. Ecotoxicology and Environmental Safety 72: 1489–1498.

    CAS  PubMed  Google Scholar 

  • Stankovic, S., M. Jovic, R. Milanov & D. Joksimovic, 2011. Trace elements concentrations (Zn, Cu, Pb, Cd, As and Hg) in the Mediterranean mussel (Mytilus galloprovincialis) and evaluation of mussel quality and possible human health risk from cultivated and wild sites of the southeastern Adriatic Sea, Montenegro. Journal of Serbian Chemistry Society 76: 1725–1737.

    CAS  Google Scholar 

  • Traversetti, L., F. Del Grosso, V. Malafoglia, M. Colasanti, S. Ceschin, S. Larsen & M. Scalici, 2017. The Hydra regeneration assay reveals ecological risks in running waters: a new proposal to detect environmental teratogenic threats. Ecotoxicology 26: 184–195.

    CAS  PubMed  Google Scholar 

  • Van Gestel, C. A. M. & T. C. Van Brummelen, 1996. Incorporation of the biomarker concept in ecotoxicology calls for a redefinition of terms. Ecotoxicology 5: 217–225.

    PubMed  Google Scholar 

  • Viarengo, A. & J. A. Nott, 1993. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comparative Biochemistry and Physiology Part C 104: 355–372.

    Google Scholar 

  • Viarengo, A., D. Lowe, C. Bolognesi, E. Fabbri & A. Koehler, 2007. The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant induced stress syndrome in sentinel organisms. Comparative Biochemistry and Physiology 146: 281–300.

    CAS  PubMed  Google Scholar 

  • Wang, Z. S., C. Z. Yan, C. D. Vulpe, Y. J. Yan & Q. Q. Chi, 2012. Incorporation of in situ exposure and biomarkers response in clams Ruditapes philippinarum for assessment of metal pollution in coastal areas from the Maluan Bay of China. Marine Pollution Bulletin 64: 90–98.

    CAS  PubMed  Google Scholar 

  • Zwick, W. R. & W. F. Velicer, 1986. Comparison of five rules for determining the number of components to retain. Psychological Bulletin 99: 432–442.

    Google Scholar 

Download references

Acknowledgements

We are indebted to two anonymous reviewers, whose comments helped to improve the quality of text and contents, and to a professional mother tongue for the language revision. This investigation was supported by the SYSTEMS BIOLOGY project (coordinated by Prof. S. Fasulo, University of Messina, Grant Number 2010ARBLT7_001/008) and by the Grant of Excellence Departments, MIUR-Italy (ARTICOLO 1, COMMI 314 – 337 LEGGE 232/2016).

Author information

Authors and Affiliations

  1. Department of Sciences, University Roma Tre, Viale Guglielmo Marconi 446, 00146, Rome, Italy

    Massimiliano Scalici, Monica Colamartino, Federica Spani, Lorenzo Traversetti, Tiziana Persichini & Marco Colasanti

  2. Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Viale Ferdinando Stagno d’Alcontres 31, 98166, Messina, Italy

    Maria Maisano & Salvatore Fasulo

Authors
  1. Massimiliano Scalici
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monica Colamartino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Federica Spani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lorenzo Traversetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tiziana Persichini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Maisano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Salvatore Fasulo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marco Colasanti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Massimiliano Scalici.

Additional information

Handling editor: Manuel Lopes Lima

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Supplementary material 2 (DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Scalici, M., Colamartino, M., Spani, F. et al. Integrated early warning systems in marine bivalves reveal detrimental alterations of coastal habitats. Hydrobiologia 847, 2573–2585 (2020). https://doi.org/10.1007/s10750-020-04275-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-020-04275-1

Keywords

Search

Navigation