Identifying Toxic Impacts of Metals Potentially Released during Deep-Sea Mining—A Synthesis of the Challenges to Quantifying Risk

In January 2017, the International Seabed Authority released a discussion paper on the development of Environmental Regulations for deep-sea mining within the Area Beyond National Jurisdiction (the ‘Area’). With the release of this paper, the prospect for commercial mining in the Area within the next decade has become very real. Moreover, within nations’ Exclusive Economic Zones, the exploitation of deep-sea mineral ore resources could take place on very much shorter time scales and, indeed, may have already started. However, potentially toxic metal mixtures may be released at sea during different stages of the mining process and in different physical phases (dissolved or particulate). As toxicants, metals can disrupt organism physiology and performance, and therefore may impact whole populations, leading to ecosystem scale effects. A challenge to the prediction of toxicity is that deep-sea ore deposits include complex mixtures of minerals, including potentially toxic metals such as copper, cadmium, zinc, and lead, as well as rare earth elements. Whereas the individual toxicity of some of these dissolved metals has been established in laboratory studies, the complex and variable mineral composition of seabed resources makes the a priori prediction of the toxic risk of deep-sea mining extremely challenging. Furthermore, although extensive data quantify the toxicity of metals in solution in shallow-water organisms, these may not be representative of the toxicity in deep-sea organisms, which may differ biochemically and physiologically and which will experience those toxicants under conditions of low temperature, high hydrostatic pressure, and potentially altered pH. In this synthesis, we present a summation of recent advances in our understanding of the potential toxic impacts of metal exposure to deep-sea meio- to megafauna at low temperature and high pressure, and consider the limitation of deriving lethal limits based on the paradigm of exposure to single metals in solution. We consider the potential for long-term and far-field impacts to key benthic invertebrates, including the very real prospect of sub-lethal impacts and behavioural perturbation of exposed species. In conclusion, we advocate the adoption of an existing practical framework for characterising bulk resource toxicity in advance of exploitation.

[1]  J. R. García-March,et al.  Shell gaping behaviour of Pinna nobilis L., 1758: circadian and circalunar rhythms revealed by in situ monitoring , 2008 .

[2]  T. Crompton Toxicants in the aqueous ecosystem , 1997 .

[3]  F. Biandolino,et al.  Effects of temperature on the acute toxicity of cadmium to Corophium Insidiosum , 2007, Environmental monitoring and assessment.

[4]  Temel Oguz,et al.  Modeling dissolved oxygen dynamics and hypoxia , 2010 .

[5]  A. Ivanina,et al.  Effects of cadmium exposure on expression and activity of P-glycoprotein in eastern oysters, Crassostrea virginica Gmelin. , 2008, Aquatic toxicology.

[6]  Adrian G. Glover,et al.  Insights into the abundance and diversity of abyssal megafauna in a polymetallic-nodule region in the eastern Clarion-Clipperton Zone , 2016, Scientific Reports.

[7]  John P Sumpter,et al.  Towards improved behavioural testing in aquatic toxicology: Acclimation and observation times are important factors when designing behavioural tests with fish. , 2017, Chemosphere.

[8]  Ana Colaço,et al.  A primer for the Environmental Impact Assessment of mining at seafloor massive sulfide deposits , 2013 .

[9]  S. Simpson,et al.  Slow avoidance response to contaminated sediments elicits sublethal toxicity to benthic invertebrates. , 2013, Environmental science & technology.

[10]  Jingjin Pan,et al.  Trace Metal Mixture Toxicity in Aquatic Organism Reviewed from a Biotoxicity Perspective , 2015 .

[11]  Introduction: mechanisms of metal toxicity special issue. , 2010, Chemical research in toxicology.

[12]  W. Hagen,et al.  Trophic interactions and life strategies of epi- to bathypelagic calanoid copepods in the tropical Atlantic Ocean , 2014 .

[13]  M. Kawachi,et al.  Leaching of Metals and Metalloids from Hydrothermal Ore Particulates and Their Effects on Marine Phytoplankton , 2017, ACS omega.

[14]  P. Lucas,et al.  New electroantennography method on a marine shrimp in water , 2016, Journal of Experimental Biology.

[15]  Kamil Kuča,et al.  Redox- and non-redox-metal-induced formation of free radicals and their role in human disease , 2015, Archives of Toxicology.

[16]  Brennan T. Phillips Beyond the vent: New perspectives on hydrothermal plumes and pelagic biology , 2017 .

[17]  R. Danovaro,et al.  Seafloor heterogeneity influences the biodiversity–ecosystem functioning relationships in the deep sea , 2016, Scientific Reports.

[18]  M. Bebianno,et al.  Environmental hazard assessment of a marine mine tailings deposit site and potential implications for deep-sea mining. , 2017, Environmental pollution.

[19]  T. Wolff Composition and endemism of the deep-sea hydrothermal vent fauna , 2005 .

[20]  T. A. DelValls,et al.  Integrative sediment quality assessment using a biomarker approach: review of 3 years of field research , 2008, Cell Biology and Toxicology.

[21]  F. D. De Leo,et al.  Abyssal food limitation, ecosystem structure and climate change. , 2008, Trends in ecology & evolution.

[22]  S. Simpson,et al.  Demonstrating the appropriateness of developing sediment quality guidelines based on sediment geochemical properties. , 2013, Environmental science & technology.

[23]  S. Matondkar,et al.  Impacts on Surface Productivity during Sediment Dispersal Experiment in Central Indian Basin , 2005 .

[24]  P. A. Lewis,et al.  Differences in acute toxicity test results of three reference toxicants on Daphnia at two temperatures , 1991 .

[25]  M. Bebianno,et al.  Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. , 2004, Marine environmental research.

[26]  P. Legendre,et al.  Biodiversity patterns, environmental drivers and indicator species on a high-temperature hydrothermal edifice, Mid-Atlantic Ridge , 2015 .

[27]  S. Simpson,et al.  Predicting metal toxicity in sediments: A critique of current approaches , 2007, Integrated environmental assessment and management.

[28]  F. Onorati,et al.  Assessing sediment hazard through a weight of evidence approach with bioindicator organisms: a practical model to elaborate data from sediment chemistry, bioavailability, biomarkers and ecotoxicological bioassays. , 2011, Chemosphere.

[29]  A. Khodadoust,et al.  Effect of temperature on heavy metal toxicity to juvenile crayfish, Orconectes immunis (Hagen) , 2006, Environmental toxicology.

[30]  Alastair Brown,et al.  A comparative experimental approach to ecotoxicology in shallow-water and deep-sea holothurians suggests similar behavioural responses. , 2017, Aquatic toxicology.

[31]  M. Hannington,et al.  Subsea mining moves closer to shore , 2017 .

[32]  Horst U Oebius,et al.  Parametrization and evaluation of marine environmental impacts produced by deep-sea manganese nodule mining , 2001 .

[33]  M. Bebianno,et al.  Development of an ecotoxicological protocol for the deep-sea fauna using the hydrothermal vent shrimp Rimicaris exoculata. , 2016, Aquatic toxicology.

[34]  M. Bebianno,et al.  The effect of cadmium on antioxidant responses and the susceptibility to oxidative stress in the hydrothermal vent mussel Bathymodiolus azoricus , 2006 .

[35]  S. Simpson,et al.  Sediment Toxicity Testing , 2016 .

[36]  I. Sokolova,et al.  Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change , 2008 .

[37]  S. Simpson,et al.  Sub-lethal effects of copper to benthic invertebrates explained by sediment properties and dietary exposure. , 2012, Environmental science & technology.

[38]  M. Aschner,et al.  Revelations from the Nematode Caenorhabditis elegans on the Complex Interplay of Metal Toxicological Mechanisms , 2011, Journal of toxicology.

[39]  S. Petersen,et al.  Oxidative dissolution of hydrothermal mixed-sulphide ore: An assessment of current knowledge in relation to seafloor massive sulphide mining , 2017 .

[40]  B. Berthet,et al.  Metal transfer in marine food chains: bioaccumulation and toxicity. , 1993, Acta biologica Hungarica.

[41]  H. Setälä,et al.  Using the Copse snail Arianta arbustorum (Linnaeus) to Detect Repellent Compounds and theQuality ofwoodVinegar , 2015 .

[42]  Edison Barbieri,et al.  Efeito do cádmio e zinco na excreção de amônia e consumo de oxigênio do camarão sete-barbas, de acordo com a temperatura , 2013 .

[43]  P. Sarradin,et al.  The influence of nutritional conditions on metal uptake by the mixotrophic dual symbiosis harboring vent mussel Bathymodiolus azoricus. , 2011, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[44]  M. Hannington,et al.  News from the seabed – Geological characteristics and resource potential of deep-sea mineral resources , 2016 .

[45]  Karla,et al.  EFFECTS OF CADMIUM AND ZINC ON OXYGEN CONSUMPTION AND AMMONIA EXCRETION OF THE SEA-BOB SHRIMP, ACCORDING TO THE TEMPERATURE* , 2013 .

[46]  Bruce H Robison,et al.  Conservation of Deep Pelagic Biodiversity , 2009, Conservation biology : the journal of the Society for Conservation Biology.

[47]  I. Sokolova,et al.  Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. , 2012, Marine environmental research.

[48]  B. D. Smith,et al.  Pathways of trace metal uptake in the lugworm Arenicola marina. , 2009, Aquatic toxicology.

[49]  F. Denis,et al.  Do organisms living around hydrothermal vent sites contain specific metallothioneins? The case of the genus Bathymodiolus (Bivalvia, Mytilidae). , 2004, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[50]  E. Ramirez-Llodra,et al.  An ecosystem-based deep-ocean strategy , 2017, Science.

[51]  S. Simpson,et al.  The mismatch between bioaccumulation in field and laboratory environments: Interpreting the differences for metals in benthic bivalves. , 2015, Environmental pollution.

[52]  A. Ivanina,et al.  Effects of cadmium on cellular protein and glutathione synthesis and expression of stress proteins in eastern oysters, Crassostrea virginica Gmelin , 2008, Journal of Experimental Biology.

[53]  C. German,et al.  Evolution and Biogeography of Deep-Sea Vent and Seep Invertebrates , 2002, Science.

[54]  Herbert E. Allen,et al.  Ecotoxicology of metals in aquatic sediments : binding and release, bioavailability, risk assessment, and remediation , 1998 .

[55]  G. Tokuda,et al.  Occurrence and recent long-distance dispersal of deep-sea hydrothermal vent shrimps , 2006, Biology Letters.

[56]  M. Bebianno,et al.  Integrated approach to assess ecosystem health in harbor areas. , 2015, The Science of the total environment.

[57]  A. Soares,et al.  Exploitation of deep-sea resources: the urgent need to understand the role of high pressure in the toxicity of chemical pollutants to deep-sea organisms. , 2014, Environmental pollution.

[58]  S. Valsecchi,et al.  Importance of dietary uptake of trace elements in the benthic deposit-feeding Lumbriculus variegatus , 2012 .

[59]  P. Calow,et al.  Ecotoxicology , 2019, Encyclopedia of Theoretical Ecology.

[60]  M. Johnson,et al.  Accumulation of Lead, Zinc, and Cadmium in a Wild Population of Clethrionomys glareolus from an Abandoned Lead Mine , 2003, Archives of environmental contamination and toxicology.

[61]  J. Gordon Deep-water fisheries at the Atlantic frontier , 2001 .

[62]  A. Booth,et al.  Characterisation of fine-grained tailings from a marble processing plant and their acute effects on the copepod Calanus finmarchicus. , 2017, Chemosphere.

[63]  M. Bebianno,et al.  Temporal variation in the antioxidant defence system and lipid peroxidation in the gills and mantle of hydrothermal vent mussel Bathymodiolus azoricus , 2006 .

[64]  A. Tchesunov,et al.  Description of two free-living nematode species of Halomonhystera disjuncta complex (Nematoda: Monhysterida) from two peculiar habitats in the sea , 2014, Helgoland Marine Research.

[65]  M. Jonker,et al.  Significance testing of synergistic/antagonistic, dose level‐dependent, or dose ratio‐dependent effects in mixture dose‐response analysis , 2005, Environmental toxicology and chemistry.

[66]  W. Clements,et al.  Effects of Metals on Stream Macroinvertebrate Assemblages from Different Altitudes , 1996 .

[67]  V. Riou,et al.  Physiological impacts of acute Cu exposure on deep-sea vent mussel Bathymodiolus azoricus under a deep-sea mining activity scenario. , 2017, Aquatic toxicology.

[68]  May Gómez,et al.  Modeling vertical carbon flux from zooplankton respiration , 2013 .

[69]  A. Koschinsky,et al.  Importance of different types of marine particles for the scavenging of heavy metals in the deep-sea bottom water , 2003 .

[70]  M. Bebianno,et al.  Antioxidant biochemical responses to long-term copper exposure in Bathymodiolus azoricus from Menez-Gwen hydrothermal vent , 2007 .

[71]  M. Bebianno,et al.  Adaptation to metal toxicity: a comparison of hydrothermal vent and coastal shrimps , 2007 .

[72]  M. Bebianno,et al.  Adaptation of the antioxidant defence system in hydrothermal-vent mussels (Bathymodiolus azoricus) transplanted between two Mid-Atlantic Ridge sites , 2007 .

[73]  M. Aresta,et al.  Impact of heavy metals and PCBs on marine picoplankton , 2006, Environmental toxicology.

[74]  Sven Thatje,et al.  The Effects of Temperature and Hydrostatic Pressure on Metal Toxicity: Insights into Toxicity in the Deep Sea. , 2017, Environmental science & technology.

[75]  L. Levin,et al.  Incorporating ecosystem services into environmental management of deep-seabed mining , 2017 .

[76]  J. Keaney,et al.  Role of oxidative modifications in atherosclerosis. , 2004, Physiological reviews.

[77]  J. Powell,et al.  Enrichment in Trace Metals (Al, Mn, Co, Cu, Mo, Cd, Fe, Zn, Pb and Hg) of Macro-Invertebrate Habitats at Hydrothermal Vents Along the Mid-Atlantic Ridge , 2005, Hydrobiologia.

[78]  Ann Vanreusel,et al.  Threatened by mining, polymetallic nodules are required to preserve abyssal epifauna , 2016, Scientific Reports.

[79]  C. Liao,et al.  Sensory determinants of valve rhythm dynamics provide in situ biodetection of copper in aquatic environments , 2016, Environmental Science and Pollution Research.

[80]  Cindy Lee Van Dover,et al.  Defining “serious harm” to the marine environment in the context of deep-seabed mining , 2016 .

[81]  Mike Roberts,et al.  Principles of sound ecotoxicology. , 2014, Environmental science & technology.

[82]  W. Munns,et al.  Assessing and managing multiple risks in a changing world—The Roskilde recommendations , 2017, Environmental toxicology and chemistry.

[83]  P. Tyler,et al.  Microdistribution of Faunal Assemblages at Deep-Sea Hydrothermal Vents in the Southern Ocean , 2012, PloS one.

[84]  Sebastiaan A L M Kooijman,et al.  Making Sense of Ecotoxicological Test Results: Towards Application of Process-based Models , 2006, Ecotoxicology.

[85]  Michael F. Vardaro,et al.  Climate variation, carbon flux, and bioturbation in the abyssal North Pacific , 2009 .

[86]  Silvia Giuliani,et al.  A multidisciplinary weight of evidence approach for environmental risk assessment at the Costa Concordia wreck: Integrative indices from Mussel Watch. , 2014, Marine environmental research.

[87]  Antonio Ayala,et al.  Lipid Peroxidation: Production, Metabolism, and Signaling Mechanisms of Malondialdehyde and 4-Hydroxy-2-Nonenal , 2014, Oxidative medicine and cellular longevity.

[88]  F. Piva,et al.  Environmental hazards from natural hydrocarbons seepage: integrated classification of risk from sediment chemistry, bioavailability and biomarkers responses in sentinel species. , 2014, Environmental pollution.

[89]  Steven D. Scott,et al.  Deep Ocean Mining , 2001 .

[90]  Michiel Rutgers,et al.  Integration of bioavailability, ecology and ecotoxicology by three lines of evidence into ecological risk indexes for contaminated soil assessment. , 2008, The Science of the total environment.

[91]  R. Byrne,et al.  Acid-Base Balance during Emergence in the Freshwater Bivalve Corbicula fluminea , 1991, Physiological Zoology.

[92]  K. McPhail,et al.  Deep-sea hydrothermal vents: potential hot spots for natural products discovery? , 2010, Journal of natural products.

[93]  P. Rainbow Trace metal bioaccumulation: models, metabolic availability and toxicity. , 2007, Environment international.

[94]  R. Gates,et al.  Improving the ecological relevance of toxicity tests on scleractinian corals: Influence of season, life stage, and seawater temperature. , 2016, Environmental pollution.

[95]  R. Aitken,et al.  Antioxidant systems and oxidative stress in the testes , 2008, Oxidative medicine and cellular longevity.

[96]  J Salánki,et al.  Avoidance responses to aluminium in the freshwater bivalve Anodonta cygnea. , 2001, Aquatic toxicology.

[97]  Lene Buhl-Mortensen,et al.  Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins , 2010 .

[98]  M. Lam,et al.  The difference between temperate and tropical saltwater species' acute sensitivity to chemicals is relatively small. , 2014, Chemosphere.

[99]  A. Rowden,et al.  Seafloor massive sulfide deposits support unique megafaunal assemblages: Implications for seabed mining and conservation. , 2016, Marine environmental research.

[100]  H. Harden‐Davies Deep-sea genetic resources: new frontiers for science and stewardship in areas beyond national jurisdiction , 2017 .

[101]  L. Schiesari,et al.  Biogeographic Biases in Research and Their Consequences for Linking Amphibian Declines to Pollution , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[102]  A. Hoffmann,et al.  Ecological evidence links adverse biological effects to pesticide and metal contamination in an urban Australian watershed , 2014 .

[103]  C. Smith,et al.  The deep-sea floor ecosystem: current status and prospects of anthropogenic change by the year 2025 , 2003, Environmental Conservation.

[104]  A. Hendriks,et al.  Temperature-dependent effects of cadmium on Daphnia magna: accumulation versus sensitivity. , 2003, Environmental science & technology.

[105]  I. Sokolova,et al.  Combined effects of temperature acclimation and cadmium exposure on mitochondrial function in eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae) , 2006, Environmental toxicology and chemistry.

[106]  F. Onorati,et al.  A multidisciplinary weight of evidence approach for classifying polluted sediments: Integrating sediment chemistry, bioavailability, biomarkers responses and bioassays. , 2012, Environment international.

[107]  P. Chapman,et al.  Global geographic differences in marine metals toxicity. , 2006, Marine pollution bulletin.

[108]  G. Glasby,et al.  Deep-Sea Nodules and Co-rich Mn Crusts , 2015 .

[109]  G. Verriopoulos,et al.  Individual and combined toxicity of three heavy metals, Cu, Cd and Cr for the marine copepod Tisbe holothuriae , 1982, Hydrobiologia.

[110]  Roberto Danovaro,et al.  Deep, diverse and definitely different: unique attributes of the world's largest ecosystem , 2010 .

[111]  M. Bebianno,et al.  Antioxidant systems and lipid peroxidation in Bathymodiolus azoricus from Mid-Atlantic Ridge hydrothermal vent fields. , 2005, Aquatic toxicology.

[112]  Vandersteene Jelle,et al.  The Halomonhystera disjuncta population is homogeneous across the Håkon Mosby mud volcano (Barents Sea) but is genetically differentiated from its shallow-water relatives , 2014 .

[113]  S. Cobbina,et al.  A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment , 2016, Environmental Science and Pollution Research.

[114]  Qunli Xu,et al.  Leiodermatolide, a novel marine natural product, has potent cytotoxic and antimitotic activity against cancer cells, appears to affect microtubule dynamics, and exhibits antitumor activity , 2016, International journal of cancer.

[115]  Aline Jaeckel,et al.  Deep seabed mining and adaptive management: The procedural challenges for the International Seabed Authority , 2016 .

[116]  C. German,et al.  Deep-sea mining of seafloor massive sulfides , 2010 .

[117]  P. Calow Physiological costs of combating chemical toxicants: ecological implications. , 1991, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.

[118]  A. Vanreusel,et al.  Hydrostatic pressure and temperature affect the tolerance of the free-living marine nematode Halomonhystera disjuncta to acute copper exposure. , 2017, Aquatic toxicology.

[119]  S. Simpson,et al.  Bioavailability and Chronic Toxicity of Metal Sulfide Minerals to Benthic Marine Invertebrates: Implications for Deep Sea Exploration, Mining and Tailings Disposal. , 2016, Environmental science & technology.

[120]  D. Bagchi,et al.  Oxidative mechanisms in the toxicity of metal ions. , 1995, Free radical biology & medicine.

[121]  Cindy Lee Van Dover,et al.  The Ecology of Deep-Sea Hydrothermal Vents , 2000 .

[122]  Valery E. Forbes,et al.  Uncertainties in Sediment Quality Weight-of-Evidence (WOE) Assessments , 2002 .

[123]  K. Auerswald,et al.  Establishing mussel behavior as a biomarker in ecotoxicology. , 2016, Aquatic toxicology.