Advertisement

Ecotoxicology

, Volume 27, Issue 10, pp 1341–1352 | Cite as

Spatial and taxonomic variation of mercury concentration in low trophic level fauna from the Mediterranean Sea

  • Kate L. Buckman
  • Oksana Lane
  • Jože Kotnik
  • Arne Bratkic
  • Francesca Sprovieri
  • Milena Horvat
  • Nicola Pirrone
  • David C. Evers
  • Celia Y. Chen
Article

Abstract

Studies of mercury (Hg) in the Mediterranean Sea have focused on pollution sources, air-sea mercury exchange, abiotic mercury cycling, and seafood. Much less is known about methylmercury (MeHg) concentrations in the lower food web. Zooplankton and small fish were sampled from the neuston layer at both coastal and open sea stations in the Mediterranean Sea during three cruise campaigns undertaken in the fall of 2011 and the summers of 2012 and 2013. Zooplankton and small fish were sorted by morphospecies, and the most abundant taxa (e.g. euphausiids, isopods, hyperiid amphipods) analyzed for methylmercury (MeHg) concentration. Unfiltered water samples were taken during the 2011 and 2012 cruises and analyzed for MeHg concentration. Multiple taxa suggested elevated MeHg concentrations in the Tyrrhenian and Balearic Seas in comparison with more eastern and western stations in the Mediterranean Sea. Spatial variation in zooplankton MeHg concentration is positively correlated with single time point whole water MeHg concentration for euphausiids and mysids and negatively correlated with maximum chlorophyll a concentration for euphausiids, mysids, and “smelt” fish. Taxonomic variation in MeHg concentration appears driven by taxonomic grouping and feeding mode. Euphausiids, due to their abundance, relative larger size, importance as a food source for other fauna, and observed relationship with surface water MeHg are a good candidate biotic group to evaluate for use in monitoring the bioavailability of MeHg for trophic transfer in the Mediterranean and potentially globally.

Keywords

Methylmercury Zooplankton Mediterranean Sea Euphausiid Myctophid 

Notes

Acknowledgements

We gratefully acknowledge the assistance of the captain and crew of the RV Urania in accomplishing successful sampling campaigns, as well as the collaborative spirit and congeniality of the science parties. V. Taylor and B. Jackson of the Dartmouth Trace Element Analysis Core were instrumental in achieving low biomass sample detection. Technical assistance of E. Begu and K. Obu Vazner to carry out some of the MeHg analysis of sea water is also acknowledged, as is support from L.Tier for assistance with 2013 sample collections. The cruise campaigns performed in the framework of the ongoing Med-Oceanor measurements program were funded by the Italian National Research Council and were also supported by the FP7 (2010–2015) Global Mercury Observation System (GMOS) project. The financial support of the EC funded project GMOS (Grant agreement no: 265113) and the Slovenian ARRS funded program P1-0143 are acknowledged. In addition, funding for the research presented in this publication was provided by the National Institute of Environmental Health Sciences of the National Institutes of Health (Stanton P42 ES007373). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Funding

The research was funded in part the European Commission 7th Framework Program Global Mercury Observation System (265113, coordinated by Pirrone), the Slovenian Research Agency (P1-0143, Horvat), and the National Institute of Environmental Health Sciences of the National Institutes of Health (P42 ES007373, Stanton). Ship time was provided by the Italian Research Council as part of the Med-Oceanor program.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. All applicable guidelines were followed for collection and use of invertebrate and fish samples in this study

Supplementary material

10646_2018_1986_MOESM1_ESM.docx (30.8 mb)
Supporting Information

References

  1. Andersson ME, Gårdfeldt K, Wängberg I, Sprovieri F, Pirrone N, Lindqvist O (2007) Seasonal and daily variation of mercury evasion at coastal and off shore sites from the Mediterranean Sea. Mar Chem 104:214–226CrossRefGoogle Scholar
  2. Arcos J, Ruiz X, Bearhop S, Furness R (2002) Mercury levels in seabirds and their fish prey at the Ebro Delta (NW Mediterranean): the role of trawler discards as a source of contamination. Mar Ecol-Prog Ser 232:281–290CrossRefGoogle Scholar
  3. Azoury S, Tronczynski J, Chiffoleau JF, Cossa D, Nakhle K, Schmidt S, Khalaf G (2013) Historical records of mercury, lead, and polycyclic aromatic hydrocarbons depositions in a dated sediment core from the Eastern Mediterranean. Environ Sci Technol 47:7101–7109.  https://doi.org/10.1021/es4005637 CrossRefGoogle Scholar
  4. Baldi F, Bargagli R (1984) Mercury pollution in marine sediments near a chloralkali plant: distribution and availability of the metal. Sci Total Environ 39:15–26CrossRefGoogle Scholar
  5. Bargagli R, Monaci F, Sanchez-Hernandez JC, Cateni D (1998) Biomagnification of mercury in an Antarctic marine coastal food web. Mar Ecol-Prog Ser 169:65–76.  https://doi.org/10.3354/meps169065 CrossRefGoogle Scholar
  6. Bellante A et al. (2012) Stranded cetaceans as indicators of mercury pollution in the Mediterranean Sea. Ital J Zool 79:151–160.  https://doi.org/10.1080/11250003.2011.621072 CrossRefGoogle Scholar
  7. Campbell LM, Norstrom RJ, Hobson KA, Muir DCG, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci Total Environ 351:247–263.  https://doi.org/10.1016/j.scitotenv.2005.02.043 CrossRefGoogle Scholar
  8. Canese S, Cardinali A, Fortuna CM, Giusti M, Lauriano G, Salvati E, Greco S (2006) The first identified winter feeding ground of fin whales (Balaenoptera physalus) in the Mediterranean Sea. J Mar Biol Assoc UK 86:903–907.  https://doi.org/10.1017/S0025315406013853 CrossRefGoogle Scholar
  9. Cardoso PG, Marques SC, D’Ambrosio M, Pereira E, Duarte AC, Azeiteiro UM, Pardal MA (2013) Changes in zooplankton communities along a mercury contamination gradient in a coastal lagoon (Ria de Aveiro, Portugal). Mar Pollut Bull 76:170–177.  https://doi.org/10.1016/j.marpolbul.2013.09.007 CrossRefGoogle Scholar
  10. Chouvelon T et al. (2018) Oligotrophy as a major driver of mercury bioaccumulation in medium-to high-trophic level consumers: a marine ecosystem-comparative study. Environ Pollut 233:844–854.  https://doi.org/10.1016/j.envpol.2017.11.015 CrossRefGoogle Scholar
  11. Cinnirella S, Pirrone N, Horvat M, Kocman D, Kotnik J (2013) Mercury bioaccumulation in the Mediterranean. In: Pirrone N (ed) Proceedings of the 16th International Conference on heavy metals in the environment, vol 1. E3S Web of Conferences. 1100510.1051/e3sconf/20130111005Google Scholar
  12. Clayden MG, Arsenault LM, Kidd KA, O’Driscoll NJ, Mallory ML (2015) Mercury bioaccumulation and biomagnification in a small Arctic polynya ecosystem. Sci Total Environ 509:206–215.  https://doi.org/10.1016/j.scitotenv.2014.07.087 CrossRefGoogle Scholar
  13. Cossa D, Averty B, Pirrone N (2009) The origin of methylmercury in open Mediterranean waters. Limnol Oceanogr 54:837–844.  https://doi.org/10.4319/lo.2009.54.3.0837 CrossRefGoogle Scholar
  14. Cossa D et al. (2012) Influences of bioavailability, trophic position, and growth on methylmercury in hakes (Merluccius merluccius) from Northwestern Mediterranean and Northeastern Atlantic. Environ Sci Technol 46:4885–4893.  https://doi.org/10.1021/es204269w CrossRefGoogle Scholar
  15. Covelli S, Faganeli J, Horvat M, Brambati A (1999) Porewater distribution and benthic flux measurements of mercury and methylmercury in the Gulf of Trieste (northern Adriatic Sea). Estuar Coast Shelf Sci 48:415–428CrossRefGoogle Scholar
  16. Covelli S, Faganeli J, Horvat M, Brambati A (2001) Mercury contamination of coastal sediments as the result of long-term cinnabar mining activity (Gulf of Trieste, northern Adriatic sea). Appl Geochem 16:541–558CrossRefGoogle Scholar
  17. Covelli S, Langone L, Acquavita A, Piani R, Emili A (2012) Historical flux of mercury associated with mining and industrial sources in the Marano and Grado Lagoon (northern Adriatic Sea). Estuar, Coast Shelf Sci 113:7–19CrossRefGoogle Scholar
  18. Cresson P et al. (2014) Mercury in organisms from the Northwestern Mediterranean slope: importance of food sources. Sci Total Environ 497:229–238.  https://doi.org/10.1016/j.scitotenv.2014.07.069 CrossRefGoogle Scholar
  19. dos Santos IR et al. (2006) Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ Pollut 140:304–311.  https://doi.org/10.1016/j.envpol.2005.07.007 CrossRefGoogle Scholar
  20. Driscoll CT et al. (2012) Nutrient supply and mercury dynamics in marine ecosystems: a conceptual model. Environ Res 119:118–131.  https://doi.org/10.1016/j.envres.2012.05.002 CrossRefGoogle Scholar
  21. Faganeli J, Hines ME, Horvat M, Falnoga I, Covelli S (2014) Methylmercury in the Gulf of Trieste (Northern Adriatic Sea): from Microbial sources to seafood consumers. Food Technol Biotechnol 52:188–197Google Scholar
  22. Fantozzi L, Ferrara R, Sprovieri F (2013) Dissolved gaseous mercury and mercury flux measurements in Mediterranean coastal waters: A short review. In: Pirrone N (ed) Proceedings of the 16th International Conference on heavy metals in the environment, vol 1. E3S Web of Conferences. 3200410.1051/e3sconf/20130132004Google Scholar
  23. Foster KL, Stern GA, Pazerniuk MA, Hickie B, Wallcusz W, Wang FY, Macdonald RW (2012) Mercury biomagnification in marine zooplankton food webs in Hudson Bay. Environ Sci Technol 46:12952–12959.  https://doi.org/10.1021/es303434p CrossRefGoogle Scholar
  24. Gibičar D et al. (2009) Human exposure to mercury in the vicinity of chlor-alkali plant. Environ Res 109:355–367CrossRefGoogle Scholar
  25. Gosnell KJ, Mason RP (2015) Mercury and methylmercury incidence and bioaccumulation in plankton from the central Pacific Ocean. Mar Chem 177:772–780.  https://doi.org/10.1016/j.marchem.2015.07.005 CrossRefGoogle Scholar
  26. Guevara RS, Horvat M (2013) Stability and behaviour of low level spiked inorganic mercury in natural water samples. Anal Methods 5:1996–2006.  https://doi.org/10.1039/C3AY26496C CrossRefGoogle Scholar
  27. Hammerschmidt CR, Finiguerra MB, Weller RL, Fitzgerald WF (2013) Methylmercury accumulation in plankton on the continental margin of the Northwest Atlantic Ocean. Environ Sci Technol 47:3671–3677.  https://doi.org/10.1021/es3048619 CrossRefGoogle Scholar
  28. Harmelin-Vivien M, Mahe K, Bodiguel X, Mellon-Duval C (2012) Possible link between prey quality, condition and growth of juvenile hake (Merluccius merluccius) in the Gulf of Lions (NW Mediterranean). Cybium 36:323–328Google Scholar
  29. Heimburger LE, Cossa D, Marty JC, Migon C, Averty B, Dufour A, Ras J (2010) Methyl mercury distributions in relation to the presence of nano- and picophytoplankton in an oceanic water column (Ligurian Sea, North-western Mediterranean). Geochim Cosmochim Acta 74:5549–5559.  https://doi.org/10.1016/j.gca.2010.06.036 CrossRefGoogle Scholar
  30. Hirota R, Fukuda Y, Chiba J, Tajima S, Fujiki M Mercury content of copepods (Crustacea) collected from the Antarctic sea. In: Proceedings of the NIPR Symposium on polar biology, 1989. 国立極地研究所, pp. 65–70Google Scholar
  31. Horvat M, Degenek N, Lipej L, Tratnik JS, Faganeli J (2014) Trophic transfer and accumulation of mercury in ray species in coastal waters affected by historic mercury mining (Gulf of Trieste, northern Adriatic Sea). Environ Sci Pollut Res 21:4163–4176.  https://doi.org/10.1007/s11356-013-2262-0 CrossRefGoogle Scholar
  32. Horvat M, Kotnik J, Logar M, Fajon V, Zvonaric T, Pirrone N (2003) Speciation of mercury in surface and deep-sea waters in the Mediterranean Sea. Atmos Environ 37:S93–S108.  https://doi.org/10.1016/s1352-2310(03)00249-8 CrossRefGoogle Scholar
  33. Horvat M, Liang L, Bloom NS (1993) Comparison of distillation with other current isolation methods for the determination of methyl mercury compounds in low level environmental samples: Part II. Water Anal Chim Acta 282:153–168.  https://doi.org/10.1016/0003-2670(93)80364-Q CrossRefGoogle Scholar
  34. Jonsson S et al. (2017) Terrestrial discharges mediate trophic shifts and enhance methylmercury accumulation in estuarine biota Sci Adv 3  https://doi.org/10.1126/sciadv.1601239 CrossRefGoogle Scholar
  35. Karagas MR et al. (2012) Evidence on the human health effects of low level methylmercury exposure. Environ Health Perspect 120:799–806CrossRefGoogle Scholar
  36. Kotnik J et al. (2007) Mercury speciation in surface and deep waters of the Mediterranean Sea Mar Chem 107:13–30  https://doi.org/10.1016/j.marchem.2007.02.012 CrossRefGoogle Scholar
  37. Kotnik J et al. (2015) Mercury speciation in the Adriatic Sea Mar Pollut Bull 96:136–148  https://doi.org/10.1016/j.marpolbul.2015.05.037 CrossRefGoogle Scholar
  38. Kotnik J, Horvat M, Begu E, Shlyapnikov Y, Sprovieri F, Pirrone N (2017) Dissolved gaseous mercury (DGM) in the Mediterranean Sea: spatial and temporal trends Mar Chem 193:8-19.  https://doi.org/10.1016/j.marchem.2017.03.002 CrossRefGoogle Scholar
  39. Kotnik J, Sprovieri F, Ogrinc N, Horvat M, Pirrone N (2014) Mercury in the Mediterranean, part I: spatial and temporal trends. Environ Sci Pollut Res 21:4063–4080.  https://doi.org/10.1007/s11356-013-2378-2 CrossRefGoogle Scholar
  40. Lavoie RA, Hebert CE, Rail J-F, Braune BM, Yumvihoze E, Hill LG, Lean DR (2010) Trophic structure and mercury distribution in a Gulf of St. Lawrence (Canada) food web using stable isotope analysis. Sci Total Environ 408:5529–5539CrossRefGoogle Scholar
  41. Liang L, Horvat M, Bloom NS (1994) An improved speciation method for mercury by GC/CVAFS after aqueous phase ethylation and room temperature precollection. Talanta 41:371–379.  https://doi.org/10.1016/0039-9140(94)80141-X CrossRefGoogle Scholar
  42. Liang L, Horvat M, Danilchik P (1996) A novel analytical method for determination of picogram levels of total mercury in gasoline and other petroleum based products. Sci Total Environ 187:57–64.  https://doi.org/10.1016/0048-9697(96)05129-7 CrossRefGoogle Scholar
  43. Martin RS et al. (2012) Bioindication of volcanic mercury (Hg) deposition around Mt. Etna (Sicily). Chem Geol 310:12–22.  https://doi.org/10.1016/j.chemgeo.2012.03.022 CrossRefGoogle Scholar
  44. Maserti B, Ferrara R (1991) Mercury in plants, soil and atmosphere near a chlor-alkali complex. Water Air & Soil Pollut 56:15–20CrossRefGoogle Scholar
  45. Mayzaud P, Virtue P, Albessard E (1999) Seasonal variations in the lipid and fatty acid composition of the euphausiid Meganyctiphanes norvegica from the Ligurian Sea. Mar Ecol-Prog Ser 186:199–210.  https://doi.org/10.3354/meps186199 CrossRefGoogle Scholar
  46. Mergler D, Anderson HA, Chan LHM, Mahaffey KR, Murray M, Sakamoto M, Stern AH (2007) Methylmercury exposure and health effects in humans: A worldwide concern. Ambio 36:3–11CrossRefGoogle Scholar
  47. Naccari C et al. (2015) Toxic Metals in pelagic, benthic and demersal Fish species from Mediterranean FAO Zone 37. Bull Environ Contam Toxicol 95:567–573.  https://doi.org/10.1007/s00128-015-1585-6 CrossRefGoogle Scholar
  48. Nfon E, Cousins IT, Jarvinen O, Mukherjee AB, Verta M, Broman D (2009) Trophodynamics of mercury and other trace elements in a pelagic food chain from the Baltic Sea. Sci Total Environ 407:6267–6274.  https://doi.org/10.1016/j.scitotenv.2009.08.032 CrossRefGoogle Scholar
  49. Nygard T, Lie E, Rov N, Steinnes E (2001) Metal dynamics in an Antarctic food chain. Mar Pollut Bull 42:598–602.  https://doi.org/10.1016/s0025-326x(00)00206-x CrossRefGoogle Scholar
  50. Pirrone N et al. (2013) Toward the next generation of air quality monitoring: Mercury. Atmos Environ 80:599–611CrossRefGoogle Scholar
  51. Pucko M et al. (2014) Transformation of mercury at the bottom of the Arctic food web: an overlooked puzzle in the mercury exposure narrative. Environ Sci Technol 48:7280–7288.  https://doi.org/10.1021/es404851b CrossRefGoogle Scholar
  52. Purcell JE et al. (2015) Digestion and predation rates of zooplankton by the pleustonic hydrozoan Velella velella and widespread blooms in 2013 and 2014. J Plankton Res 37:1056–1067.  https://doi.org/10.1093/plankt/fbv031 CrossRefGoogle Scholar
  53. Rosa S, Pansera M, Granata A, Guglielmo L (2013) Interannual variability, growth, reproduction and feeding of Pelagia noctiluca (Cnidaria: Scyphozoa) in the Straits of Messina (Central Mediterranean Sea): linkages with temperature and diet. J Mar Syst 111:97–107.  https://doi.org/10.1016/j.jmarsys.2012.10.001 CrossRefGoogle Scholar
  54. Sabatés A, Pagès F, Atienza D, Fuentes V, Purcell JE, Gili J-M (2010) Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia 645:153–165.  https://doi.org/10.1007/s10750-010-0221-z CrossRefGoogle Scholar
  55. Schmidt K (2010) Chapter five - food and feeding in Northern Krill (Meganyctiphanes norvegica Sars). In: Tarling GA (ed) Advances in marine biology, vol 57. Academic Press, pp. 127–171.  https://doi.org/10.1016/B978-0-12-381308-4.00005-4 Google Scholar
  56. Simonsen KA, Ressler PH, Rooper CN, Zador SG (2016) Spatio-temporal distribution of euphausiids: an important component to understanding ecosystem processes in the Gulf of Alaska and eastern Bering Sea. ICES J Mar Sci 73:2020–2036.  https://doi.org/10.1093/icesjms/fsv272 CrossRefGoogle Scholar
  57. Soerensen AL, Schartup AT, Gustafsson E, Gustafsson BG, Undeman E, Björn E (2016) Eutrophication increases phytoplankton methylmercury concentrations in a Coastal Sea—a Baltic Sea case study. Environ Sci Technol 50:11787–11796.  https://doi.org/10.1021/acs.est.6b02717 CrossRefGoogle Scholar
  58. Sprovieri F, Hedgecock I, Pirrone N (2010a) An investigation of the origins of reactive gaseous mercury in the Mediterranean marine boundary layer. Atmos Chem Phys 10:3985–3997CrossRefGoogle Scholar
  59. Sprovieri F, Pirrone N, Ebinghaus R, Kock H, Dommergue A (2010b) A review of worldwide atmospheric mercury measurements. Atmos Chem Phys 10:8245–8265CrossRefGoogle Scholar
  60. Sprovieri F, Pirrone N, Gärdfeldt K, Sommar J (2003) Mercury speciation in the marine boundary layer along a 6000km cruise path around the Mediterranean Sea. Atmos Environ 37:63–71CrossRefGoogle Scholar
  61. Squadrone S, Brizio P, Chiaravalle E, Abete MC (2015a) Sperm whales (Physeter macrocephalus), found stranded along the Adriatic coast (Southern Italy, Mediterranean Sea), as bioindicators of essential and non-essential trace elements in the environment. Ecol Indic 58:418–425.  https://doi.org/10.1016/j.ecolind.2015.06.016 CrossRefGoogle Scholar
  62. Squadrone S, Chiaravalle E, Gavinelli S, Monaco G, Rizzi M, Abete MC (2015b) Analysis of mercury and methylmercury concentrations, and selenium:mercury molar ratios for a toxicological assessment of sperm whales (Physeter macrocephalus) in the most recent stranding event along the Adriatic coast (Southern Italy, Mediterranean Sea). Chemosphere 138:633–641.  https://doi.org/10.1016/j.chemosphere.2015.07.047 CrossRefGoogle Scholar
  63. Storelli M, Storelli A, Giacominelli-Stuffler R, Marcotrigiano G (2005) Mercury speciation in the muscle of two commercially important fish, hake (Merluccius merluccius) and striped mullet (Mullus barbatus) from the Mediterranean sea: estimated weekly intake. Food Chem 89:295–300CrossRefGoogle Scholar
  64. Taylor VF, Carter A, Davies C, Jackson BP (2011) Trace-level automated mercury speciation analysis. Anal Methods 3:1143–1148CrossRefGoogle Scholar
  65. Taylor VF, Jackson BP, Chen CY (2008) Mercury speciation and total trace element determination of low-biomass biological samples. Anal Bioanal Chem 392:1283–1290.  https://doi.org/10.1007/s00216-008-2403-3 CrossRefGoogle Scholar
  66. Wängberg I et al. (2008) Atmospheric mercury at mediterranean coastal stations. Environ Fluid Mech 8:101–116CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Kate L. Buckman
    • 1
  • Oksana Lane
    • 2
  • Jože Kotnik
    • 3
  • Arne Bratkic
    • 3
    • 4
    • 5
  • Francesca Sprovieri
    • 6
  • Milena Horvat
    • 3
    • 4
  • Nicola Pirrone
    • 6
  • David C. Evers
    • 2
  • Celia Y. Chen
    • 1
  1. 1.Dartmouth College, Department of Biological SciencesHanoverUSA
  2. 2.Biodiversity Research InstitutePortlandUSA
  3. 3.Jožef Stefan Institute, Department of Environmental SciencesLjubljanaSlovenia
  4. 4.International Postgraduate School Jožef StefanLjubljanaSlovenia
  5. 5.Vrije Universiteit Brussel, AnalyticalEnvironmental, and Geo-ChemistryBrusselsBelgium
  6. 6.CNR Institute of Atmospheric PollutionRendeItaly

Personalised recommendations