Abstract
Seabirds accumulate mercury (Hg) due to their long-life span together with their high trophic position. A Hg monitoring in Venice’s Lagoon using three seabird species occupying different trophic habitat (Thalasseus sandvicensis, Ichthyaetus melanocephalus, and Chroicocephalus ridibundus) confirmed that fledgelings might effectively be used as sentinels of Hg bioavailability. The significant differences in Hg residues in feathers observed among the species highlighted a possible differential exposure due to different diets, with C. ridibundus accumulating more Hg than the other species. Average residues in feathers were not above the threshold associated with adverse effects on birds (5 mg kg− 1). Nevertheless, a large part of the C. ridibundus individuals (58%) exceeded the adverse effect level, underlining the need for strengthening Hg monitoring. Seabirds indeed may provide relevant insight on Hg transfer in food webs and a better picture of the hazards to men when bird species forage on species exploited for human consumption.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analysed during this study are included in this published article in forms of figures and tables (and its supplementary information files). Raw data are available from the corresponding author on reasonable request.
References
Ackerman JT, Eagles-Smith CA, Herzog MP (2011) Bird mercury concentrations change rapidly as chicks age: toxicological risk is highest at hatching and fledging. Environ Sci Technol 45:5418–5425. https://doi.org/10.1021/es200647g
Apitz SE, Barbanti A, Bocci M, Carlin A, Montobbio L, Bernstein AG (2007) The sediments of the Venice lagoon (Italy) evaluated in a screening risk assessment approach: part II - lagoon sediment quality compared to hot spots, regional, and international case studies. Integr Environ Assess Manag 3:415–438. https://doi.org/10.1002/ieam.5630030311
Binkowski LJ, Fort J, Brault-Favrou M, Gallien F, Le Guillou G, Chastel O, Bustamante P (2021) Foraging ecology drives mercury contamination in chick gulls from the English Channel. Chemosphere 267:128622. https://doi.org/10.1016/J.CHEMOSPHERE.2020.128622
Blévin P, Carravieri A, Jaeger A, Chastel O, Bustamante P, Cherel Y (2013) Wide range of mercury contamination in chicks of Southern Ocean seabirds. PLoS ONE 8:e54508. https://doi.org/10.1371/journal.pone.0054508
Bloom NS, Moretto LM, Scopece P, Ugo P (2004) Seasonal cycling of mercury and monomethyl mercury in the Venice lagoon (Italy). Mar Chem 91:85–99. https://doi.org/10.1016/j.marchem.2004.06.002
Borghesi F, Andreotti A, Baccetti N, Bianchi N, Birke M, Migani F, Dinelli E (2011) Flamingo feathers to monitor metal contamination of coastal wetlands: methods and initial results concerning the presence of mercury at six Mediterranean sites. Chem Ecol 27:137–151. https://doi.org/10.1080/02757540.2011.625942
Borghesi F, Dinelli E, Migani F, Béchet A, Rendón-Martos M, Amat JA, Sommer S, Gillingham MAF (2017) Assessing environmental pollution in birds: a new methodological approach for interpreting bioaccumulation of trace elements in feather shafts using geochemical sediment data. Methods Ecol Evol 8:96–108. https://doi.org/10.1111/2041-210X.12644
Braune BM, Scheuhammer AM, Crump D, Jones S, Porter E, Bond D (2012) Toxicity of methylmercury injected into eggs of thick-billed murres and arctic terns. Ecotoxicology 21:2143–2152. https://doi.org/10.1007/S10646-012-0967-3/FIGURES/3
Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 5:203–311
Burger J, Gochfeld M (2000) Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci Total Environ 257:37–52. https://doi.org/10.1016/S0048-9697(00)00496-4
Burger J, Gochfeld M (1997) Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172. https://doi.org/10.1006/ENRS.1997.3778
Carravieri A, Fort J, Tarroux A, Cherel Y, Love OP, Prieur S, Brault-Favrou M, Bustamante P, Descamps S (2018) Mercury exposure and short-term consequences on physiology and reproduction in Antarctic petrels. Environ Pollut 237:824–831. https://doi.org/10.1016/J.ENVPOL.2017.11.004
Chen C, Amirbahman A, Fisher N, Harding G, Lamborg C, Nacci D, Taylor D (2008) Methylmercury in marine ecosystems: spatial patterns and processes of production, bioaccumulation, and biomagnification. EcoHealth 5:399–408. https://doi.org/10.1007/S10393-008-0201-1
Chen CY, Borsuk ME, Bugge DM, Hollweg T, Balcom PH, Ward DM, Williams J, Mason RP (2014) Benthic and pelagic pathways of methylmercury bioaccumulation in estuarine food webs of the Northeast United States. PLoS ONE 9:e89305. https://doi.org/10.1371/JOURNAL.PONE.0089305
Chételat J, Ackerman JT, Eagles-Smith CA, Hebert CE (2020) Methylmercury exposure in wildlife: a review of the ecological and physiological processes affecting contaminant concentrations and their interpretation. Sci Total Environ 711:135117. https://doi.org/10.1016/j.scitotenv.2019.135117
Dauwe T, Bervoets L, Pinxten R, Blust R, Eens M (2003) Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination. Environ Pollut 124:429–436. https://doi.org/10.1016/s0269-7491(03)00044-7
Distefano GG, Zangrando R, Basso M, Panzarin L, Gambaro A, Volpi Ghirardini A, Picone M (2022) Assessing the exposure to human and veterinary pharmaceuticals in waterbirds: the use of feathers for monitoring antidepressants and nonsteroidal anti-inflammatory drugs. Sci Total Environ 821:153473. https://doi.org/10.1016/J.SCITOTENV.2022.153473
Dominik J, Tagliapietra D, Bravo AG, Sigovini M, Spangenberg JE, Amouroux D, Zonta R (2014) Mercury in the food chain of the lagoon of Venice, Italy. Mar Pollut Bull 88:194–206. https://doi.org/10.1016/J.MARPOLBUL.2014.09.005
Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983. https://doi.org/10.1021/es305071v
Eisler R (2000) Handbook of Chemical Risk Assessment. CRC Press. https://doi.org/10.1201/9781420032741
Ek KH, Morrison GM, Lindberg P, Rauch S (2004) Comparative tissue distribution of metals in birds in Sweden using ICP-MS and laser ablation ICP-MS. Arch. Environ. Contam. Toxicol. 2004 472 47, 259–269. https://doi.org/10.1007/S00244-004-3138-6
Evers DC (2018) The Effects of Methylmercury on Wildlife: a Comprehensive Review and Approach for Interpretation. In: Della Sala DA, Goldstein MI (eds) The Encyclopedia of the Anthropocene. Elsevier, Oxford, pp 181–194. https://doi.org/10.1016/B978-0-12-809665-9.09985-7
Evers DC, Savoy LJ, DeSorbo CR, Yates DE, Hanson W, Taylor KM, Siegel LS, Cooley JH, Bank MS, Major A, Munney K, Mower BF, Vogel HS, Schoch N, Pokras M, Goodale MW, Fair J (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81. https://doi.org/10.1007/s10646-007-0168-7
Fasola M, Bogliani G, Saino N, Canova L (1989) Foraging, feeding and time-activity niches of eight species of breeding seabirds in the coastal wetlands of the adriatic sea. Bolletino di Zool 56:61–72. https://doi.org/10.1080/11250008909355623
Fijn RC, de Jong J, Courtens W, Verstraete H, Stienen EWM, Poot MJM (2017) GPS-tracking and colony observations reveal variation in offshore habitat use and foraging ecology of breeding Sandwich Terns. J Sea Res 127:203–211. https://doi.org/10.1016/j.seares.2016.11.005
Furness RW, Greenwood JJD (1993) Birds as monitors of environmental change. Springer Netherlands, Dordrecht. https://doi.org/10.1007/978-94-015-1322-7
Goede AA, de Bruin M (1984) The use of bird feather parts as a monitor for metal pollution. Environ Pollut Ser B Chem Phys 8:281–298. https://doi.org/10.1016/0143-148X(84)90028-4
Goutner V (1994) The diet of Mediterranean Gull (Larus melanocephalus) chicks at fledging. J Ornithol 135:193–201. https://doi.org/10.1007/BF01640288
Harding G, Dalziel J, Vass P (2018) Bioaccumulation of methylmercury within the marine food web of the outer Bay of Fundy, Gulf of Maine. PLoS ONE 13:e0197220. https://doi.org/10.1371/journal.pone.0197220
Helsel DR (2005) More than obvious: better methods for interpreting nondetect data. Environ Sci Technol 39:419. https://doi.org/10.1021/ES053368A. A-423A
Jaspers VLB, Covaci A, Herzke D, Eulaers I, Eens M (2019) Bird feathers as a biomonitor for environmental pollutants: prospects and pitfalls. TrAC Trends Anal Chem 118:223–226. https://doi.org/10.1016/J.TRAC.2019.05.019
Le Croizier G, Point D, Renedo M, Munaron JM, Espinoza P, Amezcua-Martinez F, Bertrand L, Lorrain S, A (2022) Mercury concentrations, biomagnification and isotopic discrimination factors in two seabird species from the Humboldt Current ecosystem. Mar Pollut Bull 177:113481. https://doi.org/10.1016/J.MARPOLBUL.2022.113481
Mills WF, Bustamante P, McGill RAR, Anderson ORJ, Bearhop S, Cherel Y, Votier SC, Phillips RA (2020) Mercury exposure in an endangered seabird: long-term changes and relationships with trophic ecology and breeding success. Proc. R. Soc. B 287, 20202683. https://doi.org/10.1098/RSPB.2020.2683
Paiva VH, Tavares PC, Ramos JA, Pereira E, Antunes S, Duarte AC (2008) The influence of diet on mercury intake by little tern chicks. Arch Environ Contam Toxicol 55:317–328. https://doi.org/10.1007/s00244-007-9118-x
Picone M, Bergamin M, Losso C, Delaney E, Arizzi Novelli A, Volpi Ghirardini A (2016) Assessment of sediment toxicity in the lagoon of Venice (Italy) using a multi-species set of bioassays. Ecotoxicol Environ Saf 123:32–44. https://doi.org/10.1016/j.ecoenv.2015.09.002
Picone M, Corami F, Gaetan C, Basso M, Battiston A, Panzarin L, Volpi Ghirardini A (2019) Accumulation of trace elements in feathers of the Kentish plover Charadrius alexandrinus. Ecotoxicol Environ Saf 179:62–70. https://doi.org/10.1016/j.ecoenv.2019.04.051
Picone M, Distefano GG, Corami F, Franzoi P, Redolfi Bristol S, Basso M, Panzarin L, Ghirardini V, A (2022) Occurrence of rare earth elements in fledgelings of Thalasseus sandvicensis. Environ Res 204:112152. https://doi.org/10.1016/J.ENVRES.2021.112152
Provencher JF, Mallory ML, Braune BM, Forbes MR, Gilchrist HG (2014) Mercury and marine birds in Arctic Canada: Effects, current trends, and why we should be paying closer attention. Environ Rev 22:244–255. https://doi.org/10.1139/ER-2013-0072/ASSET/IMAGES/ER-2013-0072TAB5.GIF
Rosati G, Solidoro C, Canu D (2020) Mercury dynamics in a changing coastal area over industrial and postindustrial phases: Lessons from the Venice lagoon. Sci Total Environ 743:140586. https://doi.org/10.1016/j.scitotenv.2020.140586
Ruus A, Øverjordet IB, Braaten HFV, Evenset A, Christensen G, Heimstad ES, Gabrielsen GW, Borgå K (2015) Methylmercury biomagnification in an Arctic pelagic food web. Environ Toxicol Chem 34:2636–2643. https://doi.org/10.1002/etc.3143
Sánchez-Fortún M, Ouled-Cheikh J, Jover C, García-Tarrasón M, Carrasco JL, Sanpera C (2020) Following up mercury pollution in the Ebro Delta (NE Spain): Audouin’s gull fledglings as model organisms to elucidate anthropogenic impacts on the environment. Environ Pollut 266:115232. https://doi.org/10.1016/J.ENVPOL.2020.115232
Seewagen CL (2018) The threat of global mercury pollution to bird migration: potential mechanisms and current evidence. https://doi.org/10.1007/s10646-018-1971-z. Ecotoxicology 1–14
Sfriso A, Argese E, Bettiol C, Facca C (2008) Tapes philippinarum seed exposure to metals in polluted areas of the Venice lagoon. Estuar Coast Shelf Sci 4:581–590. https://doi.org/10.1016/J.ECSS.2008.05.012
Tartu S, Goutte A, Bustamante P, Angelier F, Moe B, Clément-Chastel C, Bech C, Gabrielsen GW, Bustnes JO, Chastel O (2013) To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird. Biol Lett 9:20130317. https://doi.org/10.1098/rsbl.2013.0317
Tavares PC, Monteiro LR, Lopes RJ, Pereira ME, Duarte AC, Furness RW (2005) Variation of mercury contamination in chicks of Little Tern Sterna albifrons in Southwest Europe: Brood, age, and colony related effects. Bull. Environ. Contam. Toxicol. 2005 741 74, 177–183. https://doi.org/10.1007/S00128-004-0565-Z
Vizuete J, Pérez-López M, Míguez-Santiyán MP, Hernández-Moreno D (2018) Mercury (hg), lead (pb), cadmium (cd), selenium (Se), and arsenic (as) in liver, kidney, and feathers of gulls: a review. Reviews of Environmental Contamination and Toxicology. Springer, pp 85–146. https://doi.org/10.1007/398_2018_16
Whitney MC, Cristol DA (2018) Impacts of sublethal mercury exposure on birds: a detailed review. Rev Env Contam Toxicol 244:113–163. https://doi.org/10.1007/398_2017_4
Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury, in: Handbook of Ecotoxicology, Second Edition. CRC Press, pp. 409–463. https://doi.org/10.1201/9781420032505.CH16
Zenatello M, Baccetti N, Lucchetta A (2021) International Waterbird Census Report - ITALY 2009–2018. Ozzano dell’Emilia (BO). https://doi.org/10.13140/RG.2.2.24870.45123
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
Marco Picone: Conceptualisation, Methodology. Investigation. Data curation. Writing-Original draft preparation. Writing - Review & Editing. Gabriele Giuseppe Distefano: Investigation. Resources. Formal analysis. Data curation. Writing-Original draft preparation. Godbless Adu Benhene: Investigation. Resources. Formal analysis. Data curation. Writing-Original draft preparation. Fabiana Corami: Investigation. Resources. Formal analysis. Data curation. Writing-Original draft preparation. Marco Basso: Investigation. Resources. Lucio Panzarin: Investigation. Resources. Caterina Carabelli: Investigation. Resources. Formal analysis. Data curation. Annamaria Volpi Ghirardini: Supervision. Writing - Review & Editing.
Corresponding author
Ethics declarations
Ethical Approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.
Competing Interests
The authors have no relevant financial or non-financial interests to disclose. The authors have no competing interests to declare that are relevant to the content of this article. All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript. The authors have no financial or proprietary interests in any material discussed in this article.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Picone, M., Distefano, G.G., Benhene, G.A. et al. Seabirds as Biomonitors of Mercury Bioavailability in the Venice Lagoon. Bull Environ Contam Toxicol 110, 2 (2023). https://doi.org/10.1007/s00128-022-03650-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00128-022-03650-z