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Histopathological effects of short-term aqueous exposure to environmentally relevant concentration of lead (Pb) in shorthorn sculpin (Myoxocephalus scorpius) under laboratory conditions

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Abstract

Shorthorn sculpin (Myoxocephalus scorpius) has been used as a sentinel species for environmental monitoring, including heavy metal contamination from mining activities. Former lead–zinc (Pb–Zn) mines in Greenland resulted in elevated concentrations of metals, especially Pb, in marine biota. However, the potential accumulation of Pb and effects of the presence of Pb residues in fish on health of sculpins observed in the field have not been validated in laboratory experiments. Therefore, our aim was to validate field observation of shorthorn sculpin via controlled laboratory exposure to environmentally relevant concentrations of dissolved Pb. We evaluated the effects of a short-term (28 days) exposure to Pb on Pb residues in sculpin blood, gills, liver, and muscle and the morphology of gills and liver. The highest level of Pb was found in the gills, followed by muscle and then liver. Pb levels in liver, gills, and blood of Pb-exposed sculpins were significantly higher than those in control fish, showing that blood is suitable for assessing Pb accumulation and exposure in sculpins. Histopathological investigations showed that the severity score of liver necrosis and gill telangiectasia of Pb-exposed sculpins was significantly greater than in control fish. The number of mucous cells in gills was positively correlated with Pb concentrations in organs. Overall, the results validated field observation for the effects of Pb on wild sculpin and contributed to the improved use of the shorthorn sculpin as sentinel species for monitoring contamination from Pb mines in the Arctic.

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Acknowledgements

The authors gratefully acknowledge the Development and Promotion of Science and Technology Talents Project (DPST), Royal Government of Thailand scholarship, for providing a grant for Khattapan Jantawongsri PhD study. We would like to thank Dr. Brian Jones and Dr. Judy Handlinger for valuable suggestions for interpretation of histopathology and Dr. Sabrina Sonda for her comments and suggestions on the manuscript. We acknowledge the Blue Planet including Chief Curator and Technical manager Lars Olsen for providing their expertise, time, and facilities for the present experiment.

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Authors and Affiliations

  1. Institute for Marine and Antarctic Studies (IMAS), University of Tasmania, Launceston, Tasmania, 7250, Australia

    Khattapan Jantawongsri, James Haddy, Ruth Eriksen & Barbara Nowak

  2. Department of Bioscience, Faculty of Technical Sciences, Arctic Research Centre (ARC), Aarhus University, Frederiksborgvej 399, Box 358, DK-4000, Roskilde, PO, Denmark

    Rasmus Dyrmose Nørregaard, Lis Bach, Rune Dietz, Christian Sonne, Bjørn Munro Jenssen & Barbara Nowak

  3. Den Blå Planet, National Aquarium Denmark, Jacob Fortlingsvej 1, DK-2770 Kastrup, Copenhagen, Denmark

    Kasper Jørgensen

  4. Department of Chemistry, Norwegian University of Science and Technology, NO-7491, Trondheim, Norway

    Syverin Lierhagen

  5. Department of Biology, Norwegian University of Science and Technology, Høgskoleringen 5, NO-7491, Trondheim, Norway

    Tomasz Maciej Ciesielski & Bjørn Munro Jenssen

  6. CSIRO Oceans and Atmosphere, Castray Esplanade, Battery Point, Hobart, Tasmania, 7004, Australia

    Ruth Eriksen

Authors
  1. Khattapan Jantawongsri
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  2. Rasmus Dyrmose Nørregaard
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  3. Lis Bach
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  10. James Haddy
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  12. Barbara Nowak
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Contributions

K.J.: data curation, formal analysis, funding acquisition, investigation, writing—original draft, formal analysis, investigation, methodology; R.D.N.: conceptualization, data curation, funding acquisition, investigation, resources; L.B.: conceptualization, supervision, writing—review & editing; R.D.: conceptualization, writing—review & editing; C.S.: conceptualization, funding acquisition, project administration, resources, supervision, writing—review & editing; K.J.: investigation, resources, methodology; S.L.: investigation, resources, methodology; T.M.C.: conceptualization, funding acquisition, investigation, methodology, writing—review & editing; B.M.J.: conceptualization, funding acquisition, investigation, methodology, writing—review & editing; J.H.: methodology, writing—review & editing; R.E.: conceptualization, investigation, supervision, writing—review & editing; B.N.: conceptualization, funding acquisition, investigation, project administration, supervision, writing—review & editing. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Barbara Nowak.

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Ethics approval and consent to participate

The Pb exposure experiment was conducted at the Blue Planet, National Aquarium, Copenhagen Denmark, using shorthorn sculpin caught in the southern Kattegat, Denmark (License numbers for the experiment: 2015-15-0201-00692 (Dyreforsøgstilsynet), Ministry of Environment and Food of Denmark approved 28 September 2015).

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The authors declare no competing interests.

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Main findings

After 28 days of Pb exposure of shorthorn sculpins (Myoxocephalus scorpius) to environmentally relevant concentration of aqueous Pb (4.01 ± 3.77 μg/L dissolved Pb), Pb residues were highest in the gills followed by muscle and liver. The Pb residues in gills and liver and Pb concentrations in blood were significantly higher in the sculpin exposed to aqueous Pb than control fish. The number of gill mucous cells/interlamellar unit (ILU) was significantly greater in the exposed fish, and there was a positive correlation between Pb residues in organs (gills, liver, and muscle) and the number of mucous cells/ILU in the gills. The severity score of liver necrosis and telangiectasia in gills was significantly greater in the exposed fish. The severity score of necrosis was positively correlated with Pb levels in liver, and the severity score of telangiectasia in gills was positively correlated with Pb levels in blood.

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Jantawongsri, K., Nørregaard, R.D., Bach, L. et al. Histopathological effects of short-term aqueous exposure to environmentally relevant concentration of lead (Pb) in shorthorn sculpin (Myoxocephalus scorpius) under laboratory conditions. Environ Sci Pollut Res 28, 61423–61440 (2021). https://doi.org/10.1007/s11356-021-14972-6

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