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Does acute lead (Pb) contamination influence membrane fatty acid composition and freeze tolerance in intertidal blue mussels in arctic Greenland?

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Abstract

In their natural habitats, organisms are exposed to multiple stressors. Heavy metal contamination stresses the cell membrane due to increased peroxidation of lipids. Likewise, sub-zero air temperatures potentially reduce membrane functionality in ectothermal animals. We tested if acute lead (Pb) exposure for 7 days would influence survival in intertidal blue mussels (Mytilus edulis) after exposure to realistic sub-zero air temperatures. A full factorial experiment with five tissue Pb concentrations between 0 and 3500 μg Pb/g and six sub-zero temperatures from 0 to −17 °C were used to test the hypothesis that sub-lethal effects of Pb may increase the lethality caused by freezing in blue mussels exposed to temperatures simulating Greenland winter conditions. We found a significant effect of temperature on mortality. However, the short-term exposure to Pb did not result in any effects of Pb, nor did we find interactions between Pb and temperature. We analysed the relative abundance of major phospholipid fatty acids (PLFAs) in the gill tissue, but we found no significant effect of Pb tissue concentration on PLFA composition. Results suggest that Pb accumulation has limited effects on freeze tolerance and does not induce membrane damage in terms of persistent lipid peroxidation.

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References

  • Aarset AV (1982) Freezing tolerance in intertidal invertebrates: a review. Comp Biochem Physiol A Physiol 73:571–580. doi:10.1016/0300-9629(82)90264-X

    Article  Google Scholar 

  • Aarset AV, Zachariassen KE (1982) Effects of oil pollution on the freezing tolerance and solute concentration of the blue mussel Mytilus edulis. Mar Biol 72:45–51. doi:10.1007/Bf00393946

    Article  Google Scholar 

  • AMAP (2010) Assessment 2007: oil and gas activities in the Arctic - effects and potential effects, vol I. Arctic Monitoring and Assessment Programme (AMAP), Oslo

    Google Scholar 

  • Ansari TM, Marr IL, Tariq N (2004) Heavy metals in marine pollution perspective: a mini review. J App Sci 4:1–20. doi:10.3923/jas.2004.1.20

    Article  Google Scholar 

  • Bindesbøl AM, Bayley M, Damgaard C, Hedlund K, Holmstrup M (2009) Changes in membrane phospholipids as a mechanistic explanation for decreased freeze tolerance in earthworms exposed to sublethal copper concentrations. Environ Sci Technol 43:5495–5500. doi:10.1021/Es900898y

    Article  Google Scholar 

  • Blicher ME, Sejr MK, Høgslund S (2013) Population structure of Mytilus edulis in the intertidal zone in a sub-Arctic fjord, SW Greenland. Mar Ecol Prog Ser 487:12. doi:10.3354/meps10317

    Article  Google Scholar 

  • Bourget E (1983) Seasonal variations of cold tolerance in intertidal mollusks and relation to environmental conditions in the St. Lawrence Estuary. Can J Zool 61:1193–1201. doi:10.1139/z83-162

    Article  Google Scholar 

  • Burnett NP et al (2013) An improved noninvasive method for measuring heartbeat of intertidal animals. Limnol Oceanogr-Meth 11:91–100. doi:10.4319/Lom.2013.11.91

    Article  Google Scholar 

  • Depledge MH, Rainbow PS (1990) Models of regulation and accumulation of trace-metals in marine invertebrates. Comp Biochem Physiol C 97:1–7. doi:10.1016/0742-8413(90)90163-4

    Article  Google Scholar 

  • Donaldson WE, Knowles SO (1993) Is lead toxicosis a reflection of altered fatty acid composition of membranes? Comp Biochem Physiol 104:377–379. doi:10.1016/0742-8413(93)90003-4

    Article  CAS  Google Scholar 

  • Dowling NJE, Widdel F, White DC (1986) Phospholipid ester linked fatty acid biomarkers of acetate-oxidizing sulfate-reducers and other sulfide-forming bacteria. J Gen Microbiol 132:1815–1825. doi:10.1099/00221287-132-7-1815

    CAS  Google Scholar 

  • Goldberg ED (1986) The mussel watch concept. Environ Monit Assess 7:91–103. doi:10.1007/Bf00398031

    Article  CAS  Google Scholar 

  • Guédard ML, Faure O, Bessoule J-J (2012) Early changes in the fatty acid composition of photosynthetic membrane lipids from Populus nigra grown on a metallurgical landfill. Chemosphere 88:693–698. doi:10.1016/j.chemosphere.2012.03.079

    Article  Google Scholar 

  • Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation. Annu Rev Physiol 57:19–42. doi:10.1146/Annurev.Ph.57.030195.000315

    Article  CAS  Google Scholar 

  • Heugens EHW, Hendriks AJ, Dekker T, van Straalen NM, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31:247–284. doi:10.1080/20014091111695

    Article  CAS  Google Scholar 

  • Høgslund S, Sejr MK, Wiktor J Jr, Blicher ME, Wegeberg S (2014) Intertidal community composition along rocky shores in South-west Greenland: a quantitative approach. Polar Biol. doi:10.1007/s00300-014-1541-7

    Google Scholar 

  • Holmstrup M et al (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408(3746–3762):2009. doi:10.1016/J.Scitotenv.10.067

    Google Scholar 

  • Hooper MJ, Ankley GT, Cristol DA, Maryoung LA, Noyes PD, Pinkerton KE (2013) Interactions between chemical and climate stressors: a role for mechanistic toxicology in assessing climate change risks. Environ Toxicol Chem 32:32–48. doi:10.1002/Etc.2043

    Article  CAS  Google Scholar 

  • Johansen P, Asmund G, Glahder CM, Aastrup P, Secher K (2001) Minedrift og miljø i Grønland. Temarappot fra DMU vol 38. Danmarks Milijøundersøgelser, Aarhus Universitet, 58 pp

  • Johansen P, Asmund G, Riget F, Johansen K (2008) Environmental monitoring at the cryolite mine in Ivittuut, South Greenland 2007. NERI Technical Report No. 674. National Environmental Institute, Aarhus University, 32 pp

  • Koštál V, Berková P, Šimek P (2003) Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comp Biochem Physiol B Biochem Mol Bio 135:407–419. doi:10.1016/S1096-4959(03)00117-9

    Article  Google Scholar 

  • Kramer KJM, Jenner HA, Dezwart D (1989) The valve movement response of mussels: a tool in biological monitoring. Hydrobiologia 188:433–443. doi:10.1007/Bf00027811

    Article  Google Scholar 

  • Lawton LJ, Donaldson WE (1991) Lead-induced tissue fatty acid alterations and lipid peroxidation. Biol Trace Elem Res 28:83–97. doi:10.1007/Bf02863075

    Article  CAS  Google Scholar 

  • Liu GX, Shu MA, Chai XL, Shao YQ, Wu HX, Sun CS, Yang SB (2014) Effect of chronic sublethal exposure of major heavy metals on filtration rate, sex ratio, and gonad development of a bivalve species. Bull Environ Contam Tox 92:71–74. doi:10.1007/S00128-013-1138-9

    Article  CAS  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman & Hall, London

    Book  Google Scholar 

  • Pernet F, Tremblay R, Comeau L, Guderley H (2007) Temperature adaptation in two bivalve species from different thermal habitats: energetics and remodelling of membrane lipids. J Exp Biol 210:2999–3014. doi:10.1242/Jeb.006007

    Article  Google Scholar 

  • Rainbow PS (1995) Biomonitoring of heavy metal availability in the marine environment. Mar Pollut Bull 31:183–192. doi:10.1016/0025-326x(95)00116-5

    Article  CAS  Google Scholar 

  • Schulz-Baldes M (1974) Lead uptake from sea water and food, and lead loss in the common mussel Mytilus edulis. Mar Biol 25:177–193. doi:10.1007/BF00394964

    Article  CAS  Google Scholar 

  • Seed R (1976) Ecology. In: Bayne BL (ed) Marine mussels: their ecology and physiology. Cambridge University Press, New York, p 411 (International Biological Programme 10)

    Google Scholar 

  • Søndergaard J, Asmund G, Johansen P, Riget F (2011) Long-term response of an arctic fiord system to lead-zinc mining and submarine disposal of mine waste (Maarmorilik, West Greenland). Mar Environ Res 71:331–341. doi:10.1016/j.marenvres.2011.03.001

    Article  Google Scholar 

  • Søndergaard J, Bach L, Gustavson K (2014) Measuring bioavailable metals using diffusive gradients in thin films (DGT) and transplanted seaweed (Fucus vesiculosus), blue mussels (Mytilus edulis) and sea snails (Littorina saxatilis) suspended from monitoring buoys near a former lead-zinc mine in West Greenland. Mar Pollut Bull 78:102–109. doi:10.1016/Marpolbul.2013.10.054

    Article  Google Scholar 

  • Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208. doi:10.2174/0929867053764635

    Article  CAS  Google Scholar 

  • Waagner D, Holmstrup M, Bayley M, Sørensen JG (2013) Induced cold-tolerance mechanisms depend on duration of acclimation in the chill-sensitive Folsomia candida (Collembola). J Exp Biol 216:1991–2000. doi:10.1242/Jeb.079814

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. doi:10.1111/J.2041-210x.2009.00001.X

    Article  Google Scholar 

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Acknowledgments

The authors thank Lise Lauridsen for technical support and Christian Damgaard for statistical advice. We also thank Kattegatcentret, Denmark, for providing filtrated seawater. This work is a contribution to the Arctic Science Partnership (ASP) and the ARC cake club.

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Authors and Affiliations

  1. Department of Bioscience, Arctic Research Centre, Aarhus University, C. F. Møllers Allé 8, Building 1110, 8000, Aarhus C, Denmark

    Jakob Thyrring, Bodil Klein Juhl, Martin Holmstrup & Mikael K. Sejr

  2. Section of Soil Fauna Ecology and Ecotoxicology, Department of Bioscience, Aarhus University, Vejlsøvej 25, 8600, Silkeborg, Denmark

    Martin Holmstrup

  3. Greenland Climate Research Centre, Greenland Institute of Natural Resources, Nuuk, Greenland

    Martin E. Blicher & Mikael K. Sejr

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  1. Jakob Thyrring
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  2. Bodil Klein Juhl
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  3. Martin Holmstrup
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  4. Martin E. Blicher
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  5. Mikael K. Sejr
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Correspondence to Jakob Thyrring.

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The authors declare that they have no conflict of interest.

Funding

The study received support from the Danish Environmental Protection Agency within the Danish Cooperation for Environment in the Arctic (DANCEA) and JT was supported by a grant from ‘Selskabet for Arktisk Forskning og Teknologi (SAFT)’.

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Thyrring, J., Juhl, B.K., Holmstrup, M. et al. Does acute lead (Pb) contamination influence membrane fatty acid composition and freeze tolerance in intertidal blue mussels in arctic Greenland?. Ecotoxicology 24, 2036–2042 (2015). https://doi.org/10.1007/s10646-015-1539-0

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  • DOI: https://doi.org/10.1007/s10646-015-1539-0

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