Skip to main content
SpringerLink
Log in

The mussel Mytilus galloprovincialis (Crimea, Black Sea) as a source of essential trace elements in human nutrition

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Micronutrients, or essential trace elements, are important components in various metabolic processes inherent to the normal functioning of organism. To date, a substantial part of the world population suffers from a lack of micronutrients in the diet. Mussels are an important and cheap source of nutrients, which can be utilized to mitigate the micronutrient deficiency in the world. In the present work, using inductively coupled plasma mass spectrometry, the contents of the micronutrients Cr, Fe, Cu, Zn, Se, I, and Mo were studied for the first time in soft tissues, shell liquor, and byssus of females and males of the mussel Mytilus galloprovincialis as the promising sources of essential elements in the human diet. Fe, Zn, and I were the most abundant micronutrients in the three body parts. Significant sex-related differences in the body parts were detected only for Fe, which was more abundant in byssus of males, and Zn, which exhibited higher levels in shell liquor of females. Significant tissue-related differences were registered in the contents of all the elements under study. M. galloprovincialis meat was characterized as the optimal source of I and Se for covering the daily human needs. Regardless of sex, byssus turned out to be richer in Fe, I, Cu, Cr, and Mo in comparison with soft tissues, which fact allows recommending this body part for the preparation of dietary supplements to compensate for the deficiency of these micronutrients in the human body.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data that support the finding of this study are available from corresponding author upon reasonable request.

References

  1. Agadzhanian NA, Skalny AV (2001) Chemical elements in the environment and the human ecological portrait. KMK, Moscow (in Russian)

    Google Scholar 

  2. Skalnaya MG, Skalny AV (2018) Essential trace elements in human health: a physician’s view. Tomsk State University Publishing House, Tomsk

    Google Scholar 

  3. Dahl L, Molin M, Amlund H, Meltzer HM, Julshamn K, Alexander J, Sloth JJ (2010) Stability of arsenic compounds in seafood samples during processing and storage by freezing. Food Chem 123(3):720–727. https://doi.org/10.1016/j.foodchem.2010.05.041

    Article  CAS  Google Scholar 

  4. Ritchie H, Roser M (2017) Micronutrient deficiency. Our World in Data. WHO

    Google Scholar 

  5. Santos I, Diniz MS, Carvalho ML, Santos JP (2014) Assessment of essential elements and heavy metals content on Mytilus galloprovincialis from river Tagus estuary. Biol Trace Elem Res 159(1–3):233–240. https://doi.org/10.1007/s12011-014-9974-y

  6. Singh R, Gautam N, Mishra A, Gupta R (2011) Heavy metals and living systems: an overview. Ind J Pharmacol 43(3):246–253. https://doi.org/10.4103/0253-7613.81505

    Article  CAS  Google Scholar 

  7. Willer DF, Aldridge DC (2020) Vitamin bullets. Microencapsulated feeds to fortify shellfish and tackle human nutrient deficiencies. Front Nutr 2:102. https://doi.org/10.3389/fnut.2020.00102

    Article  CAS  Google Scholar 

  8. Mertz W (1998) Review of the scientific basis for establishing the essentiality of trace elements. Biol Trace Elem Res 66(1–3):185–191. https://doi.org/10.1007/BF02783137

    Article  CAS  PubMed  Google Scholar 

  9. WHO (1996) Trace elements in human nutrition and health. World Health Organization, Geneva

    Google Scholar 

  10. WHO (2005) Vitamin and mineral requirements in human nutrition. World Health Organization, Geneva

    Google Scholar 

  11. Bertini I, Gray HB, Lippard SJ, Valentine JS (1994) Bioinorganic Chemistry. University Science Books, Mill Valley, CA

    Google Scholar 

  12. Bertini I, Sigel A, Sigel H (2001) Handbook on Metalloproteins. Marcel Dekker, New York

    Google Scholar 

  13. Bugg TDH (2012) Introduction to enzyme and coenzyme chemistry. Wiley, Chichester, UK

    Book  Google Scholar 

  14. Foster AW, Osman D, Robinson NJ (2014) Metal preferences and metallation. J Biol Chem 289(41):28095–28103. https://doi.org/10.1074/jbc.R114.588145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Prejanò M, Alberto ME, Russo N, Toscano M, Marino T (2020) The effects of the metal ion substitution into the active site of metalloenzymes: a theoretical insight on some selected cases. Catalysts 10(9):1038. https://doi.org/10.3390/catal10091038

    Article  CAS  Google Scholar 

  16. Skalny AV (2004) Chemical elements in human physiology and ecology. Mir, Moscow (in Russian)

    Google Scholar 

  17. Poznyakovskiy AA (2009)

  18. Sukhanov BP, Tutel'yan VA, Onishchenko GG (2009) State policy of healthy nutrition of the population: objectives and ways of implementation. GEOTAR-Media, Moscow (in Russian)

    Google Scholar 

  19. Tutel'yan VA, Razumov AN, Vyalkov AI, Mikhailov VI, Moskalenko KA, Odinets AG, Sbezhneva VG, Sergeev VN (2010) Scientific basics of healthy nutrition. Panorama Publishing House, Moscow (in Russian)

    Google Scholar 

  20. Koral S, Süleyman B (2017) Determination of seasonal variation of amino acid and fatty acid composition of Mediterranean mussel (Mytilus galloprovincialis Lamarck, 1819) in the eastern Black Sea. Aquacult Stud 17(1):17–28 (in Turkish). https://doi.org/10.17693/yunusae.v17i26557.274790

    Google Scholar 

  21. Rodríguez-Hernández Á, Zumbado M, Henríquez-Hernández LA, Boada LD, Luzardo OP (2019) Dietary intake of essential, toxic, and potentially toxic elements from mussels (Mytilus spp.) in the Spanish population: a nutritional assessment. Nutrients 11:864. https://doi.org/10.3390/nu11040864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Venugopal V, Gopakumar K (2017) Shellfish: nutritive value, health benefits, and consumer safety. Compr Rev Food Sci Food Saf 16(6):1219–1242. https://doi.org/10.1111/1541-4337.12312

    Article  CAS  PubMed  Google Scholar 

  23. Arnautov MV (2013) Development of technology of prodcing enzymatic hydrolyzate from mussel meat to create fortified foods. PhD thesis. VNIRO, Moscow

    Google Scholar 

  24. Konrad G, Lieske B (1979) Herstellung und Verwendung von Protein Hydrolysaten: Ein Überblick. Lebensmittel Industrie 10:445–449

    Google Scholar 

  25. Moniruzzaman M, Sku S, Chowdhury P, Tanu MB, Yeasmine S, Hossen MN, Min T, Bai SC, Mahmud Y (2021) Nutritional evaluation of some economically important marine and freshwater mollusc species of Bangladesh. Heliyon 7(5):e07088. https://doi.org/10.1016/j.heliyon.2021.e07088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. FAO (2022) The State of World Fisheries and Aquaculture 2022. FAO, Rome

    Google Scholar 

  27. Wada O (2004) What are trace elements? —their deficiency and excess states. JMAJ 47(8):351–358

    Google Scholar 

  28. Budko DF, Lobus NV, Vedenin AA (2021) Dataset on the content of major, trace, and rare-earth elements in the bottom sediments and bivalve mollusks of the Kara Sea (Arctic Ocean). Data in Brief 36:107087. https://doi.org/10.1016/j.dib.2021.107087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Esposito M, Canzanella S, Danese A, Pepe A, Gallo P (2022) Essential and non-essential elements in razor clams (Solen marginatus, Pulteney, 1799) from the Domitio littoral in Campania (southwestern Tyrrhenian Sea, Italy). Toxics 10(8):452. https://doi.org/10.3390/toxics10080452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nicholson S, Szefer P (2003) Accumulation of metals in the soft tissues, byssus and shell of the mytilid Perna viridis (Bivalvia: Mytilidae) from polluted and uncontaminated locations in Hong Kong coastal waters. Mar Pollut Bull 46(8):1039–1043. https://doi.org/10.1016/S0025-326X(03)00152-8

    Article  CAS  Google Scholar 

  31. Pavlov DF, Bezuidenhout J, Frontasyeva MV, Goryainova ZI (2015) Differences in trace element content between non-indigenous farmed and invasive bivalve mollusks of the South African coast. Am J Anal Chem 6(11):886–897. https://doi.org/10.4236/ajac.2015.611084

    Article  CAS  Google Scholar 

  32. Kapranov SV, Karavantseva NV, Bobko NI, Ryabushko VI, Kapranova LL (2021b) Sex- and sexual maturation-related aspects of the element accumulation in soft tissues of the bivalve Mytilus galloprovincialis Lam. collected off coasts of Sevastopol (southwestern Crimea, Black Sea). Environ Sci Pollut Res 28:21553–21576. https://doi.org/10.1007/s11356-020-12024-z

    Article  Google Scholar 

  33. Latouche YD, Mix MC (1982) The effects of depuration, size and sex on trace metal levels in bay mussels. Mar Pollut Bull 13(1):27–29. https://doi.org/10.1016/0025-326X(82)90494-5

    Article  CAS  Google Scholar 

  34. Lobel PB, Bajdik CD, Belkhode SP, Jackson SE, Longerich HP (1991) Improved protocol for collecting mussel watch specimens taking into account sex, size, condition, shell shape, and chronological age. Arch Environ Contam Toxicol 21:409–414. https://doi.org/10.1007/BF01060364

    Article  Google Scholar 

  35. Richir J, Gobert S (2014) The effect of size, weight, body compartment, sex and reproductive status on the bioaccumulation of 19 trace elements in rope-grown Mytilus galloprovincialis. Ecol Indicat 36:33–47. https://doi.org/10.1016/j.ecolind.2013.06.021

    Article  CAS  Google Scholar 

  36. Grinchenko ОА, Baban VM, Yanchuk PI (2011) The influence of taurine on the ion content of gastric juice at the histamine stimulation of secretion in dogs. Sci Notes of VI Vernadsky Taurida Nat Univ Biol Chem 24(63):107–116

    Google Scholar 

  37. Ayushin NB (2001) Taurine: pharmaceutical properties and prospects for isolating it from marine organisms. Izvestiya TINRO 129:129–145 (in Russian)

    Google Scholar 

  38. O’Brien EC, Farkas E, Rockenbauer A, Nolan KB (1999) Metal complexes of taurine. The first reported solution equilibrium studies for complex formation by taurine at physiological pH; the copper(II)–glycylglycinate–taurine and the copper(II)–glycylaspartate–taurine systems. J Inorg Biochem 77(3-4):135–139. https://doi.org/10.1016/S0162-0134(99)00182-8

    Article  PubMed  Google Scholar 

  39. Petrova YS, Neudachina LK (2013) Potentiometric study of complexation between taurine and metal ions. Russ J Inorg Chem 58:617–620. https://doi.org/10.1134/S0036023613050173

    Article  CAS  Google Scholar 

  40. Priemel T, Palia G, Förste F, Jehle F, Sviben S, Mantouvalou I, Zaslansky P, Bertinetti L, Harrington MJ (2021) Microfluidic-like fabrication of metal ion–cured bioadhesives by mussels. Science 374(6564):206–211. https://doi.org/10.1126/science.abi9702

    Article  CAS  PubMed  Google Scholar 

  41. Sever MJ, Weisser JT, Monahan J, Srinivasan S, Wilker JJ (2004) Metal-mediated cross-linking in the generation of a marine-mussel adhesive. Angewandte Chemie Int Ed 43(4):448–450. https://doi.org/10.1002/anie.200352759

    Article  Google Scholar 

  42. Zhong C, Gurry T, Cheng AA, Downey J, Deng Z, Stultz CM, Lu TK (2014) Strong underwater adhesives made by self-assembling multi-protein nanofibres. Nat Nanotechnol 9:858–866 https://doi.org/10.1038/nnano.2014.199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Chelyadina NS, Kapranov SV, Popov MA, Smirnova LL, Bobko NI (2022) Trace elements in the detoxifying and accumulating body parts of Mytilus galloprovincialis Lamark, 1819 (Crimea, Black Sea): human health risks and effect of the sampling site location. Environ Sci Pollut Res 29(40):61352–61369. https://doi.org/10.1007/s11356-022-20186-1

    Article  CAS  Google Scholar 

  44. Szefer P, Frelek K, Szefer K, Lee CB, Kim BS, Warzocha J, Zdrojewska I, Ciesielski T (2002) Distribution and relationships of trace metals in soft tissue, byssus and shells of Mytilus edulis trossulus from the southern Baltic. Environ Pollut 120(2):423–444. https://doi.org/10.1016/S0269-7491(02)00111-2

    Article  CAS  PubMed  Google Scholar 

  45. Szefer P, Ikuta K, Frelek K, Zdrojewska I, Nabrzyski M (1999) Mercury and other trace metals (Ag, Cr, Co, and Ni) in soft tissue and byssus of Mytilus edulis from the east coast of Kyushu Island, Japan. Sci Total Environ 229(3):227–234. https://doi.org/10.1016/S0048-9697(99)00079-0

    Article  CAS  PubMed  Google Scholar 

  46. Yap CK, Tan SG (2007) Iron (Fe) concentrations in the byssus and soft tissues of the green-lipped mussel Perna viridis (L.): Byssus as an excretion route of Fe and Fe bioavailability in the coastal waters. Ind J Geo-Mar Sci 36(3):227–234

    CAS  Google Scholar 

  47. Kuftarkova EA, Gubanov VI, Kovrigina NP, Eremin IY, Senicheva MI (2006) Ecological assessment of modern state of waters in the region of interaction of the Sevastopol bay and part of the sea contiguous to it. Mar Ecol J 5(1):72–91 (in Russian)

    Google Scholar 

  48. Ryabushko LI, Pospelova NV, Balycheva DS, Kovrigina NP, Troshchenko OA, Kapranov SV (2017) Epizoon microalgae of the cultivated mollusk Мytilus galloprovincialis Lam. 1819, phytoplankton, hydrological and hydrochemical characteristics in the mussel-and-oyster farm area (Sevastopol, Black Sea). Mar Biol J 2(4):67–83 (in Russian). https://doi.org/10.21072/mbj.2017.02.4.07

    Article  Google Scholar 

  49. Kapranov SV, Kovrigina NP, Troshchenko OA, Rodionova NY (2020) Long-term variations of thermohaline and hydrochemical characteristics in the mussel farm area in the coastal waters off Sevastopol (Black Sea) in 2001–2018. Cont Shelf Res 206:104185. https://doi.org/10.1016/j.csr.2020.104185

    Article  Google Scholar 

  50. Suhre MH, Gertz M, Steegborn C, Scheibel T (2014) Structural and functional features of a collagen-binding matrix protein from the mussel byssus. Nat Commun 5:3392. https://doi.org/10.1038/ncomms4392

    Article  CAS  PubMed  Google Scholar 

  51. Szefer P, Fowler SW, Ikuta K, Osuna PF, Ali AA, Kim BS, Fernandes HM, Belzunce MJ, Guterstam B, Kunzendorf H, Wolowicz M, Hummel H, Deslous-Paoli M (2006) A comparative assessment of heavy metal accumulation in soft parts and byssus of mussels from subarctic, temperate, subtropical and tropical marine environments. Environ Pollut 139(1):70–78. https://doi.org/10.1016/j.envpol.2005.04.031

    Article  CAS  PubMed  Google Scholar 

  52. Ivanov VN, Kholodov VI, Senicheva MI, Pirkova AV, Bulatov KV (1989) Biology of cultivated mussels. Naukova Dumka, Kiev (in Russian)

    Google Scholar 

  53. Kholodov VI, Pirkova AV, Ladygina LV (2017) Cultivation of mussels and oysters in the Black Sea. LLC Izdat-Print, Voronezh (in Russian)

  54. Pirkova AV, Ladygina LV, Shchurov SV (2019) Formation of settlements of mussel Mytilus galloprovincialis (Lamarck, 1819) on collectors of the Laspi Bay farm depending on environmental factors. Sci Notes of VI Vernadsky Crim Fed Univ Biol Chem 5(71):92–106

    Google Scholar 

  55. Chelyadina NS, Pospelova NV, Kopytov YP (2015) Distribution of copper in the tissues of males and females of Mytilus galloprovincialis. Hydrobiol J 51(4):74–79. https://doi.org/10.1615/HydrobJ.v51.i4.90

    Article  Google Scholar 

  56. Pospelova NV (2008) Elements of budget of carotenoids, α-Tocopherol and some metals in the ‘‘Suspended Matter – Mussels – Bio-deposits’’ System. PhD thesis. A.O. Kovalevsky Institute of Biology of the Southern Seas, Sevastopol

  57. George SG, BJS P, Coombs TL (1976) The kinetics of accumulation and excretion of ferric hydroxide in Mytilus edulis (I.) and its distribution in the tissues. J Exp Mar Biol Ecol 23(1):71–84. https://doi.org/10.1016/0022-0981(76)90086-1

    Article  CAS  Google Scholar 

  58. Kapranov SV, Karavantseva NV, Bobko NI, Ryabushko VI, Kapranova LL (2021a) Element contents in three commercially important edible mollusks harvested off the southwestern coast of Crimea (Black Sea) and assessment of human health risks from their consumption. Foods 10(10):2313. https://doi.org/10.3390/foods10102313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Chemnitzer R (2019) Strategies for achieving the lowest possible detection limits in ICP-MS. Spectroscopy 34(10):12–16

    CAS  Google Scholar 

  60. Clarke KR, Gorley RN, Somerfield PJ, Warwick RM (2014) Change in marine communities: an approach to statistical analysis and Interpretation. PRIMER-E, Plymouth, UK

    Google Scholar 

  61. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):4

    Google Scholar 

  62. Mégevand P (2017) Games-Howell post-hoc test for one-way ANOVA. https://github.com/pierremegevand/games_howell. Accessed 29 Aug 2022.

  63. Boran M, Altinok I (2010) A review of heavy matals in water, sediment and living organisms in the Black Sea. Turk J Fish Aquat Sci 10:565–572. https://doi.org/10.4194/trjfas.2010.0418

    Article  Google Scholar 

  64. Fowler SW (1990) Critical review of selected heavy metal and chlorinated hydrocarbon concentrations in the marine environment. Mar Environ Res 29(1):1–64. https://doi.org/10.1016/0141-1136(90)90027-L

    Article  CAS  Google Scholar 

  65. Rainbow PS, Phillips DJH (1993) Cosmopolitan biomonitors of trace metals. Mar Pollut Bull 26(11):593–601. https://doi.org/10.1016/0025-326X(93)90497-8

    Article  CAS  Google Scholar 

  66. Casas S, Gonzalez J-L, Andral B, Cossa D (2008) Relation between metal concentration in water and metal content of marine mussels (Mytilus galloprovincialis): impact of physiology. Environ Toxicol Chem 27(7):1543–1552. https://doi.org/10.1897/07-418.1

    Article  CAS  PubMed  Google Scholar 

  67. Chasapis CT, Loutsidou AC, Spiliopoulou CA, Stefanidou ME (2012) Zinc and human health: an update. Arch Toxicol 86(4):521–534. https://doi.org/10.1007/s00204-011-0775-1

  68. MAGRAMA (2015) El mercado del mejillón en España. MAGRAMA (Ministerio de Agricultura, Alimentación y Medio Ambiente) (in Spanish), Madrid, Spain

  69. Campolim MB, Henriques MB, Petesse ML, Rezende KFO, Barbieri E (2017) Metal trace elements in mussels in Urubuqueçaba Island, Santos Bay, Brazil. Pesquisa Agropecuária Brasileira, Brasília 52(12):1131–1139. https://doi.org/10.1590/S0100-204X2017001200001

    Article  Google Scholar 

  70. Catharino MGM, Vasconcellos MBA, Kirschbaum AA, Gasparro MR, Minei CC, de Sousa ECPM, Seo D, Moreira EG (2012) Biomonitoring of coastal regions of São Paulo state, Brazil, using mussels Perna perna. J Radioanal Nucl Chem 291:113–117. https://doi.org/10.1007/s10967-011-1291-8

    Article  CAS  Google Scholar 

  71. Richir J, Gobert S (2016) Trace elements in marine environments: occurrence, threats and monitoring with special focus on the coastal Mediterranean. J Anal Toxicol 6(1):1000349. https://doi.org/10.4172/2161-0525.1000349

    Article  Google Scholar 

  72. Yigit M, Celikkol B, Yilmaz S, Bulut M, Ozalp B, Dwyer RL, Maita M, Kizilkaya B, Yigit Ü, Ergün S, Gürses K, Buyukates Y (2018) Bioaccumulation of trace metals in Mediterranean mussels (Mytilus galloprovincialis) from a fish farm with copper-alloy mesh pens and potential risk assessment. Hum Ecol Risk Assess 24(2):465–481. https://doi.org/10.1080/10807039.2017.1387476

    Article  CAS  Google Scholar 

  73. Gupta SK, Singh J (2011) Evaluation of mollusc as sensitive indicatior of heavy metal pollution in aquatic system: a review. IIOAB J 2(1):49–57

    Google Scholar 

  74. Goldhaber SB (2003) Trace element risk assessment: essentiality vs. toxicity. Regul Toxicol Pharmacol 38(2):232–242. https://doi.org/10.1016/S0273-2300(02)00020-X

    Article  CAS  PubMed  Google Scholar 

  75. Nordberg GF, Fowler BA, Nordberg M, Friberg LT (2007) Handbook on the toxicology of metals, 3rd edn. Elsevier, Amsterdam

  76. George SG (1990) Biochemical and cytological assessments of metal toxicity in marine animals. In: Furness RW, Rainbow PS (eds) Heavy metals in the marine environment. CRC Press, Boca Raton, FL, pp 123–142

    Google Scholar 

  77. Ganz T (2013) Systemic iron homeostasis. Physiol Rev 93(4):1721–1741. https://doi.org/10.1152/physrev.00008.2013

    Article  CAS  PubMed  Google Scholar 

  78. Jelani QU, Katz SD (2010) Treatment of anemia in heart failure: potential risks and benefits of intravenous iron therapy in cardiovascular disease. Cardiol Rev 18(5):240–250. https://doi.org/10.1097/CRD.0b013e3181e71150

    Article  PubMed  PubMed Central  Google Scholar 

  79. Outten FW, Theil EC (2009) Iron-based redox switches in biology. Antioxid Redox Signal 11(5):1029–1046. https://doi.org/10.1089/ars.2008.2296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Ni S, Yuan Y, Kuang Y, Li X (2022) Iron metabolism and immune regulation. Front Immunol 13:816282. https://doi.org/10.3389/fimmu.2022.816282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Ward RJ, Crichton RR, Taylor DL, Della Corte L, Srai SK, Dexter DT (2011) Iron and the immune system. J Neur Trans 118(3):315–328. https://doi.org/10.1007/s00702-010-0479-3

    Article  CAS  Google Scholar 

  82. de Benoist B, McLean E, Egli I, Cogswell M (2008) Worldwide prevalence of anaemia 1993–2005: WHO global database on anaemia. World Health Organization, Geneva, Switzerland, p 40

    Google Scholar 

  83. McLean E, Cogswell M, Egli I, Woidyla D, de Benoist B (2009) Worldwide prevalence of anaemia, WHO vitamin and mineral nutrition information system, 1993–2005. Public Health Nutr 12(4):444–454. https://doi.org/10.1017/S1368980008002401

    Article  PubMed  Google Scholar 

  84. WHO (2007) Assessing the Iron Status of Populations: Including Literature Reviews. World Health Organization, Geneva, Switzerland

    Google Scholar 

  85. Aggett PJ (2012) Iron. In: Erdman JW, Macdonald IA, Zeisel SH (eds) Present knowledge in nutrition. Wiley-Blackwell, Washington, DC, pp 506–520

    Chapter  Google Scholar 

  86. Murray-Kolbe LE, Beard J (2010) Iron. In: Coates PM, Betz JM, Blackman MR, Cragg GM, Levine M, Moss J, White JD (eds) Encyclopedia of dietary supplements, 2nd edn. Informa Healthcare, London, pp 432–438

    Chapter  Google Scholar 

  87. Gobert S, Daemers-Lambert C, Bouquegneau JM (1992) Physiological stress and heavy metal contamination of mussels Mytilus edulis along the Belgian coast. Bulletin de la Societe Royale des Sciences de Liege (Belgium) 61(1-2):177–194

    CAS  Google Scholar 

  88. Desideri D, Meli MA, Roselli C, Feduzi L (2009) A biomonitoring study: 210Po and heavy metals in mussels. J Radioanal Nucl Chem 279(2):591–600. https://doi.org/10.1007/s10967-008-7334-0

    Article  CAS  Google Scholar 

  89. Çevik U, Damla N, Kobya AI, Bulut VN, Duran C, Dalgıc G, Bozacı R (2008) Assessment of metal element concentrations in mussel (M. Galloprovincialis) in Eastern Black Sea, Turkey. J Hazard Mater 160(2):396–401. https://doi.org/10.1016/j.jhazmat.2008.03.010

    Article  CAS  PubMed  Google Scholar 

  90. Priemel T, Degtyar E, Dean M, Harrington MJ (2017) Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication. Nat Commun 8:14539. https://doi.org/10.1038/ncomms14539

  91. Chelyadina NS, Popov MA (2021) Mortality of the mussel. Mytilus galloprovincialis (Lamark, 1819) depending on sex. Tomsk State University Jornal Biology 55:166–176. https://doi.org/10.17223/19988591/55/9/

  92. Prasad AS (2008) Zinc in human health: effect of zinc on immune cells. Mol Med 14(5-6):353–357. https://doi.org/10.2119/2008-00033.Prasad

    Article  CAS  PubMed Central  Google Scholar 

  93. Barnard ND (2020) Micronutrients in health and disease. In: Barnard ND (ed) Nutrition guide for clinicians, 3rd edn. Physicians Committee for Responsible Medicine

    Google Scholar 

  94. John E, Laskow TC, Buchser WJ, Pitt BR, Basse PH, Butterfield LH, Kalinski P, Lotze MT (2010) Zinc in innate and adaptive tumor immunity. J Transl Med 8:118. https://doi.org/10.1186/1479-5876-8-118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Rink L, Haase H (2007) Zinc homeostasis and immunity. Trends Immunol 28(1):1–4. https://doi.org/10.1016/j.it.2006.11.005

    Article  CAS  PubMed  Google Scholar 

  96. Rutter GA (2010) Think zinc: New roles for zinc in the control of insulin secretion. Islets 2(1):49–50. https://doi.org/10.4161/isl.2.1.10259

    Article  PubMed  Google Scholar 

  97. Dong FM (2001) The nutritional value of shellfish. University of Washington, Seattle, WA

    Google Scholar 

  98. Pearson HBC, Dallas LJ, Comber SDW, Braungardt CB, Worsfold PJ, Jha AN (2018) Mixtures of tritiated water, zinc and dissolved organic carbon: assessing interactive bioaccumulation and genotoxic effects in marine mussels, Mytilus galloprovincialis. J Environ Radioact 187:133–143. https://doi.org/10.1016/j.jenvrad.2017.12.018

    Article  CAS  PubMed  Google Scholar 

  99. Stanković S, Jović M, Milanov R, Joksimović D (2011) Trace elements concentrations (Zn, Cu, Pb, Cd, As and Hg) in the Mediterranean mussel (Mytilus galloprovincialis) and evaluation of mussel quality and possible human health risk from cultivated and wild sites of the southeastern Adriatic Sea, Montenegro. J Serb Chem Soc 76(12):1725–1737. https://doi.org/10.2298/JSC110420095S

    Article  CAS  Google Scholar 

  100. Viarengo A, Marro A, Marchi B, Burlando B (2000) Single and combined effects of heavy metals and hormones on lysosomes of haemolymph cells from the mussel Mytilus galloprovincialis. Mar Biol 137:907–912. https://doi.org/10.1007/s002270000391

    Article  CAS  Google Scholar 

  101. Elliott NG, Swain R, Ritz DA (1986) Metal interaction during accumulation by the mussel Mytilus edulis planulatus. Mar Biol 93(3):395–399. https://doi.org/10.1007/BF00401107

    Article  CAS  Google Scholar 

  102. Kapranova LL, Ryabushko VI, Nekhoroshev MV, Kapranov SV (2021) Steroid hormones, selenium, and zinc in the gonads – gametes – larvae biological system of the mussel Mytilus galloprovincialis Lam. Mar Biol J 6(4):39–50. https://doi.org/10.21072/mbj.2021.06.4.04

    Article  Google Scholar 

  103. Prasad AS (2014) Zinc: An antioxidant and anti-inflammatory agent: role of zinc in degenerative disorders of aging. J Trace Elem Med Biol 28(4):364–371. https://doi.org/10.1016/j.jtemb.2014.07.019

    Article  CAS  PubMed  Google Scholar 

  104. George SG, Pirie BJS (2009) Metabolism of zinc in the mussel, Mytilus edulis (L.): a combined ultrastructural and biochemical study. J Mar Biol Assoc UK 60(3):575–590. https://doi.org/10.1017/S0025315400040273

    Article  Google Scholar 

  105. Karavantseva NV (2012) The content of copper and zinc in gametes and gonads of the mussel Mytilus galloprovincialis Lam. In: The 2nd International Scientific and Practical Conference "Biodiversity and Sustainable Development". Simferopol, Ukraine, pp 367–369

    Google Scholar 

  106. Bilandžić N, Sedak M, Đokić M, Varenina I, Solomun Kolanović B, Božić Đ, Brstilo M, Šimić B (2014) Determination of zinc concentrations in foods of animal origin, fish and shellfish from Croatia and assessment of their contribution to dietary intake. J Food Comp Anal 35(2):61–66. https://doi.org/10.1016/j.jfca.2014.04.006

    Article  CAS  Google Scholar 

  107. Belivermiş M, Kılıç Ö, Çotuk Y (2016) Assessment of metal concentrations in indigenous and caged mussels (Mytilus galloprovincialis) on entire Turkish coastline. Chemosphere 144:1980–1987. https://doi.org/10.1016/j.chemosphere.2015.10.098

    Article  CAS  PubMed  Google Scholar 

  108. Strogyloudi E, Angelidis MO, Christides A, Papathanassiou E (2012) Metal concentrations and metallothionein levels in Mytilus galloprovincialis from Elefsis bay (Saronikos gulf, Greece). Environ Monit Assess 184(12):7189–7205. https://doi.org/10.1007/s10661-011-2490-z

    Article  CAS  PubMed  Google Scholar 

  109. Bat L, Üstün F, Baki OG (2012) Trace element concentrations in the Mediterranean mussel Mytilus galloprovincialis Lamarck, 1819 caught from Sinop coast of the Black Sea, Turkey. Open Mar Biol J 6:1–5. https://doi.org/10.2174/1874450801206010001

    Article  Google Scholar 

  110. Türk Çulha S, Çulha M, Karayücel İ, Çelik MY, Işler Y (2017) Heavy metals in Mytilus galloprovincialis, suspended particulate matter and sediment from offshore submerged longline system, Black Sea. Int J Environ Sci Technol 14(2):385–396. https://doi.org/10.1007/s13762-016-1158-1

    Article  CAS  Google Scholar 

  111. Bat L, Öztekin HC (2016) Heavy metals in Mytilus galloprovincialis, Rapana venosa and Eriphia verrucosa from the Black Sea coasts of Turkey as bioindicators of pollution. Walailak J Sci Technol 13(9):715–728

    Google Scholar 

  112. Tepe Y, Süer N (2016) The levels of heavy metals in the Mediterranean mussel (Mytilus Galloprovincialis Lamarck, 1819); example of Giresun coasts of the Black Sea Turkey. Ind J Geo-Mar Sci 45(2):283–289

    Google Scholar 

  113. Ryabushko VI, Toichkin AM, Kapranov SV (2022) Heavy metals and arsenic in soft tissues of the gastropod Rapana venosa (Valenciennes, 1846) collected on a mollusk farm off Sevastopol (southwestern Crimea, Black Sea): assessing human health risk and locating regional contamination areas. Bull Environ Contam Toxicol 108(6):1039–1045. https://doi.org/10.1007/s00128-021-03451-w

    Article  CAS  Google Scholar 

  114. Casarini LM, Henriques MB, Graça-Lopes R, de Souza MR (2010) Chemical and bacteriological evaluation of the water and mussels from Santos bay, São Paulo. Brazil. Revista do Instituto Adolfo Lutz 69(3):297–303

    CAS  Google Scholar 

  115. Carvalho CEV, Cavalcante MPO, Gomes MP, Faria VV, Rezende CE (2001) Heavy metal distribution in mussel (Perna perna, L.) from Santana Island, Macaé, SE, Brazil. Ecol Manag Restor 4(1):1–5

    Google Scholar 

  116. Roméo M, Sidoumou Z, Gnassia-Barelli M (2000) Heavy metals in various molluscs from the Mauritanian coast. Bull Environ Contam Toxicol 65(2):269–276. https://doi.org/10.1007/s0012800124

    Article  PubMed  Google Scholar 

  117. Yap CK, Edward FB, Tan SG (2007) Determination of heavy metal distributions in the green-lipped mussel Perna viridis as bioindicators of heavy metal contamination in the Johore Straits and Senggarang, Peninsular Malaysia. Trends Appl Sci Res 2(4):284–294. https://doi.org/10.3923/tasr.2007.284.294

    Article  CAS  Google Scholar 

  118. Falchuk KH, Montorzi M (2001) Zinc physiology and biochemistry in oocytes and embryos. In: Maret W (ed) Zinc biochemistry, physiology, and homeostasis: recent insights and current trends. Springer, Dordrecht, Netherlands, pp 199–209

    Chapter  Google Scholar 

  119. Seeler JF, Sharma A, Zaluzec NJ, Bleher R, Lai B, Schultz EG, Hoffman BM, LaBonne C, Woodruff TK, O’Halloran TV (2021) Metal ion fluxes controlling amphibian fertilization. Nat Chem 13(7):683–691. https://doi.org/10.1038/s41557-021-00705-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Oberleas D, Harland B, Skalny A (2008) Biological role of macro- and trace elements in humans and animals. Nauka, Saint Petersburg

    Google Scholar 

  121. Portulano C, Paroder-Belenitsky M, Carrasco N (2014) The Na+/I− Symporter (NIS): mechanism and medical impact. Endocr Rev 35(1):106–149. https://doi.org/10.1210/er.2012-1036

    Article  CAS  PubMed  Google Scholar 

  122. Syed S (2015) Iodine and the "near" eradication of cretinism. Pediatrics 135(4):594–596. https://doi.org/10.1542/peds.2014-3718

    Article  PubMed  Google Scholar 

  123. Roti E, Uberti ED (2001) Iodine excess and hyperthyroidism. Thyroid 11(5):493–500. https://doi.org/10.1089/105072501300176453

    Article  CAS  PubMed  Google Scholar 

  124. Markova ML (2014) Iodine and foodstuffs containing it. Federal Biomedical Agency, Moscow (in Russian)

    Google Scholar 

  125. Otis B, Oliveira N (2001) Iodine. In: Harvard TH (ed) The nutrition source. Chan School of Public Health, Boston, MA

    Google Scholar 

  126. Nekhoroshkov P, Bezuidenhout J, Zinicovscaia I, Yushin N, Vergel K, Frontasyeva M (2021) Levels of eements in typical mussels from the southern coast of Africa (Namibia, South Africa, Mozambique): Safety aspect. Water 13(22):3238. https://doi.org/10.3390/w13223238

    Article  CAS  Google Scholar 

  127. Gorbman A, Clements M, O'Brien R (1954) Utilization of radioiodine by invertebrates, with special study of several annelida and mollusca. J Exp Zool 127(1):75–92. https://doi.org/10.1002/jez.1401270105

    Article  CAS  Google Scholar 

  128. Anke M (2004) Essential and toxic effects of macro, trace and ultratrace elements in the nutrition of man. In: Anke M, Merian E, Ihnat M, Stoeppler M (eds) Elements and their compounds in the environment. Wiley-VCH, Weinheim, pp 343–367

    Chapter  Google Scholar 

  129. Parakhonsky AP (2015) The role of copper in the body and the implications of its imbalance. Nat Human Stud 10(4):73–84 (in Russian)

    Google Scholar 

  130. Collins JF (2014) Copper. In: Ross AC, Caballero B, Cousins RJ, Tucker KL, Ziegler TR (eds) Modern Nutrition in Health and Disease, 11th edn. Lippincott Williams & Wilkins, Baltimore, MD, pp 206–216

    Google Scholar 

  131. Prohaska JR (2012) Copper. In: Erdman JW, Macdonald IA, Zeisel SH (eds) Present knowledge in nutrition, 10th edn. Wiley-Blackwell, Washington, DC, pp 540–553

    Chapter  Google Scholar 

  132. Giacomin M, Gillis PL, Bianchini A, Wood CM (2013) Interactive effects of copper and dissolved organic matter on sodium uptake, copper bioaccumulation, and oxidative stress in juvenile freshwater mussels (Lampsilis siliquoidea). Aquat Toxicol 144-145:105–115. https://doi.org/10.1016/j.aquatox.2013.09.028

    Article  CAS  PubMed  Google Scholar 

  133. Solomon EI, Lowery MD (1993) Electronic structure contributions to function in bioinorganic chemistry. Science 259(5101):1575–1581. https://doi.org/10.1126/science.8384374

    Article  CAS  PubMed  Google Scholar 

  134. Taylor HH, Anstiss JM (1999) Copper and haemocyanin dynamics in aquatic invertebrates. Mar Freshw Res 50(8):907–931. https://doi.org/10.1071/MF99117

    Article  CAS  Google Scholar 

  135. Jitar O, Teodosiu C, Oros A, Plavan G, Nicoara M (2015) Bioaccumulation of heavy metals in marine organisms from the Romanian sector of the Black Sea. New Biotechnol 32(3):369–378. https://doi.org/10.1016/j.nbt.2014.11.004

    Article  CAS  Google Scholar 

  136. Temerdashev ZA, Eletskii II, Kaunova AA, Korpakova IG (2017) Determination of heavy metals in Mytilus galloprovincialis Lamarck mussels using the IСP-AES method. Anal Control 21(2):116–124. https://doi.org/10.15826/analitika.2017.21.2.009

    Article  Google Scholar 

  137. Francioni E, Wagener AD, Calixto RD, Bastos GC (2004) Evaluation of Perna perna (Linné, 1758) as a tool to monitoring trace metals contamination in estuarine and coastal waters of Rio de Janeiro, Brazil. J Braz Chem Soc 15(1):103–110. https://doi.org/10.1590/S0103-50532004000100016

    Article  CAS  Google Scholar 

  138. Akberali HB, Earnshaw MJ, Marriott KRM (1985) The action of heavy metals on the gametes of the marine mussel, Mytilus edulis (L.)-II. Uptake of copper and zinc and their effect on respiration in the sperm and unfertilized egg. Mar Environ Res 16(1):37–59. https://doi.org/10.1016/0141-1136(85)90019-4

    Article  CAS  Google Scholar 

  139. Hatfield DL, Tsuji PA, Carlson BA, Gladyshev VN (2014) Selenium and selenocysteine: roles in cancer, health, and development. Trends Biochem Sci 39(3):112–120. https://doi.org/10.1016/j.tibs.2013.12.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Anonymous (2021) Selenium injection. In: Anderson LA, Sinha S, Durbin K, Entringer S, Stewart J, Thornton P, Fookes C, Puckey M, France N, Grigg J, Chao S (eds). https://www.drugs.com/pro/selenium-injection.html (accessed 29 August 2022)

  141. Jacobs DS, Finley PR, Demott WR, Horvat RT, Kasten BL Jr, Tilzer LL (2001) Laboratory test handbook with key word index. Lexi-Comp Inc., Hudson, OH

    Google Scholar 

  142. Ahsan U, Kamran Z, Raza I, Ahmad S, Babar W, Riaz MH, Iqbal Z (2014) Role of selenium in male reproduction—A review. Anim Reprod Sci 146(1):55–62. https://doi.org/10.1016/j.anireprosci.2014.01.009

    Article  CAS  PubMed  Google Scholar 

  143. Hill KE, Wu S, Motley AK, Stevenson TD, Winfrey VP, Capecchi MR, Atkins JF, Burk RF (2012) Production of selenoprotein P (Sepp1) by hepatocytes is central to selenium homeostasis. J Biol Chem 287(48):40414–40424. https://doi.org/10.1074/jbc.M112.421404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Aliasgharpour M, Farzami MR (2013) Trace elements in human nutrition: a review. Int J Med Investig 2(3):115–128

    Google Scholar 

  145. Rayman MP (2012) Selenium and human health. Lancet 379(9822):1256–1268. https://doi.org/10.1016/S0140-6736(11)61452-9

    Article  CAS  PubMed  Google Scholar 

  146. WHO (1987) Selenium (environmental health criteria 58). World Health Organization, Geneva, Switzerland

    Google Scholar 

  147. Bartolomé L, Navarro P, Raposo JC, Arana G, Zuloaga O, Etxebarria N, Soto M (2010) Occurrence and distribution of metals in mussels from the Cantabrian coast. Arch Environ Contam Toxicol 59(2):235–243. https://doi.org/10.1007/s00244-010-9476-7

    Article  CAS  PubMed  Google Scholar 

  148. Reutina SV (2009) The rolе of chromium in the person's organism. RUDN J Ecol Life Safety 4:50–55 (in Russian)

    Google Scholar 

  149. Di Bona KR, Love S, Rhodes NR, McAdory D, Sinha SH, Kern N, Kent J, Strickland J, Wilson A, Beaird J, Ramage J, Rasco JF, Vincent JB (2011) Chromium is not an essential trace element for mammals: effects of a “low-chromium” diet. JBIC 16(3):381–390. https://doi.org/10.1007/s00775-010-0734-y

    Article  CAS  PubMed  Google Scholar 

  150. Yoshida M (2012) Is chromium an essential trace element in human nutrition? Nihon Eiseigaku Zasshi 67(4):485–491 (in Japanese). https://doi.org/10.1265/jjh.67.485

    Article  CAS  PubMed  Google Scholar 

  151. Laschinsky N, Kottwitz K, Freund B, Dresow B, Fischer R, Nielsen P (2012) Bioavailability of chromium(III)-supplements in rats and humans. BioMetals 25(5):1051–1060. https://doi.org/10.1007/s10534-012-9571-5

    Article  CAS  Google Scholar 

  152. Dokmeci AH (2017) Assessment of heavy metals in wild mussels Mytilus galloprovincialis from the Marmara Sea coast of Tekirdag (Turkey). 15th International Conference on Environmental Science and Technology. Rhodes, Greece, p CEST2017_00569

  153. Chassard-Bouchaud C, Boutin JF, Hallegot P, Galle P (1989) Chromium uptake, distribution and loss in the mussel Mytilus edulis: a structural, ultrastructural and microanalytical study. Dis Aquat Org 7:117–136. https://doi.org/10.3354/dao007117

    Article  CAS  Google Scholar 

  154. Mendel RR, Kruse T (2012) Cell biology of molybdenum in plants and humans. Biochim Biophys Acta Mol Cell Res 1823(9):1568–1579. https://doi.org/10.1016/j.bbamcr.2012.02.007

    Article  CAS  Google Scholar 

  155. Turnlund JR, Weaver CM, Kim SK, Keyes WR, Gizaw Y, Thompson KH, Peiffer GL (1999) Molybdenum absorption and utilization in humans from soy and kale intrinsically labeled with stable isotopes of molybdenum. Am J Clin Nutr 69(6):1217–1223. https://doi.org/10.1093/ajcn/69.6.1217

    Article  CAS  PubMed  Google Scholar 

  156. Turnlund JR, Keyes WR, Peiffer GL, Chiang G (1995) Molybdenum absorption, excretion, and retention studied with stable isotopes in young men during depletion and repletion. Am J Clin Nutr 61(5):1102–1109. https://doi.org/10.1093/ajcn/61.5.1102

    Article  CAS  PubMed  Google Scholar 

  157. Novotny JA, Turnlund JR (2006) Molybdenum kinetics in men differ during molybdenum depletion and repletion. J Nutr 136(4):953–957. https://doi.org/10.1093/jn/136.4.953

    Article  CAS  PubMed  Google Scholar 

  158. National Research Council (1989) Recommended Dietary Allowances. The National Academies Press, Washington, DC

    Google Scholar 

  159. Eckhert CD (2014) Trace elements. In: Ross AC, Caballero B, Cousins RJ, Tucker KL, Ziegler TR (eds) Modern nutrition in health and disease, 11th edn. Lippincott Williams & Wilkins, Baltimore, MD, pp 206–216

    Google Scholar 

  160. Haque I (1987) Molybdenum in soils and plants and its potential importance to livestock nutrition, with special reference to sub-Saharan Africa. Ilca Bull 26:20–28

    Google Scholar 

  161. Brooks RR, Rumsby MG (1965) The biogeochemistry of trace element uptake by some New Zealand bivalves. Limnol Oceanogr 10(4):521–527. https://doi.org/10.4319/lo.1965.10.4.0521

    Article  Google Scholar 

  162. Yap CK, Ismail A, Tan SG (2005) Byssus of the green-lipped mussel Perna viridis (Linnaeus) as a biomonitoring material for Zn. Russ J Mar Biol 31(2):102–108. https://doi.org/10.1007/s11179-005-0050-5

    Article  CAS  Google Scholar 

  163. Wang W-X, Fisher NS (1997) Modeling the influence of body size on trace element accumulation in the mussel Mytilus edulis. Mar Ecol Prog Ser 161:103–155. https://doi.org/10.3354/meps161103

    Article  Google Scholar 

  164. Coombs TL, Keller PJ (1981) Mytilus byssal threads as an environmental marker for metals. Aquat Toxicol 1(5):291–300. https://doi.org/10.1016/0166-445X(81)90023-0

    Article  CAS  Google Scholar 

  165. Anand PP, Vardhanan YS (2021) Dye and metal ion adsorption ability of Asian green mussel byssus thread complex; their microscopic and thermal property characterization. Environ Technol 9:1–17. https://doi.org/10.1080/09593330.2021.1971776

    Article  CAS  Google Scholar 

  166. Ho T-Y, Quigg A, Finkel ZV, Milligan AJ, Wyman K, Falkowski PG, Morel FMM (2003) The elemental composition of some marine phytoplankton. J Phycol 39(6):1145–1159. https://doi.org/10.1111/j.0022-3646.2003.03-090.x

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Ministry of Science and Higher Education of the Russian Federation within the state assignments 121030300149-0 (“Research on the mechanisms of control of production processes in biotechnological complexes for developing scientific foundations for the production of biologically active materials and technical products of marine genesis»”) and 0012-2021-0007 (“Fundamental and applied research on patterns and mechanisms of formation of regional changes in the natural environment and climate under the influence of global processes in the ocean-atmosphere system and anthropogenic impact”).

Author information

Authors and Affiliations

  1. A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS, 2 Nakhimov ave., 299011, Sevastopol, Russian Federation

    Natalya S. Chelyadina, Sergey V. Kapranov, Mark A. Popov & Nikolay I. Bobko

  2. Institute of Natural and Technical Systems of RAS, Lenin str. 28, Sevastopol, Russian Federation, 299011

    Lyudmila L. Smirnova

Authors
  1. Natalya S. Chelyadina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergey V. Kapranov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark A. Popov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lyudmila L. Smirnova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nikolay I. Bobko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natalya S. Chelyadina.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1:

Supplementary materials

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chelyadina, N.S., Kapranov, S.V., Popov, M.A. et al. The mussel Mytilus galloprovincialis (Crimea, Black Sea) as a source of essential trace elements in human nutrition. Biol Trace Elem Res 201, 5415–5430 (2023). https://doi.org/10.1007/s12011-023-03607-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-023-03607-1

Keywords

Search

Navigation