Skip to main content
SpringerLink
Log in
Book cover

Vanadium pp 73–92Cite as

Hyper-Accumulation of Vanadium in Polychaetes

  • Chapter
  • First Online:

Abstract

The present chapter summarizes our current knowledge on vanadium accumulation in polychaetes, with special emphasis on tube-dwelling fan worms of the Sabellidae family. Some of these species exhibit the unusual capability to hyperaccumulate vanadium at levels several order of magnitude higher than those commonly found in most aquatic organisms. Concentrations higher than 5,000 and 10,000 μg/g were measured in branchial crowns of Pseudopotamilla occelata and Perkinsiana littoralis respectively, stored in vacuoles of the epithelial cells. These tissues appear as feather-like filaments, typically expanded for filter-feeding and respiration activities, while the rest of the body remain protected inside the tube. Feeding trials suggested that the elevated levels of vanadium in branchial filaments of sabellids can act as chemical deterrents against predation in more exposed tissues. A similar function, recently proposed also for the elevated levels of arsenic in branchial crowns of Sabella spallanzanii suggest that hyperaccumulation of toxic metals is a common antipredatory strategy for branchial crowns of sabellid polychaetes, which often results unpalatable for consumers.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms. Science 281:207–209

    Article  CAS  Google Scholar 

  2. Rehder D (2003) Biological and medicinal aspects of vanadium. Inorg Chem Commun 6: 604–617

    Article  CAS  Google Scholar 

  3. Sepe A, Ciaralli L, Ciprotti M, Giordano R, Funari E, Costantini S (2003) Determination of cadmium, chromium, lead and vanadium in six fish species from the Adriatic Sea. Food Addit Contam 20:543–552

    Article  CAS  Google Scholar 

  4. Trefry JH, Metz S (1989) Role of hydrothermal precipitates in the geochemical cycling of vanadium. Nature 342:531–533

    Article  CAS  Google Scholar 

  5. Popham JD, D’Auria JM (1982) A new sentinel organism for vanadium and titanium. Mar Pollut Bull 13:25–27

    Article  CAS  Google Scholar 

  6. Ishii T, Otake T, Okoshi K, Nakahara M, Nakamura R (1994) Intracellular localization of vanadium in the fan worm Pseudopotamilla occelata. Mar Biol 121:143–151

    Article  CAS  Google Scholar 

  7. Fattorini D, Notti A, Nigro M, Regoli F (2010) Hyperaccumulation of vanadium in the Antarctic polychaete Perkinsiana littoralis as a natural chemical defense against predation. Environ Sci Pollut Res Int 17:220–228

    Article  CAS  Google Scholar 

  8. Gibbs PE, Bryan GW, Ryan KP (1981) Copper accumulation by the polychaete Melinna palmata: an antipredation mechanism? J Mar Biol Assoc UK 61:707–722

    Article  CAS  Google Scholar 

  9. Fattorini D, Notti A, Halt MN, Gambi MC, Regoli F (2005) Levels and chemical speciation of arsenic in polychaetes: a review. Mar Ecol 26:255–264

    Article  CAS  Google Scholar 

  10. Sandrini JZ, Regoli F, Fattorini D, Notti A, Ferreira Inácio A, Linde-Arias AR, Laurino J, Bainy ACS, Marins LFF, Monserrat JM (2006) Short-term responses to cadmium exposure in the estuarine polychaete Laeonereis acuta (polychaeta, Nereididae): subcellular distribution and oxidative stress generation. Environ Toxicol Chem 25:1337–1344

    Article  CAS  Google Scholar 

  11. Fukushima M, Suzuki H, Saito K, Chatt A (2008) Vanadium levels in marine organisms of Onagawa Bay in Japan. Environ Monit Assess 141:329–337

    Article  Google Scholar 

  12. Grotti M, Soggia F, Lagomarsino C, Dalla Riva S, Goessler W, Francesconi KA (2008) Natural variability and distribution of trace elements in marine organisms from Antarctic coastal environments. Antarctic Sci 20:39–51

    Article  Google Scholar 

  13. Bellante A, Sprovieri M, Buscaino G, Salvagio Manta D, Buffa G, Di Stefano V, Bonanno A, Barra M, Patti B, Giacoma C, Mazzola S (2009) Trace elements and vanadium in tissues and organs of species of cetaceans from Italian coasts. Chem Ecol 25:311–323

    Article  CAS  Google Scholar 

  14. Bashirpoor M, Schmidt H, Schulzke C, Rehder D (1997) Models for vanadate-dependent haloperoxidases: vanadium complexes with 04N-Donor Sets. Chem Ber 130:651–657

    Article  CAS  Google Scholar 

  15. Kawakami N, Ueki T, Amata Y, Kanamori K, Matsuo K, Gekko K, Michibata H (2009) A novel vanadium reductase, Vanabin2, forms a possible cascade involved in electron transfer. Biochim Biophys Acta 1794:674–679

    CAS  Google Scholar 

  16. Michibata H, Hirata J, Uesaka M, Numakunai T, Sakurai H (1987) Separation of vanadocytes: determination and characterization of vanadium ion in the separated blood cells of the ascidian, Ascidia ahodori. J Exp Zool 244:33–38

    Article  CAS  Google Scholar 

  17. Michibata H, Hirose H, Sugiyama K, Ookubo Y, Kanamori K (1990) Extraction of a vanadium-binding substance (vanadobin) from the blood cells of several ascidian species. Biol Bull Mar Biol Lab Woods Hole 179:140–147

    Article  CAS  Google Scholar 

  18. Michibata H, Terada T, Anada N, Yamakawa K, Numakunai T (1986) The accumulation and distribution of vanadium, iron and manganese in some solitary ascidians. Biol Bull Mar Biol Lab Woods Hole 171:672–681

    Article  CAS  Google Scholar 

  19. Michibata H, Uyama T (1990) Extraction of vanadium-binding substances (vanadobin) from a subpopulation of signet ring cells newly identified as vanadocytes in ascidians. J Exp Zool 254:132–137

    Article  CAS  Google Scholar 

  20. Michibata H, Uyama T, Ueki T, Kanamori K (2002) Vanadocytes, cells hold the key to resolving the highly selective accumulation and reduction of vanadium in ascidians. Microsc Res Tech 56:421–434

    Article  CAS  Google Scholar 

  21. Kanda T, Nose Y, Wuchiyama J, Uyama T, Moriyama Y, Michibata H (1997) Identification of a vanadium-associated protein from the vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 14:37–42

    Article  CAS  Google Scholar 

  22. Ueki T, Adachi T, Kawano S, Aoshima M, Yamaguchi N, Kanamori K, Michibata H (2003) Vanadium-binding proteins (vanabins) from a vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1626:43–50

    CAS  Google Scholar 

  23. Minganti V, Capelli R, De Pellegrini R (1998) The concentrations of Pb, Cd, Cu, Zn, and V in Adamussium colbecki from Terra Nova Bay (Antarctica). Int J Environ Anal Chem 71: 257–263

    Article  CAS  Google Scholar 

  24. El-Naggar MEE, Al-Amoudi OA (1989) Heavy metal levels in several species of marine algae from the Red Sea of Saudi Arabia. JKAU Sci 1:5–13

    Article  Google Scholar 

  25. Lavilla I, Vilas P, Bendicho C (2008) Fast determination of arsenic, selenium, nickel and vanadium in fish and shellfish by electrothermal atomic absorption spectrometry following ultrasound-assisted extraction. Food Chem 106:403–409

    Article  CAS  Google Scholar 

  26. Protasowicki M, Dural M, Jaremek J (2008) Trace metals in the shells of blue mussels (Mytilus edulis) from the Poland coast of Baltic sea. Environ Monit Assess 141:329–337

    Article  CAS  Google Scholar 

  27. Chiffoleau JF, Chauvaud L, Amouroux D, Barats A, Dufour A (2004) Nickel and vanadium contamination of benthic invertebrates following the “Erika” wreck. Aquat Living Resour 17:273–280

    Article  CAS  Google Scholar 

  28. Alfonso JA, Azócar JA, LaBrecque JJ, Benzo Z, Marcano E, Gómez CV, Quintal M (2005) Temporal and spatial variation of trace metals in clams Tivela mactroidea along the Venezuelan coast. Mar Pollut Bull 50:1713–1744

    Article  Google Scholar 

  29. Fattorini D, Notti A, Di Mento R, Cicero AM, Gabellini M, Russo A, Regoli F (2008) Seasonal, spatial and inter-annual variations of trace metals in mussels from the Adriatic Sea: a regional gradient for arsenic and implications for monitoring the impact of off-shore activities. Chemosphere 72:1524–1533

    Article  CAS  Google Scholar 

  30. Regoli F (1998) Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean mussel Mytilus galloprovincialis. Arch Environ Contam Toxicol 34:48–63

    Article  CAS  Google Scholar 

  31. Miramand P, Guary JC (1980) High concentrations of some heavy metals in tissues of the Mediterranean Octopus. Bull Environ Contam Toxicol 24:738–788

    Article  Google Scholar 

  32. Miramand P, Bentley D (1992) Concentration and distribution of heavy metals in tissues of two cephalopods, Eledone cirrhosa and Sepia officinalis, from the French coast of the English Channel. Mar Biol 114:407–414

    Article  CAS  Google Scholar 

  33. Miramand P, Bustamante P, Bentley D, Kouéta N (2006) Variation of heavy metal concentrations (Ag, Cd, Co, Cu, Fe, Pb, V and Zn) during the life cycle of the common cuttlefish Sepia officinalis. Sci Total Environ 361:132–143

    Article  CAS  Google Scholar 

  34. Bustamante P, Grigioni S, Boucher-Rodoni R, Caurant F, Miramand P (2000) Bioaccumulation of 12 trace elements in the tissues of the nautilus Nautilus macromphalus from New Caledonia. Mar Pollut Bull 40:688–696

    Article  CAS  Google Scholar 

  35. Abdel-Moati MAR, Nasir NA (1997) Bioaccumulation of chromium, nickel, lead and vanadium in some commercial fish and prawn from Qatari waters. Qatar Univ Sci J 17:195–203

    Google Scholar 

  36. Bu-Olayan AH, Subrahmanyam MNV (1998) Trace metal concentrations in the crab Macrophthalmus depressus and sediments on the Kuwait coast. Environ Monit Assess 53:297–304

    Article  CAS  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Ikemoto T, Tu NPC, Okuda N, Iwata A, Omori K, Tanabe S, Tuyen BC, Takeuchi I (2008) Biomagnification of trace elements in the aquatic food web in the Mekong Delta, South Vietnam using stable carbon and nitrogen isotope analysis. Arch Environ Contam Toxicol 54:504–515

    Article  CAS  Google Scholar 

  39. Anan Y, Kunito K, Tanabe S, Mitrofanov I, Aubrey DG (2005) Trace element accumulation in fishes collected from coastal waters of the Caspian Sea. Mar Pollut Bull 51:882–888

    Article  CAS  Google Scholar 

  40. Mackey EA, Becker PR, Demiralp R, Greenberg RR, Koster BJ, Wise SA (1996) Bioccumulation of vanadium and other trace metals in liver of Alaskan cetaceans and pinnipeds. Arch Environ Contam Toxicol 30:503–512

    Article  CAS  Google Scholar 

  41. Mackey EA, Demiralp R, Becker PR, Greenberg RR, Koster BJ, Wise SA (1995) Trace element concentrations in cetacean liver tissues archived in the National Marine Mammal Tissue Bank. Sci Total Environ 175:25–41

    Article  CAS  Google Scholar 

  42. Kunito T, Nakamura S, Ikemoto T, Anan Y, Kubota R, Tanabe S, Rosas CW, Fillmann G, Readman JW (2004) Concentration and subcellular distribution of trace elements in liver of small cetaceans incidentally caught along the Brazilian coast. Mar Pollut Bull 49:574–587

    Article  CAS  Google Scholar 

  43. Agusa T, Nomura K, Kunito T, Anan Y, Iwata H, Miyazaki N, Tatsukawa R, Tanabe S (2008) Interelement relationship and age-related variation of trace element concentrations in liver of striped dolphins (Stenella coeruleoalba) from Japanese coastal waters. Mar Pollut Bull 57: 807–815

    Article  CAS  Google Scholar 

  44. Young JS, Adee RR, Piscopo I, Buschbom RL (1981) Effects of copper on the sabellid polychaete. Eudistylia vancouveri. II. Copper accumulation and tissue injury in the branchial crown. Arch Environ Contam Toxicol 10:87–104

    Article  CAS  Google Scholar 

  45. Young JS, Buschbom RL, Gurtisen JM, Joyce SP (1979) Effects of copper on the sabellid polychaete. Eudistylia vancouveri: I. Concentration limits for copper accumulation. Arch Environ Contam Toxicol 8:97–106

    Article  CAS  Google Scholar 

  46. Ishii T, Nakai I, Numako C, Okoshi K, Otake T (1993) Discovery of a new vanadium accumulator, the fan worm Pseudopotamilla occelata. Naturwissenschaften 80:268–270

    Article  CAS  Google Scholar 

  47. Bagaveeva EV, Zvyagintsev AY (2000) The introduction of polychaetes Hydroides elegans (Haswell), Polydora limicola (Annenkova), and Pseudopotamilla occelata (Moore) to the Northwestern part of the East Sea. Ocean Res 22:25–36

    Google Scholar 

  48. Cole AG, Hall BK (2004) The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage-like tissues within the Metazoa. Zoology 107:261–273

    Article  Google Scholar 

  49. Yoshihara M, Ueki T, Yamaguchi N, Kamino K, Michibata H (2008) Characterization of a novel vanadium-binding protein (VBP-129) from blood plasma of vanadium-rich ascidian Ascidia sydneiensis samea. Biochim Biophys Acta 1780:256–263

    CAS  Google Scholar 

  50. Uyama T, Nose Y, Wuchiyama J, Moriyama Y, Michibata H (1997) Finding of the same antigens in the polychaete, Pseudopotamilla occelata, as those in the vanadium-rich ascidian, Ascidia sydneiensis samea. Zool Sci 14:43–47

    Article  CAS  Google Scholar 

  51. Giangrande A, Gambi MC (1997) The genus Perkinsiana (Polychaeta, Sabellidae) from Antarctica, with descriptions of the new species P. milae and P. borsibrunoi. Zool Scripta 26:267–278

    Article  Google Scholar 

  52. Bocchetti R, Fattorini D, Gambi MC, Regoli F (2004) Trace metal concentrations and susceptibility to oxidative stress in the polychaete Sabella spallanzanii (Gmelin) (Sabellidae): potential role of antioxidants in revealing stressful environmental conditions in the Mediterranean. Arch Environ Contam Toxicol 46:353–361

    Article  CAS  Google Scholar 

  53. Fattorini D, Bocchetti R, Bompadre S, Regoli F (2004) Total content and chemical speciation of arsenic in the polychaete Sabella spallanzanii. Mar Environ Res 58:839–843

    Article  CAS  Google Scholar 

  54. Fattorini D, Regoli F (2004) Arsenic speciation in tissues of the Mediterranean polychaete Sabella spallanzanii. Environ Toxicol Chem 23:1881–1887

    Article  CAS  Google Scholar 

  55. Bargagli R (2005) Antarctic ecosystems. Environmental contamination, climate change and human impact. Springer, Berlin

    Google Scholar 

  56. Lichtenegger HC, Schöberl T, Bartl MH, Waite H, Stucky GD (2002) High abrasion resistance with sparse mineralization: copper biomineral in worm jaws. Science 298:389–392

    Article  CAS  Google Scholar 

  57. Lichtenegger HC, Schöberl T, Ruokolainen JT, Cross JO, Heald SM, Birkedal H, Waite JH, Stucky GD (2003) Zinc and mechanical prowess in the jaws of Nereis, a marine worm. P Natl Acad Sci USA 100:9144–9149

    Article  CAS  Google Scholar 

  58. Nejmeddine A, Dhainaut-Courtois N, Baert JL, Sautière P, Fournet B, Boulenguer P (1988) Purification and characterization of a cadmium-binding protein from Nereis diversicolor (Annelida, Polychaeta). Comp Biochem Physiol C 89:321–326

    Article  Google Scholar 

  59. McClintock JB, Baker BJ (1997) A review of the chemical ecology of Antarctic marine invertebrates. Am Zool 37:329–342

    CAS  Google Scholar 

  60. McClintock JB, Baker BJ (2001) Marine chemical ecology, Marine science series. CRC, Boca Raton

    Book  Google Scholar 

  61. Paul VJ, Puglisi MP, Ritson-Williams R (2006) Marine chemical ecology. Nat Prod Res 23:153–180

    Article  CAS  Google Scholar 

  62. Kicklighter CE, Hay ME (2006) Integrating prey defensive traits: contrasts of marine worms from temperate and tropical habitats. Ecol Monogr 76:195–215

    Article  Google Scholar 

  63. Kicklighter CE, Hay ME (2007) To avoid or deter: interactions among defensive and escape strategies in sabellid worms. Oecologia 151:161–173

    Article  Google Scholar 

  64. Fattorini D, Alonso-Hernandez CM, Diaz-Asencio M, Munoz-Caravaca A, Pannacciulli FG, Tangherlini M, Regoli F (2004) Chemical speciation of arsenic in different marine organisms: importance in monitoring studies. Mar Environ Res 58:845–850

    Article  CAS  Google Scholar 

  65. Fattorini D, Notti A, Regoli F (2006) Characterization of arsenic content in marine organisms from temperate, tropical, and polar environments. Chem Ecol 22:405–414

    Article  CAS  Google Scholar 

  66. Ventura-Lima J, Fattorini D, Notti A, Monserrat JM, Regoli F (2010) Bioaccumulation patterns and biological effects of arsenic in aquatic organisms. In: Gosselin JD, Fancher IM (eds) Environmental health risks: lead poisoning and arsenic exposure. Nova Science Publishers Inc., New York, Chapter 6. ISBN 978-1-60741-781-1

    Google Scholar 

  67. Notti A, Fattorini D, Razzetti EM, Regoli F (2007) Bioaccumulation and biotransformation of arsenic in the Mediterranean polychaete Sabella spallanzanii: experimental observations. Environ Toxicol Chem 26:1186–1191

    Article  CAS  Google Scholar 

  68. Avila C, Taboada S, Nuñez-Pons L (2008) Antarctic marine chemical ecology: what is next? Mar Ecol 29:1–71

    Article  CAS  Google Scholar 

  69. Goerke H, Emrich R, Weber K, Duchene JC (1991) Concentrations and localization of brominated metabolites in the genus Thelepus (Polychaeta, Terebellidae). Comp Biochem Physiol B 99:203–206

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, Via Ranieri (Montedago) 65, Ancona, 60131, Italy

    Daniele Fattorini & Francesco Regoli

Authors
  1. Daniele Fattorini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Francesco Regoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francesco Regoli .

Editor information

Editors and Affiliations

  1. , Biological Sciences, Hiroshima University, Kagamiyama 1-3-1, Hiroshima, 739-8526, Japan

    Hitoshi Michibata

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Fattorini, D., Regoli, F. (2012). Hyper-Accumulation of Vanadium in Polychaetes. In: Michibata, H. (eds) Vanadium. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0913-3_4

Download citation

Publish with us

Policies and ethics

Search

Navigation