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.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms. Science 281:207–209
Rehder D (2003) Biological and medicinal aspects of vanadium. Inorg Chem Commun 6: 604–617
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
Trefry JH, Metz S (1989) Role of hydrothermal precipitates in the geochemical cycling of vanadium. Nature 342:531–533
Popham JD, D’Auria JM (1982) A new sentinel organism for vanadium and titanium. Mar Pollut Bull 13:25–27
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Miramand P, Guary JC (1980) High concentrations of some heavy metals in tissues of the Mediterranean Octopus. Bull Environ Contam Toxicol 24:738–788
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Fattorini D, Regoli F (2004) Arsenic speciation in tissues of the Mediterranean polychaete Sabella spallanzanii. Environ Toxicol Chem 23:1881–1887
Bargagli R (2005) Antarctic ecosystems. Environmental contamination, climate change and human impact. Springer, Berlin
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
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
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
McClintock JB, Baker BJ (1997) A review of the chemical ecology of Antarctic marine invertebrates. Am Zool 37:329–342
McClintock JB, Baker BJ (2001) Marine chemical ecology, Marine science series. CRC, Boca Raton
Paul VJ, Puglisi MP, Ritson-Williams R (2006) Marine chemical ecology. Nat Prod Res 23:153–180
Kicklighter CE, Hay ME (2006) Integrating prey defensive traits: contrasts of marine worms from temperate and tropical habitats. Ecol Monogr 76:195–215
Kicklighter CE, Hay ME (2007) To avoid or deter: interactions among defensive and escape strategies in sabellid worms. Oecologia 151:161–173
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
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
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
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
Avila C, Taboada S, Nuñez-Pons L (2008) Antarctic marine chemical ecology: what is next? Mar Ecol 29:1–71
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
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-94-007-0913-3_4
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-0912-6
Online ISBN: 978-94-007-0913-3
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)