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Acute Toxicity of Bismuth to the Earthworm Eisenia andrei
International Journal of Ecotoxicology and Ecobiology
Volume 2, Issue 3, September 2017, Pages: 125-133
Received: May 30, 2017; Accepted: Jul. 3, 2017; Published: Aug. 9, 2017
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Zohra Omouri, INRS-Institut Armand Frappier, Laval, Canada; National Research Council of Canada, Montreal, Canada
Jalal Hawari, Department of Civil, Geological and Mining Engineering, Polytechnic Montreal, Montreal, Canada
Michel Fournier, INRS-Institut Armand Frappier, Laval, Canada
Pierre Yves Robidoux, National Research Council of Canada, Montreal, Canada; AGAT Laboratories, Montreal, Canada
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Bismuth (Bi) is increasingly used in several industrial applications including the production of alloys, drugs, cosmetics and munitions formulations. However, little information is available on the environmental fate and ecotoxicological effects of Bi. The present study describes 14 days acute toxicity of Bi, added as Bi citrate to a natural sandy soil, to the adult earthworm Eisenia andrei. Total measured Bi concentrations were 298.0, 399.5, 431.0, and 469.5 mg Bi/kg dry soil. Data indicates that Bi was toxic to Eisenia andrei, as determined by LC50 and LOEC, i.e., 416.0 and 399.5 mg Bi/kg dry soil, respectively. At 14 days in the presence of Eisenia andrei the bioaccessible fraction of Bi in soil, as determined in KNO3 aqueous soil extracts, increased by a factor ranging from 1.6 to 30.0 compared to those measured at the beginning of experiment. Moreover, this study shows that an increase in pH caused by the presence of earthworm in soil was accompanied by increase in Bi bioaccessibility and consequently toxicity. For example, when Bi bioaccessibility increased from 0.262 to 7.516 mg Bi/kg dry soil, the mortality rate increased from 0 to 79%. Assuming that there were at least two routes by which Eisania andrei enhanced Bi bioaccessibility; one route was guided by the mobility, the biochemical (mucus) and the biological (bacteria) interactions of Eisenia andrei with soil constituents, and the other route was marked by the death of earthworms and the release of the accumulated Bi from the carcass.
Bismuth, Bioaccessibility, Soil, Acute Toxicity, Eisenia andrei
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Zohra Omouri, Jalal Hawari, Michel Fournier, Pierre Yves Robidoux, Acute Toxicity of Bismuth to the Earthworm Eisenia andrei, International Journal of Ecotoxicology and Ecobiology. Vol. 2, No. 3, 2017, pp. 125-133. doi: 10.11648/j.ijee.20170203.15
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H. J. M. Bowen, Environmental chemistry of the elements. London; New York: Academic Press, 1979.
M. Filella, "How reliable are environmental data on ‘orphan’ elements? The case of bismuth concentrations in surface waters," Journal of Environmental Monitoring, 2010.
Migratory Bird Hunting; Extension of Decision on the Conditional Approval of Bismuth-Tin Shot as Nontoxic for the 1996–97 Season, 61, 1996.
D. S. Urgast, Ellingsen, D. G., B. Berlinger, E. Eilertsen, Friisk, G., V. Skaug, Thomassen, Y., Beattie, J. H., and I.-S. Kwun, Feldmann, J., "Multi-elemental bio-imaging of rat tissue from a study investigating the bioavailability of bismuth from shotgun pellets," Analytical and bioanalytical chemistry, 2012.
U. S. Geological Survey, "Mineral Commodity Summaries 2002,," 2002.
U. S. Geological Survey, "Mineral Commodity Summaries 2016,," 2016.
A. Marois, A. Gagnon, S. Thiboutot, G. Ampleman, and M. Bouchard, "Caractérisation des sols de surface et de la biomasse dans les secteurs d’entraînement, Base des Forces canadiennes, Valcartier," Defence Research and Development Canada Valcartier, Department of National Defence Canada DRDC-VALCARTIER-TR-2004-206, 2004.
Y. Berthelot, "Évaluation de la biodisponibilité des métaux et des matériaux énergétiques dans des sols provenant de sites d'entraînement militaire," Doctorat, Université du Québec à Montréal, Montreal, Quebec, Canada, 2007.
C. A. Johnson, H. Moench, P. Wersin, P. Kugler, and C. Wenger, "Solubility of Antimony and Other Elements in Samples Taken from Shooting Ranges," Journal of Environmental Quality, 2005.
J. Amneklev, A. Augustsson, L. Sörme, and B. Bergbäck, "Bismuth and Silver in Cosmetic Products: A Source of Environmental and Resource Concern?" Journal of Industrial Ecology, vol. 20, pp. 99-106, 2016.
H. Hou, T. Takamatsu, M. K. Koshikawa, and M. Hosomi, "Concentrations ofAg, In, Sn, Sb and Bi, and their chemical fractionation in typical soils in Japan," European Journal of Soil Science, 2006.
H. Hou, T. Takamatsu, M. K. Koshikawa, and M. Hosomi, "Migration of silver, indium, tin, antimony, and bismuth and variations in their chemical fractions on addition to uncontaminated soils," Soil Science, vol. 170, pp. 624-639, 2005.
J. R. Lambert and P. Midolo, "The actions of bismuth in the treatment of Helicobacter pylori infection," Alimentary Pharmacology & Therapeutics, vol. 11 Suppl 1, pp. 27-33, Apr 1997.
G. C. Sanderson, W. L. Anderson, G. L. Foley, K. L. Duncan, L. M. Skowron, J. D. Brawn, et al., Acute toxicity of ingested bismuth alloy shot in game-farm mallards. Toxicity of ingested bismuth alloy shot in game-farm mallards: chronic health effects and effects on reproduction vol. 35. Champaign, IL: Illinois Natural History Survey, 1997.
J. K. Ringelman, M. W. Miller, and W. F. Andelt, "Effects of Ingested Tungsten-Bismuth-Tin Shot on Captive Mallards," The Journal of Wildlife Management, 1993.
L. A. Tillman, F. M. Drake, J. S. Dixon, and J. R. Wood, "Safety of bismuth in the treatment of gastrointestinal diseases," Alimentary Pharmacology & Therapeutics vol. 10, pp. 459–467 1996.
N. S. Fahey, "The use of science in environmental policy making and the implications for health: A case study of bismuth shotshells," University of Waterloo, Ontario, Canada, 2005.
Y. Berthelot, É. Valton, A. Auroy, B. Trottier, and P. Y. Robidoux, "Integration of toxicological and chemical tools to assess the bioavailability of metals and energetic compounds in contaminated soils," Chemosphere, vol. 74, pp. 166-177, 12// 2008.
C. Wei, Q. Deng, F. Wu, Z. Fu, and L. Xu, "Arsenic, antimony, and bismuth uptake and accumulation by plants in an old antimony mine, China," Biological Trace Element Research, 2011.
C. Edwards, "The Importance of Earthworms as Key Representatives of the Soil Fauna," in Earthworm Ecology, ed: CRC Press, 2004, pp. 3-11.
W. J. G. M. Peijnenburg, R. Baerselman, A. C. de Groot, T. Jager, L. Posthuma, and R. P. M. Van Veen, "Relating Environmental Availability to Bioavailability: Soil-Type-Dependent Metal Accumulation in the Oligochaete Eisenia andrei," Ecotoxicology and Environmental Safety, vol. 44, pp. 294-310, 11// 1999.
P. Y. Robidoux, J. Hawari, G. Bardai, L. Paquet, G. Ampleman, S. Thiboutot, et al., "TNT, RDX, and HMX decrease earthworm (Eisenia andrei) life-cycle responses in a spiked natural forest soil," Arch Environ Contam Toxicol, vol. 43, pp. 379-88, Nov 2002.
K. Savard, Y. Berthelot, A. Auroy, P. A. Spear, B. Trottier, and P. Y. Robidoux, "Effects of HMX-Lead Mixtures on Reproduction of the Earthworm Eisenia Andrei," Archives of Environmental Contamination and Toxicology, vol. 53, pp. 351-358, 2007.
P. Y. Robidoux, P. Gong, M. Sarrazin, G. Bardai, L. Paquet, J. Hawari, et al., "Toxicity assessment of contaminated soils from an antitank firing range," Ecotoxicol Environ Saf, vol. 58, pp. 300-13, Jul 2004.
P. Y. Robidoux, C. Svendsen, J. Caumartin, J. Hawari, G. Ampleman, S. Thiboutot, et al., "Chronic toxicity of energetic compounds in soil determined using the earthworm (Eisenia andrei) reproduction test," Environmental Toxicology and Chemistry, 2000.
ISO, "Soil Quality — Determination of pH. International Standard ISO 10390," ed, 1994.
OECD, " Test No. 207: Earthworm, Acute Toxicity Tests," ed: OECD Publishing, 1984.
S. Sauvé, M. B. McBride, and W. H. Hendershot, "Speciation of Lead in Contaminated Soils," Environmental Pollution, 11/12/ 1997.
N. He, X. Li, D. Feng, M. Wu, R. Chen, T. Chen, et al., "Exploring the toxicity of a bismuth-asparagine coordination polymer on the early development of zebrafish embryos," Chemical Research in Toxicology, Jan 18 2013.
B. Leussink, J. F. Nagelkerke, B. van de Water, A. Slillerveer, G. B. van der Voet, A. Srinivasan, et al., "Pathways of proximal tubular cell death in bismuth nephrotoxicity," Toxicology and Applied Pharmacology, 2002.
B. S. Khangarot and S. Das, "Acute toxicity of metals and reference toxicants to a freshwater ostracod, Cypris subglobosa Sowerby, 1840 and correlation to EC50 values of other test models," Journal of Hazardous Materials, 2009.
B. S. Khangarot, "Toxicity of metals to a freshwater tubificid worm, Tubifex tubifex (Muller)," Bulletin of Environmental Contamination and Toxicology, vol. 46, pp. 906-12, Jun 1991.
C. R. Hammond, "The elements," in Handbook of Chemistry and Physics, 87th ed., D. R. E. Lide, Ed., ed CRC Press, Boca Raton, FL, USA, 2007, pp. 4.1–4.42.
A. Slikkerveer and F. A. Wolff, "Pharmacokinetics and toxicity of bismuth compounds," Medical Toxicology Adverse Drug Experience, vol. 4, pp. 303-23, Sep-Oct 1989.
V. Rodilla, A. T. Miles, W. Jenner, and G. M. Hawksworth, "Exposure of cultured human proximal tubular cells to cadmium, mercury, zinc and bismuth: toxicity and metallothionein induction," Chemico-Biological Interactions, vol. 115, pp. 71–83, 1998.
J. J. Scott-Fordsmand, D. Stevens, and M. McLaughlin, "Do earthworms mobilize fixed zinc from ingested soil?," Environmental Science and Technology, vol. 38, pp. 3036–9, 2004.
M. G. Vijver, J. P. M. Vink, C. J. H. Miermans, and C. A. M. van Gestel, "Oral sealing using glue: a new method to distinguish between intestinal and dermal uptake of metals in earthworms," Soil Biology and Biochemistry, 1// 2003.
T. Sizmur and M. E. Hodson, "Do earthworms impact metal mobility and availability in soil? – A review," Environmental Pollution, vol. 157, pp. 1981-1989, 7// 2009.
W. K. Ma, B. A. Smith, G. L. Stephenson, and S. D. Siciliano, "Development of a simulated earthworm gut for determining bioaccessible arsenic, copper, and zinc from soil," Environmental Toxicology and Chemistry, Jul 2009.
E. Meers, G. Du Laing, F. M. G. Tack, and M. G. Verloo, "Heavy Metal Displacement by Exchangeable Bases (Ca, Mg, K, Na) in Soils and Sediments," Soil Science, 2009.
J. Qian, X.-q. Shan, Z.-j. Wang, and Q. Tu, "Distribution and plant availability of heavy metals in different particle-size fractions of soil," Science of The Total Environment, 8/30/ 1996.
A. Matthews, C. Omono, and S. Kakulu, "Comparison of Digestion Methods for the Determination of Metal Levels in Soils in Itakpe, Kogi State, Nigeria," International Journal of Pure and Applied Sciences and Technology, vol. 13, pp. 42-48, 2012.
G. S. R. Krishnamurti and R. Naidu, "Solid−Solution Speciation and Phytoavailability of Copper and Zinc in Soils," Environmental Science and Technology, 2002.
B. A. Smith, B. Greenberg, and G. L. Stephenson, "Comparison of biological and chemical measures of metal bioavailability in field soils: Test of a novel simulated earthworm gut extraction," Chemosphere, vol. 81, pp. 755–766, Oct 2010.
B. Wen, X.-y. Hu, Y. Liu, W.-s. Wang, M.-h. Feng, and X.-q. Shan, "The role of earthworms (Eisenia fetida) in influencing bioavailability of heavy metals in soils," Biology and Fertility of Soils, 2004.
A. Rada, A. El Gharmali, M. Elmeray, and J. L. Morel, "Bioavailability of cadmium and copper in two soils from the sewage farm of Marrakech city (Morocco): effect of earthworms," Agricoltura Mediterranea vol. 126, pp. 364–368, 1996.
B. Wen, Y. Liu, X.-y. Hu, and X.-q. Shan, "Effect of earthworms (Eisenia fetida) on the fractionation and bioavailability of rare earth elements in nine Chinese soils," Chemosphere, May 2006.
M. P. Ireland, "The effect of earthworm Dendrobaena rubida on the solubility of lead, zinc, and calcium in heavy metal contaminated soil in Wales," Journal of Soil Science, 1975.
Y. Ma, N. M. Dickinson, and M. H. Wong, "Toxicity of Pb/Zn mine tailings to the earthworm Pheretima and the effects of burrowing on metal availability," Biol Fertil Soils, vol. 36, pp. 79–86, 2002.
M. Udovic, Z. Plavc, and D. Lestan, "The effect of earthworms on the fractionation, mobility and bioavailability of Pb, Zn and Cd before and after soil leaching with EDTA," Chemosphere, 11// 2007.
K. E. Lee, Earthworms: Their Ecology and Relationships with Soils and Land Use: Academic Press, 1985.
L. G. Garcı´a-Montero, I. Valverde-Asenjo, M. A. Grande-Ortı´z, C. Menta, and I. Hernando, "Impact of earthworm casts on soil pH and calcium carbonate in black truffle burns," Agroforest Syst, vol. 87, pp. 815–826, 2013.
S. Schrader, "Influence of earthworms on the pH conditions of their environment by cutaneous mucus secretion," Zoologischer Anzeiger vol. 233, pp. 211–219, 1994.
S. Salmon, "Earthworm excreta (mucus and urine) affect the distribution of springtails in forest soils," Biology and Fertility of Soils, 2001.
S. Sauvé, W. Hendershot, and Allen Herbert E., "Solid-Solution Partitioning of Metals in Contaminated Soils:  Dependence on pH, Total Metal Burden, and Organic Matter," Environmental Science and Technology, 2000.
D. J. Spurgeon and S. P. Hopkin, "Effects of variations of the organic matter content and pH of soils on the availability and toxicity of zinc to the earthworm Eisenia fetida," Pedobiologia, vol. 40, pp. 80-96, 1996.
M. A. Kashem and B. R. Singh, "Metal availability in contaminated soils: I. Effects of floodingand organic matter on changes in Eh, pH and solubility of Cd, Ni andZn," Nutrient Cycling in Agroecosystems, vol. 61, pp. 247-255, 2001.
J. S. Rieuwerts, I. Thornton, M. E. Farago, and M. R. Ashmore, "Factors influencing metal bioavailability in soils: preliminary investigations for the development of a critical loads approach for metals," Chemical Speciation & Bioavailability, vol. 10, pp. 61-75, 1998/01/01 1998.
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