Biokinetics of Coping Mechanism of Freshwater tilapia following Exposure to Waterborne and Dietary Copper

The purpose of this study was to understand the main sources of copper (Cu) accumulation in target organs of tilapia (Oreochromis mossambicus) and to investigate how the organism mediate the process of Cu accumulation under prolonged conditions. By measuring both dietary and waterborne Cu accumulation and total concentrations in tilapia with biokinetic modeling approach, we were able to clarify the biokinetic coping mechanisms for the long term Cu accumulation. This study showed that water and food are both the major source of Cu for the muscle and liver of tilapia. This implied that control the Cu concentration in these two routes will be correlated to the Cu bioavailability for tilapia. We found that exposure duration and level of waterborne Cu drove the Cu accumulation in tilapia. The ability for Cu biouptake and depuration in organs of tilapia were actively mediated under prolonged exposure conditions. Generally, the uptake rate, depuration rate and net bioaccumulation ability in all selected organs decreased with the increasing level of waterborne Cu and extension of exposure duration.Muscle tissues accounted for over 50%of the total accumulated Cu and played a key role in buffering the Cu burden in the initial period of exposure, alternatively, the liver acted a more important role in the storage of Cu with the extension of exposures. We concluded that assumption of the constant biokinetic rates could lead to incorrect predictions with overestimating the long-term Cu accumulation in ecotoxicological risk assessments.

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References:
[1] C. R. Janssen, D. G. Heijerick, K. A. C. De Schamphelaere, H. E. Allen,
Environmental risk assessment of metals: tools for incorporating
bioavailability. Environ Int 28:793-800. 2003.
[2] B. I. Escher, J. L. M. Hermens, Internal exposure: linking bioavailability
to effects. Environ Sci Technol 38:455A-462A. 2004.
[3] J.W. Tsai,W. Y. Chen, Y. R. Ju, C. M. Liao, Bioavailability links mode
of action can improve the long-term field risk assessment for tilapia
exposed to arsenic. Environ Int 35:727-736. 2009.
[4] M. H. Grosell, C. Hogstrand, C. M. Wood, Cu uptake and turnover in
both Cu acclimated and non-acclimated rainbow trout (Oncorhynchus
mykiss). Aquat Toxicol 38:257-276. (1997)
[5] P. S. Rainbow, Trace metal concentrations in aquatic invertebrates: why
or so what? Environ Pollut 120:497-507. 2002.
[6] D. J. Cain, S. N. Luoma, W. G. Wallace, Linking metal bioaccumulation
of aquatic insects to their distribution patterns in a mining-impacted river.
Environ Toxicol Chem 23:1463-1473. 2004.
[7] W. W. Green, R. S. Mirza,C. M. Wood, G. G. Pyle, Copper binding
dynamics and olfactory impairment in fathead minnows (Pimephale
promelas). Environ Sci Technol 44:1431-1437. (2010)
[8] J. C. McGeer, K. V. Brix, J .M. Skeaff, D. K. DeForest, S. I. Brigham, W.
J. Adams, A. Green, Inverse relationship between bioconcentration factor
and exposure concentration for metals: implications for hazard
assessment of metals in the aquatic environment. Environ Toxicol Chem
22:1017-1037. 2003.
[9] C. M. Liao, B. C. Chen, S. Singh, M. C. Lin, C. W. Liu, B. C. Han,
Acute toxicity and bioaccumulation of arsenic in tilapia (Oreochromis
mossambicus) from a blackfoot disease area in Taiwan. Environ Toxicol
18:252-259. 2003.
[10] C. M. Wood, M. Grosell, M. D. McDonald, R. C. Playle, P. J. Walsh,
Effects of waterborne silver in a marine teleost, the gulf toadfish
(Opsanus beta): Effects of feeding and chronic exposure on
bioaccumulation and physiological responses. Aquat Toxicol 99:138-148.
2010.
[11] C. Kamunde, M. Grosell, D. Higgs, C. M. Wood, Copper, metabolism
in actively growing rainbow trout (Oncorhynchus mykiss) interactions
between dietary and waterborne copper uptake. J Exp Biol 205:279-290.
2002.
[12] M. Grosell, I. Boetius, H. J. M. Hansen, P. Rosenkilde, Influence of
preexposure to sublethal levels of copper on 64Cu uptake and distribution
among tissues of the European eel (Anguilla anguilla). Comp Biochem
Physiol C 114:229-235. 1996.
[13] F. Dang, H. Zhong, W. X. Wang, Copper uptake kinetics and regulation
in a marine fish after waterborne copper Acclimation. Aquat Toxicol
94:238-244. 2009.
[14] L. D. Kraemer, P. G. C. Campbell, L . Hare, A field study examining
metal elimination kinetics in juvenile yellow perch (Perca flavescens).
Aquat Toxicol 75:108-126. 2005.
[15] J. C. McGeer, S. Nadella, D. H. Alsop, L. Hollis, L. N. Taylor, D. G.
McDonald, C.M. Wood , Influence of acclimation and cross-acclimation
of metals on acute Cd toxicity and Cd uptake and distribution in rainbow
trout (Oncorhynchus mykiss). Aquat Toxicol 84(2):190-197. 2007.
[16] A. Suhendrayatna Ohki, T. Nakajima, S. Maeda, Studies on the
accumulation and transformation of arsenic in fresh organisms II.
Accumulation and transformation of arsenic compounds by Tilapia
mossambica. Chemosphere 46:325-331. 2002.
[17] C. M. Liao, J. W. Tsai, M. P. Ling, H. M. Liang, Y. H. Chou, P. T.
Yang, Organ-specific toxicokinetics and dose-response of arsenic in
tilapia Oreochromis mossambicus. Arch Environ Contam Toxicol
47:502-510. 2004.
[18] S. M. Wu, H. R. Ding, L. Y. Lin, Y. S. Lin, Juvenile tilapia
(Oreochromis mossambicus) strive to maintain physiological functions
after waterborne copper exposure. Arch Environ Contam Toxicol
54(3):482-492. 2008.
[19] Y. Iger, R. A. C. Lock, J. C. A. van der Meij, S. E. Wendelaar Bonga,
Effects of water-borne cadmium on the skin of the common carp
(Cyprinus carpio). Arch Environ Contam Toxicol 26:342-350. 1994.
[20] S.M. Wu, K. J. Jong, S. Y. Kuo, Effects of copper sulfate on ion balance
and growth in tilapia larvae (Oreochromis mossambicus). Arch Environ
Contam Toxicol 45(3):357-363. 2003.
[21] Environmental Protection Administration ROC (Taiwan).
http://ivy5.epa.gov.tw/epalaw/index.aspx. 2001.
[22] S. N. Luoma, P. S. Rainbow, Why is metal bioaccumulation so variable?
Biodynamics as a unifying concept. Environ Sci Technol 39:1921-1931.
2005.
[23] J. W. Tsai, C. M. Liao, V. H. C. Liao, A biologically based damage
assessment model to enhance aquacultural water quality management.
Aquaculture 251(2-4):280-294. (2006)
[24] L. D. Kraemer, P. G. C. Campbell, L. Hare, Modeling cadmium
accumulation in indigenous yellow perch (Perca flavescens). Can J Fish
Aquat Sci 65:1623-1634. 2008.
[25] F. Dang, W. X. Wang, Subcellular controls of mercury trophic transfer to
a marine fish. Aquat Toxicol 99:500-506. 2010.
[26] L. D. Kraemer, P. G. C. Campbell, L. Hare, J. C. Auclair, A field study
examining the relative importance of food and water as sources of
cadmium for juvenile yellow perch (Perca flavescens). Can J Fish Aquat
Sci 63(3):549-557. 2006.
[27] J. R. Erickson, D. R. Mount, T. L. Highland, J. R. Hockett, E. N. Leonard,
V. R. Mattson, T. D. Dawson, K. G. Lott, Effects of copper, cadmium,
lead, and arsenic in a live diet on juvenile fish growth. Can J Fish Aquat
Sci 67(11):1816-1826. 2010.
[28] W. G. Wallace, G. R. Lopez, Relationship between subcellular cadmium
distribution in prey and cadmium trophic transfer to a predator. Estuar
Coast 19:923-930. 1996.
[29] W. G. Wallace, G. R. Lopez, J. S. Levinton, Cadmium resistance in an
oligochaete and its effect on cadmium trophic transfer to an omnivorous
shrimp. Mar Ecol Prog Ser 172:225-237. 1998.
[30] M. C. Newman,M. A. Unger, Fundamentals of Ecotoxicology, second ed.
Lewis Publishers, CRC Press, Boca Raton, FL. 2003
[31] S. Copper, L. Hare, P. G. C. Campbell, Modeling cadmium uptake from
water and food by the freshwater bivalve Pyganodon grandis. Can J Fish
Aquat Sci 67(11):1874-1888. 2010.
[32] P. Carriquiriborde, A. E. Ronco, Distinctive accumulation patterns of
Cd(II), Cu(II), and Cr(VI) in tissue of the South American teleost, pejerrey
(Odontesthes bonariensis). Aquat Toxicol 86:313-322. (2008)
[33] J. C. McGeer, C. Szebedinszky, D. G. McDonald, C. M. Wood, Effects
of chronic sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout
2: tissue specific metal accumulation. Aquat Toxicol 50:245-256. 2000.
[34] L. D. Kraemer, P. G. C. Campbell, L. Hare, Dynamics of Cd, Cu and Zn
accumulation in organs and sub-cellular fractions in field transplanted
juvenile yellow perch (Perca flavescens). Environ Pollut 138:324-337.
2005.
[35] S. Subathra, R. Karuppasamy, Bioaccumulation and depuration pattern
of copper in different tissues of Mystus vittatus, related to various size
groups. Arch Environ Contam Toxicol 54:236-244. 2008.
[36] P. Couture, J. W. Rajotte, Morphometric and metabolic indicators of
metal stress in wild yellow perch (Perca flaveseens) from Sudbury,
Ontario: A review. J Environ Monitor 5:216-221. 2003.
[37] S. M. G. J. Pelgrom, R. A. C. Lock, P. H. M. Balm, S. E. Wendelaar
Bonga, Integrated physiological response of tilapia, Oreochromis
mossambicus, to sublethal copper exposure. Aquat Toxicol 32:303-320.
1995.
[38] C. Hogstrand,M. Grosell, C.M.Wood, H. Hansen, Internal redistribution
of radi olabelled silver among tissues of rainbow trout (Oncorhynchus
mykiss) and European eel (Anguilla anguilla): the influence of silver
speciation. Aquat Toxicol 63:139-157. 2003.
[39] P. F. Landrum, Bioavailability and toxicokinetics of polycyclic aromatic
hydrocarbons sorbed to sediments for the amphipod Pontoporeia hoyi.
Environ Sci Technol 23:588-595. 1989.
[40] C. P. Higgins , Z. J. Paesani , T. E. Chalew , R. U. Halden,
Bioaccumulation of triclocarban in Lumbriculus variegatus. Environ
Toxicol Chem 28:2580-2586. 2009.
[41] G. De Boeck, M. Eyckmans, I. Lardon, R. Bobbaers, A. K. Sinha, R.
Blust, Metal accumulation and metallothionein induction in the spotted
dogfish Scyliorhinus canicula. Comp Biochem Physiol A 155:503-508.
2010.