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Environmental stochasticity promotes copper bioaccumulation and bioenergetic response in tilapia

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Abstract

Environmental change not only undergoes in mean environmental conditions but also in their degree of stochasticity. Changes in waterborne metal variability are often associated with altered disturbance regimes and temporal patterns of source availability. Here copper (Cu) was used as an example because Cu sulfate (CuSO4) has been extensively used as a chemical tool to exterminate phytoplankton for controlling skin lesions and gill disease of fish in aquatic ecosystems. This study showed that increased variability of waterborne Cu concentrations strongly promotes a key process of biokinetics, bioaccumulation. In experimental tilapia populations, the mean growth cost coefficient in pulsed Cu exposures was 7 % lower than the control group. On the other hand, the double-pulse, constant low, and single-pulse scenarios had similar effect on biomass change (2.2–2.4 %). The greatest biomass change (~10 %) occurred where Cu concentrations were gradually increasing over time or at a constant high rate. Most importantly, this study demonstrated that chronic exposure of tilapia to a low Cu concentration rate that approximated a single large pulse of field-realistic levels damaged bioenergetic mechanisms and increased energy acquisition. This study also showed that interactions across multiple pulsed or fluctuating Cu exposures were involved in accumulation changes that could also be achieved by controlling pulse timing and duration. It can be concluded that increased metal variability can promote biokinetic and bioenergetic responses in fish; and that changes in environmental variability may interact with other global change processes and thereby substantially accelerate change in aquatic ecosystems.

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References

  • Abdel-Tawwab M, Mousa MAA (2005) Effect of calcium pre-exposure on acute copper toxicity to juvenile Nile tilapia, Oreochromis niloticus (L.). Zagazig Vet J 33:80–87

    Google Scholar 

  • Allen VJ, Marsden ID, Ragg NLC, Gieseg S (2006) The effects of tactile stimulants on feeding, growth, behaviour, and meat quality of culaured Blackfoot abalone, Haliotis iris. Aquaculture 257:294–308

    Article  Google Scholar 

  • Alunno-Bruscia M, van der Veer HW, Kooijman SALM (2009) The AquaDEB project (phase I): analysing the physiological flexibility of aquatic species and connecting physiological diversity to ecological and evolutionary processes by using dynamic energy budgets. J Sea Res 62:43–48

    Article  Google Scholar 

  • Ashauer R, Boxall ABA, Brown CD (2007) New ecotoxicological model to simulate survival of aquatic invertebrates after exposure of fluctuating and sequential pulses of pesticides. Environ Sci Technol 41:1480–1486

    Article  CAS  Google Scholar 

  • Ashauer R, Hintermeister A, Caravatti I, Kretschmann A, Escher BI (2010) Toxicokinetic and toxicodynamic modeling explains carry-over toxicity from exposure to diazinon by slow organism recovery. Environ Sci Technol 44:3963–3971

    Article  CAS  Google Scholar 

  • Authman MMN, Abbas HHH (2007) Accunulation and distribution of copper and zinc in both water and some viral tissues of two fish species (Tilapia zillii and Mugil cephalus) of Lake Qarum, Fayoum province, Egypt. Pak J Biol Sci 10:2106–2122

  • Banerjee RK, Karmakar HC, Chatterjee SK, Saha SK (1990) Evaluation of nutrient loss from sewage-fed fish ponds. Environ Ecol 8:450–453

    Google Scholar 

  • Bearr JS, Diamond J, Latimer H, Bowersox M (2006) Effects of pulsed copper exposures on early life-stage Pimephales promelas. Environ Toxicol Chem 25:1376–1382

    Article  CAS  Google Scholar 

  • Boyd CE (2005) Copper treatments control phytoplankton. Global Aquac Advocate 8:69–70

    Google Scholar 

  • Chen YC, Chen CY, Hwang HJ, Chang WB, Yeh WJ, Chen MH (2004) Comparison of the metal concentrations in muscle and liver tissues of fishes from the Erren River, southwestern Taiwan, after restoration in 2000. J Food Drug Anal 12:358–366

    CAS  Google Scholar 

  • Chen WY, Lin CJ, Ju YR, Tsa JW, Liao CM (2012a) Assessing the effects of pulsed waterborne copper toxicity on tilapia populations. Sci Total Environ 417–418:129–137

    Article  Google Scholar 

  • Chen WY, Lin CJ, Ju YR, Tsai JW, Liao CM (2012b) Coupled dynamics of energy budget and population growth of tilapia in response to pulsed waterborne copper toxicity. Ecotoxicol 21:2264–2275

    Article  CAS  Google Scholar 

  • De Boeck G, Hattink J, Franklin NM, Bucking CP, Wood S, Walsh PJ, Wood CM (2007) Copper toxicity in the spiny dogfish (Squalus acanthias): urea loss contributes to the osmoregulatory disturbance. Aquat Toxicol 84:133–141

    Article  Google Scholar 

  • Diamond JM, Bowersox M, Latimer H, Barbour C, Bearr J, Butcher J (2005) Effect of pulsed contaminant exposure on early life stage of the fathead minnow. Arch Environ Contam Toxicol 49:511–519

    Article  CAS  Google Scholar 

  • Diamond JM, Klaine SJ, Butcer JB (2006) Implications of pulsed chemical exposures for aquatic life criteria and wastewater permit limits. Environ Sci Technol 40:5132–5138

    Article  CAS  Google Scholar 

  • Fulton TW (1904) The rate of growth of fishes. 22nd Annual Report of the Fishery Board of Scotland 1904(3):141–241

  • Gammons CH, Grant TM, Nimick DA, Paker SR, DeGrandpre MD (2007) Diel changes in water chemistry in an arsenic-rich stream and treatment-pond system. Sci Total Environ 384:433–451

    Article  CAS  Google Scholar 

  • Gao H, Bai J, Xiao R, Liu P, Jiang W, Wang J (2013) Levels, sources and risk assessment of trace elements in wetland soils of a typical shallow freshwater lake, China. Stoch Environ Res Risk Assess 27:275–284

    Article  Google Scholar 

  • Grosell M, Wood CM (2002) Copper uptake across rainbow trout gills: mechanisms of apical entry. J Exp Biol 205:1179–1188

    CAS  Google Scholar 

  • Heier LS, Meland S, Ljønes M, Salbu B, Strømseng AE (2010) Short-term temporal variations in speciation of Pb, Cu, Zn and Sb in a shooting range runoff stream. Sci Total Environ 408:2409–2417

  • Hoang TC, Pryor R, Rand GM, Grakes RA (2011) Bioaccumulation and toxicity of copper in the outdoor freshwater microcosms. Ecotoxcol Environ Safe 74:1011–1020

    Article  CAS  Google Scholar 

  • Huang TC, Meng PJ, Han BC, Chuang A, Huang CC (2001) Trace metals in different species of mollusca, water and sediments form Taiwan coastal area. Chemosphere 44:833–841

    Article  Google Scholar 

  • Jang CS, Liang CP, Wang SW (2013) Integrating the spatial variability of water quality and quantity to probabilistically assess groundwater sustainability for use in aquaculture. Stoch Environ Res Risk Assess 27:1281–1291

    Article  Google Scholar 

  • Kooijman SALM, Bedaux JJM (1996) The analysis of aquatic toxicity data. VU University Press, Amsterdam

    Google Scholar 

  • Lin TS, Lin CS, Chang CL (2005) Trace elements in cultured tilapia (Oreochromis moddambicus): results form a farm in southern Taiwan. Bull Environ Contam Toxicol 74:308–313

    Article  CAS  Google Scholar 

  • Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environ Sci Tech 39:1921–1931

    Article  CAS  Google Scholar 

  • McCarty LS, Mackay D (1993) Enhancing ecotoxicological modeling and assessment. Environ Sci Technol 9:1719–1728

    Google Scholar 

  • Miao L, Hong JM, Lin B (2011) Effect on water quality and fishes of copper sulfate complex applied as algaecide for emergency control of algae bloom. J Ecol Rural Environ 27:63–66

    CAS  Google Scholar 

  • Mischke CC, Wise DJ (2009) Impact of copper sulfate on plankton in channel catfish nursery ponds. J World Aquac Soc 40:122–128

    Article  Google Scholar 

  • Nimick DA, Harper DD, Farag AM, Cleasby TE (2007) Influence of in-stream diel concentration cycles of dissolved trace metals on acute toxicity to one-year old cutthroat trout (Oncorhynchus Clarki Lewisi). Environ Toxicol Chem 26:2667–2678

    Article  CAS  Google Scholar 

  • Niyogi S, Wood CM (2004) Biotic ligand model, a flexible tool for developing site-specific water quality guidelines for metals. Environ Sci Technol 38:6177–6192

    Article  CAS  Google Scholar 

  • Parker SR, Gammons CH, Poulson SR, DeGrandpre MD (2007) Diel variations in stream chemistry and isotopic composition of dissolved inorganic carbon, upper Clark Fork River, Montana, USA. Appl Geochem 22:1329–1343

  • Patterson JW, Miner RA, Gasca E, Petropoulou C (1998) Industrial discharges of metals to water. In: Allen HE, Garrison AW, Luther GW (eds) Metals in surface waters. Ann Arbor Press, MI, pp 37–66

    Google Scholar 

  • Pereira P, de Pablo H, Vale C, Rosa-Santos F, Cesário R (2009) Metal and nutrient dynamics in a eutrophic coastal lagoon (Óbidos, Portugal): the importance of observations at different time scales. Environ Monit Assess 158:405–418

  • Pereira P, de Pablo H, Pacheco M, Vale C (2010) The relevance of temporal and organ specific factors on metals accumulation and biochemical effects in feral fish (Liza aurata) under a moderate contamination scenario. Ecotox Environ Safe 73:805–816

  • Pery ARR, Ducrot V, Mons R, Garric J (2003) Modelling toxicityand mode of action of chemicals to analyse growth and emergence tests with the midge Chironomus riparius. Aquat Toxicol 65:281–292

    Article  CAS  Google Scholar 

  • Ramskov T, Forbes VE (2008) Life history and population dynamics of the opportunistic polychaete Capitella sp. I in relation to sediment organic matter. Mar Ecol Prog Ser 369:181–192

    Article  Google Scholar 

  • Reinert KH, Giddings JA, Judd L (2002) Effects analysis of time-varying or repeated exposure in aquatic ecological risk assessment of agrochemicals. Environ Toxicol Chem 21:1977–1992

    Article  CAS  Google Scholar 

  • Sullivan CA (2011) Quantifying water vulnerability: a multi-dimensional approach. Stoch Environ Res Risk Assess 25:627–640

    Article  Google Scholar 

  • Tercier-waeber ML, Hezard T, Masson M, Schäfer J (2009) In situ monitoring of the diurnal cycling of dynamic metal species in a stream under contrasting photobenthic biofilm activity and hydrological conditions. Environ Sci Technol 43:7237–7244

  • Tsai JW, Liao CM (2006) Mode of action and growth toxicity of arsenic to tilapia Oreochromis mossambicus can be determined bioenergetically. Arch Environ Contam Toxicol 50:144–152

    Article  CAS  Google Scholar 

  • USEPA (2007) Aquatic life ambient freshwater quality criteria—copper. EPA-882-R-07-001. 2007 revision. US Environmental Protection Agency, Washington, DC

  • van Aardt WJ, Hough M (2006) Acute effect of Cu on oxygen consumption and 96hr-LC50 values in the freshwater fish Tilapia sparrmani (Teleostel: Cichlidae) in Mooi River hard water, South Africa. Afr J Aquat Sci 31:305–311

    Article  Google Scholar 

  • West GB, Brown JH, Enquist BJ (2001) A general model for ontogenetic growth. Nature 413:628–631

    Article  CAS  Google Scholar 

  • Wise DJ, Mischke CC, Greenway T, Byars TS (2006) Uniform application of copper sulfate as a potential treatment for controlling snail populations in channel catfish production ponds. N Am J Aquac 68:364–368

    Article  Google Scholar 

  • Wu SM, Jong KJ, Kuo SY (2003) Effects of copper sulfate on ion balance and growth in tilapia larvae (Oreochromis mossambicus). Arch Environ Contam Toxicol 45:357–363

    CAS  Google Scholar 

  • Zhao Y, Newman MC (2006) Effect of exposure duration and recovery time during pulsed exposures. Environ Toxicol Chem 25:1298–1304

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the financial support of the National Science Council of Republic of China under Grant NSC 98-2628-B-002-090-MY3.

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Correspondence to Wei-Yu Chen.

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Chen, WY., Ju, YR., Lin, CJ. et al. Environmental stochasticity promotes copper bioaccumulation and bioenergetic response in tilapia. Stoch Environ Res Risk Assess 29, 1545–1555 (2015). https://doi.org/10.1007/s00477-014-0993-1

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  • DOI: https://doi.org/10.1007/s00477-014-0993-1

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