Development and Validation of a Biodynamic Model for Mechanistically Predicting Metal Accumulation in Fish-Parasite Systems

Because of different reported effects of parasitism on the accumulation of metals in fish, it is important to consider parasites while interpreting bioaccumulation data from biomonitoring programmes. Accordingly, the first step is to take parasitism into consideration when simulating metal bioaccumulation in the fish host under laboratory conditions. In the present study, the accumulation of metals in fish-parasite systems was simulated by a one-compartment toxicokinetic model and compared to uninfected conspecifics. As such, metal accumulation in fish was assumed to result from a balance of different uptake and loss processes depending on the infection status. The uptake by parasites was considered an efflux from the fish host, similar to elimination. Physiological rate constants for the uninfected fish were parameterised based on the covalent index and the species weight while the parameterisation for the infected fish was carried out based on the reported effects of parasites on the uptake kinetics of the fish host. The model was then validated for the system of the chub Squalius cephalus and the acanthocephalan Pomphorhynchus tereticollis following 36-day exposure to waterborne Pb. The dissolved concentration of Pb in the exposure tank water fluctuated during the exposure, ranging from 40 to 120 μg/L. Generally, the present study shows that the one-compartment model can be an effective method for simulating the accumulation of metals in fish, taking into account effects of parasitism. In particular, the predicted concentrations of Cu, Fe, Zn, and Pb in the uninfected chub as well as in the infected chub and the acanthocephalans were within one order of magnitude of the measurements. The variation in the absorption efficiency and the elimination rate constant of the uninfected chub resulted in variations of about one order of magnitude in the predicted concentrations of Pb. Inclusion of further assumptions for simulating metal accumulation in the infected chub led to variations of around two orders of magnitude in the predictions. Therefore, further research is required to reduce uncertainty while characterising and parameterising the model for infected fish.

[1]  A. Hendriks,et al.  The power of size. 1. Rate constants and equilibrium ratios for accumulation of organic substances related to octanol‐water partition ratio and species weight , 2001, Environmental toxicology and chemistry.

[2]  M. Javed,et al.  Assessment of heavy metal (Cu, Ni, Fe, Co, Mn, Cr, Zn) pollution in effluent dominated rivulet water and their effect on glycogen metabolism and histology of Mastacembelus armatus , 2013, SpringerPlus.

[3]  A. Economou,et al.  Growth and morphological development of chub, Leuciscus cephalus (L.), during the first year of life , 1991 .

[4]  Heavy metal concentrations in adult acanthocephalans and cestodes compared to their fish hosts and to established free-living bioindicators. , 1997, Parassitologia.

[5]  J. Beauchamp,et al.  Estimation of Whole-Fish Containment Concentrations from Fish Fillet Data , 1997 .

[6]  C. Cowan-Ellsberry,et al.  Toward improved models for predicting bioconcentration of well‐metabolized compounds by rainbow trout using measured rates of in vitro intrinsic clearance , 2013, Environmental toxicology and chemistry.

[7]  Jordi Torres,et al.  Perch and Its Parasites as Heavy Metal Biomonitors in a Freshwater Environment: The Case Study of the Ružín Water Reservoir, Slovakia , 2012, Sensors.

[8]  F. Şen,et al.  Biological Properties of Chub (Leuciscus cephalus L., 1758) in Karasu Stream (Mus/Turkey) , 2008 .

[9]  M. da Luz Mathias,et al.  Response of antioxidant enzymes in freshwater fish populations (Leuciscus alburnoides complex) to inorganic pollutants exposure. , 2001, The Science of the total environment.

[10]  Aroha A. Miller,et al.  Distribution of cadmium, mercury, and lead in different body parts of Baltic herring (Clupea harengus) and perch (Perca fluviatilis): implications for environmental status assessments. , 2014, Marine pollution bulletin.

[11]  Lawrence P Burkhard,et al.  In vitro‐in vivo extrapolation of quantitative hepatic biotransformation data for fish. II. Modeled effects on chemical bioaccumulation , 2007, Environmental toxicology and chemistry.

[12]  J. Twining,et al.  Bioaccumulation from food and water of cadmium, selenium and zinc in an estuarine fish, Ambassis jacksoniensis. , 2010, Marine pollution bulletin.

[13]  Muhittin Yılmaz,et al.  Some Biological Properties of the Leuciscus cephalus (L., 1758) Population Living in Karakaya Dam Lake in Malatya (Turkey) , 2005 .

[14]  Wen-Xiong Wang,et al.  Exposure and potential food chain transfer factor of Cd, Se and Zn in marine fish Lutjanus argentimaculatus , 2002 .

[15]  B. Sures,et al.  Comparison between lead accumulation of Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) and in the body cavity of goldfish (Carassius auratus auratus). , 2001, International journal for parasitology.

[16]  C. Joiris,et al.  Mercury accumulation and speciation in marine fish from Bangladesh , 2000 .

[17]  Petr Válek,et al.  Concentrations of Zn, Mn, Cu and Cd in different tissues of perch (Perca fluviatilis) and in perch intestinal parasite (Acanthocephalus lucii) from the stream near Prague (Czech Republic). , 2012, Environmental research.

[18]  M. Coquery,et al.  Environmental relevance of laboratory-derived kinetic models to predict trace metal bioaccumulation in gammarids: Field experimentation at a large spatial scale (France). , 2016, Water research.

[19]  N. Fisher,et al.  Intraspecific comparisons of metal bioaccumulation in the juvenile Atlantic silverside Menidia menidia , 2010 .

[20]  Mark A J Huijbregts,et al.  Integration of biotic ligand models (BLM) and bioaccumulation kinetics into a mechanistic framework for metal uptake in aquatic organisms. , 2010, Environmental science & technology.

[21]  B. Sures Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective , 2003, Parasitology.

[22]  R. Peters,et al.  The biological half-time of radioactive Cs in poikilothermic and homeothermic animals. , 1989, Health physics.

[23]  Anders Wicklund,et al.  Calcium effects on cadmium uptake, redistribution, and elimination in minnows, Phoxinus phoxinus, acclimated to different calcium concentrations , 1988 .

[24]  Relative concentrations of heavy metals in the parasites Ascaris suum (Nematoda) and Fasciola hepatica (Digenea) and their respective porcine and bovine definitive hosts. , 1998, International journal for parasitology.

[25]  Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis). , 2002, International journal for parasitology.

[26]  P. Römkens,et al.  Modelling metal accumulation using humic acid as a surrogate for plant roots. , 2015, Chemosphere.

[27]  J. Garnier-Laplace,et al.  A dynamic model for radionuclide transfer from water to freshwater fish , 1997 .

[28]  M. K. Sangun,et al.  Element concentrations in the swimbladder parasite Anguillicola crassus (nematoda) and its host the European eel, Anguilla anguilla from Asi River (Hatay-Turkey) , 2008, Environmental monitoring and assessment.

[29]  D. Holdway,et al.  The effects of pulse‐exposed cadmium and zinc on embryo hatchability, larval development, and survival of Australian crimson spotted rainbow fish (Melanotaenia fluviatilis) , 2000 .

[30]  M. Wong,et al.  Mercury exposure in the freshwater tilapia Oreochromis niloticus. , 2010, Environmental pollution.

[31]  S. Woelfl,et al.  Trace metal concentrations in single specimens of the intestinal broad flatworm (Diphyllobothrium latum), compared to their fish host (Oncorhynchus mykiss) measured by total reflection X-ray fluorescence spectrometry , 2008 .

[32]  Studies on the Age, Growth and Reproduction Characteristics of the Chub, Leuciscus cephalus orientalis, (Nordmann, 1840) in Karasu River, Turkey , 2002 .

[33]  M. Fernandes,et al.  Toxicity and Differential Tissue Accumulation of Copper in the Tropical Freshwater Fish, Prochilodus scrofa (Prochilodontidae) , 1999, Bulletin of environmental contamination and toxicology.

[34]  D. Knapen,et al.  Differential Hepatic Metal and Metallothionein Levels in Three Feral Fish Species along a Metal Pollution Gradient , 2013, PloS one.

[35]  J. Garnier-Laplace,et al.  Experimental Kinetic Rates of Food-Chain and Waterborne Radionuclide Transfer to Freshwater Fish: A Basis for the Construction of Fish Contamination Charts , 2000, Archives of environmental contamination and toxicology.

[36]  A. Fritsch,et al.  Relative contributions of food and water in the accumulation of 60Co by a freshwater fish , 1989 .

[37]  E. Johnston,et al.  Relationships between body burdens of trace metals (As, Cu, Fe, Hg, Mn, Se, and Zn) and the relative body size of small tooth flounder (Pseudorhombus jenynsii). , 2012, The Science of the total environment.

[38]  M. Kraak,et al.  Dynamics of metal uptake and depuration in a parasitized cyprinid fish (Rastrineobola argentea). , 2012, Aquatic toxicology.

[39]  S. Sabater,et al.  Trace metal concentration and fish size: variation among fish species in a Mediterranean river. , 2014, Ecotoxicology and environmental safety.

[40]  J. Klaverkamp,et al.  Uptake, elimination and tissue distribution of dietary and aqueous cadmium by rainbow trout (salmo gairdneri richardson) and lake whitefish (coregonus clupeaformis mitchill) , 1989 .

[41]  M. Çalta Morphological development and growth of chub, Leuciscus cephalus (L.), larvae , 2000 .

[42]  E. Billoir,et al.  A biodynamic model predicting waterborne lead bioaccumulation in Gammarus pulex: Influence of water chemistry and in situ validation. , 2015, Environmental pollution.

[43]  Michael C. Newman,et al.  Size dependence of zinc elimination and uptake from water by mosquitofish Gambusia affinis (Baird and Girard) , 1988 .

[44]  E. Balsa-Canto,et al.  Generic parameterization for a pharmacokinetic model to predict Cd concentrations in several tissues of different fish species. , 2010, Chemosphere.

[45]  J. R. Grigera,et al.  Kinetics of bioaccumulation of heavy metals in Odontesthes bonariensis is explained by a single and common mechanism , 2014 .

[46]  Eva Balsa-Canto,et al.  Dynamic multi-compartmental modelling of metal bioaccumulation in fish: Identifiability implications , 2010, Environ. Model. Softw..

[47]  Bernd Sures,et al.  Concentrations of 17 elements in the zebra mussel (Dreissena polymorpha), in different tissues of perch (Perca fluviatilis), and in perch intestinal parasites (Acanthocephalus lucii) from the subalpine lake Mondsee, Austria , 1999 .

[48]  B. Raspor,et al.  Effect of acanthocephalan infection on metal, total protein and metallothionein concentrations in European chub from a Sava River section with low metal contamination. , 2013, The Science of the total environment.

[49]  Absorption of Radiostrontium by the Gills of Freshwater Fish , 1962, Nature.

[50]  R. Leuven,et al.  Modeling metal bioaccumulation in the invasive mussels Dreissena polymorpha and Dreissena rostriformis bugensis in the rivers Rhine and Meuse , 2011, Environmental toxicology and chemistry.

[51]  B. Sures,et al.  Analysis of trace metals in the Antarctic host-parasite system Notothenia coriiceps and Aspersentis megarhynchus (Acanthocephala) caught at King George Island, South Shetland Islands , 2003, Polar Biology.

[52]  Peter G. C. Campbell,et al.  Influence of lake chemistry and fish age on cadmium, copper, and zinc concentrations in various organs of indigenous yellow perch (Perca flavescens) , 2004 .

[53]  Wen-Xiong Wang,et al.  Comparative approaches to understand metal bioaccumulation in aquatic animals. , 2008, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[54]  R. Addison,et al.  The effect of temperature on the rate of conversion of p,p-DDT to p,p-DDE in brook trout (Salvelinus fontinalis). , 1975, Canadian journal of biochemistry.

[55]  Variability in the growth rate of chub Leuciscus cephalus along a longitudinal river gradient. , 2009, Journal of fish biology.

[56]  E. Uzunova,et al.  AGE AND GROWTH OF THE CHUB, LEUCISCUS CEPHALUS L. FROM THE MARITZA RIVER (SOUTH BULGARIA) , 2008 .

[57]  S. A. Peterson,et al.  Mercury concentration in fish from streams and rivers throughout the western United States. , 2007, Environmental science & technology.

[58]  Mark A J Huijbregts,et al.  Metal bioaccumulation in aquatic species: quantification of uptake and elimination rate constants using physicochemical properties of metals and physiological characteristics of species. , 2008, Environmental science & technology.

[59]  J. Rasmussen,et al.  Modeling the Elimination of Mercury by Fish , 1997 .

[60]  M. Karataş,et al.  Growth, Mortality and Yield of Chub (Leuciscus cephalus L., 1758) Population in Almus Dam Lake, Turkey , 2005 .

[61]  D. Wright,et al.  Effect of calcium on cadmium uptake and toxicity in larvae and juveniles of striped bass (Morone saxatilis) , 1985, Bulletin of environmental contamination and toxicology.

[62]  P. Couture,et al.  A comparison of metal concentrations in the tissues of yellow American eel (Anguilla rostrata) and European eel (Anguilla anguilla). , 2016, The Science of the total environment.

[63]  G. Jenkins An overview of bile-acid synthesis, chemistry and function , 2008 .

[64]  M. Andersen,et al.  A physiologically based toxicokinetic model for the uptake and disposition of waterborne organic chemicals in fish. , 1990, Toxicology and applied pharmacology.

[65]  U. Varanasi,et al.  Influence of water-borne and dietary calcium on uptake and retention of lead by coho salmon (Oncorhynchus kisutch). , 1978, Toxicology and applied pharmacology.

[66]  B. Sures Environmental parasitology: relevancy of parasites in monitoring environmental pollution. , 2004, Trends in parasitology.

[67]  M. Huijbregts,et al.  Estimating bioconcentration factors, lethal concentrations and critical body residues of metals in the mollusks Perna viridis and Mytilus edulis using ion characteristics , 2008, Environmental toxicology and chemistry.

[68]  J. Namieśnik,et al.  Bioaccumulation of Metals in Tissues of Marine Animals, Part I: the Role and Impact of Heavy Metals on Organisms , 2011 .

[69]  Fei Dang,et al.  Why mercury concentration increases with fish size? Biokinetic explanation. , 2012, Environmental pollution.

[70]  B. Jonsson,et al.  Effects of temperature and body size on radiocaesium retention in brown trout, Salmo trutta , 1992 .

[71]  Samuel N Luoma,et al.  Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. , 2005, Environmental science & technology.

[72]  J. Garnier-Laplace,et al.  Uptake from water, release and tissue distribution of 54Mn in the Rainbow trout (Oncorhynchus mikiss Walbaum). , 1997, Environmental pollution.

[73]  D. Pascoe,et al.  The effect of parasitism on the toxicity of cadmium to the three‐spined stickleback, Gasterosteus aculeatus L. , 1977 .

[74]  J. Reinfelder,et al.  Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach. , 1998, The Science of the total environment.

[75]  Olesya Hursky,et al.  Intestinal nematodes affect selenium bioaccumulation, oxidative stress biomarkers, and health parameters in juvenile rainbow trout (Oncorhynchus mykiss). , 2015, Environmental science & technology.

[76]  B. Sures,et al.  Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) as an indicator of metal pollution. , 2003, International journal for parasitology.

[77]  B. Sures,et al.  Fish macroparasites as indicators of heavy metal pollution in river sites in Austria , 2003, Parasitology.

[78]  Jon A Arnot,et al.  A food web bioaccumulation model for organic chemicals in aquatic ecosystems , 2004, Environmental toxicology and chemistry.

[79]  C. A. V. van Gestel,et al.  Toxicokinetics and toxicity of zinc under time‐varying exposure in the guppy (Poecilia reticulata) , 2001, Environmental toxicology and chemistry.

[80]  P. Hodson,et al.  Chronic toxicity of water-borne and dietary lead to rainbow trout (Salmo Gairdneri) in lake Ontario water , 1978 .

[81]  B. Sures,et al.  The intestinal parasite Pomphorhynchus laevis (Acanthocephala) from barbel as a bioindicator for metal pollution in the Danube River near Budapest, Hungary. , 2004, Environmental pollution.

[82]  B. Sures,et al.  Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). , 1999, Experimental parasitology.

[83]  S. Adhikari,et al.  Accumulation of Heavy Metals in Freshwater Fish-An Assessment of Toxic Interactions with Calcium , 2006 .

[84]  A. Hendriks,et al.  A QICAR approach for quantifying binding constants for metal-ligand complexes. , 2011, Ecotoxicology and environmental safety.

[85]  T. Mathews,et al.  Evaluating the trophic transfer of cadmium, polonium, and methylmercury in an estuarine food chain , 2008, Environmental toxicology and chemistry.

[86]  J. Lebrun,et al.  Waterborne nickel bioaccumulation in Gammarus pulex: comparison of mechanistic models and influence of water cationic composition. , 2011, Aquatic toxicology.

[87]  Wen-Xiong Wang Biodynamic understanding of mercury accumulation in marine and freshwater fish , 2012 .

[88]  The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (210Pb) in its fish host chub (Leuciscus cephalus). , 2003, International journal for parasitology.

[89]  B. Sures,et al.  Accumulation of persistent organic pollutants in parasites. , 2014, Chemosphere.

[90]  F. Beamish,et al.  Water Quality Modifies Uptake of Waterborne Methylmercury by Rainbow Trout, Salmo gairdneri , 1983 .

[91]  A. Savari,et al.  Detection of Acute Toxicity of Mercury Chloride in Yellowfin Sea Bream (Acanthopagrus Latus) , 2016 .

[92]  C. Liao,et al.  A dose‐based modeling approach for accumulation and toxicity of arsenic in tilapia Oreochromis mossambicus , 2006, Environmental toxicology.

[93]  M. Brown,et al.  A comparison of the accumulation, tissue distribution and secretion of cadmium in different species of freshwater fish , 1990 .

[94]  D. Krabbenhoft,et al.  Ecotoxicology of mercury , 2003 .

[95]  Mustafa Canli,et al.  The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. , 2003, Environmental pollution.

[96]  D. Marcogliese,et al.  Concentration-dependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata) , 2005, Parasitology.

[97]  B. Sures,et al.  Parasites as accumulation indicators of heavy metal pollution. , 1999, Parasitology today.

[98]  J. Rasmussen,et al.  The elimination of radiocaesium from fish , 1995 .

[99]  P. Moravec,et al.  Growth analysis of chub, Leuciscus cephalus (L.), and dace, Leuciscus leuciscus (L.), in the Úpoř stream using growth data of recaptured marked fish , 2018 .

[100]  Robert V. Thomann,et al.  A pharmacokinetic model of cadmium in rainbow trout , 1997 .

[101]  Comparative study of the metal accumulation in Hysterothalycium reliquens (nematode) and Paraphilometroides nemipteri (nematode) as compared with their doubly infected host, Nemipterus peronii (Notched threadfin bream) , 2014, Parasitology Research.

[102]  A. Mamcarz,et al.  Effect of variable and constant thermal conditions on embryonic and early larval development of fish from the genus Leuciscus (Cyprinidae, Teleostei) , 2018 .

[103]  M. C. Newman,et al.  Predicting the relative toxicity of metal ions using ion characteristics: Microtox® bioluminescence assay , 1996 .

[104]  M. Solé,et al.  The role of metallothionein and selenium in metal detoxification in the liver of deep-sea fish from the NW Mediterranean Sea. , 2014, The Science of the total environment.

[105]  Zinck Me,et al.  The Effect of Temperature on the Rate of Conversion of p,p′-DDT to p,p′-DDE in Brook Trout (Salvelinus fontinalis) , 1975 .

[106]  V. Paller,et al.  Acanthocephalan Parasites (Acanthogyrus sp.) of Nile Tilapia (Oreochromis niloticus) as Biosink of Lead (Pb) Contamination in a Philippine Freshwater Lake , 2016, Bulletin of Environmental Contamination and Toxicology.

[107]  P. Douben Metabolic rate and uptake and loss of cadmium from food by the fish Noemacheilus barbatulus L. (stone loach). , 1989, Environmental pollution.

[108]  B. Sures,et al.  Comparison of the metal accumulation capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus) , 2013, Parasites & Vectors.

[109]  K. Honda,et al.  Organ and Tissue Distribution of Heavy Metals, and Their Growth-related Changes in Antarctic Fish, Pagothenia borchgrevinki , 1983 .

[110]  W. Baeyens,et al.  Accumulation of trace metals in the muscle and liver tissues of five fish species from the Persian Gulf , 2009, Environmental monitoring and assessment.