Elsevier

Science of The Total Environment

Volume 496, 15 October 2014, Pages 11-21
Science of The Total Environment

Relating metal exposure and chemical speciation to trace metal accumulation in aquatic insects under natural field conditions

https://doi.org/10.1016/j.scitotenv.2014.07.023Get rights and content

Highlights

  • Strong relations were observed between body burdens and free metal ion activities.

  • The effect of H+ ions on insect body burdens was most clearly revealed.

  • Effects of major hardness ions on metal accumulation were rather limited.

  • Insect body burdens in natural waters can be predicted using speciation modelling.

Abstract

The present study investigated to what extent measured dissolved metal concentrations, WHAM-predicted free metal ion activity and modulating water chemistry factors can predict Ni, Cu, Zn, Cd and Pb accumulation in various aquatic insects under natural field conditions. Total dissolved concentrations and accumulated metal levels in four taxa (Leuctra sp., Simuliidae, Rhithrogena sp. and Perlodidae) were determined and free metal ion activities were calculated in 36 headwater streams located in the north-west part of England. Observed invertebrate body burdens were strongly related to free metal ion activities and competition among cations for uptake in the biota. Taking into account competitive effects generally provided better fits than considering uptake as a function of total dissolved metal levels or the free ion alone. Due to the critical importance and large range in pH (4.09 to 8.33), the H+ ion activity was the most dominant factor influencing metal accumulation. Adding the influence of Na+ on Cu2+ accumulation improved the model goodness of fit for both Rhithrogena sp. and Perlodidae. Effects of hardness ions on metal accumulation were limited, indicating the minor influence of Ca2+ and Mg2+ on metal accumulation in soft-water streams (0.01 to 0.94 mM Ca; 0.02 to 0.39 mM Mg). DOC levels (ranging from 0.6 to 8.9 mg L 1) significantly affected Cu body burdens, however not the accumulation of the other metals.

Our results suggest that 1) uptake and accumulation of free metal ions are most dominantly influenced by competition of free H+ ions in low-hardness headwaters and 2) invertebrate body burdens in natural waters can be predicted based on the free metal ion activity using speciation modelling and effects of H+ competition.

Introduction

Metal bioavailability and toxicity from water-borne exposure generally depend on the activity of the free metal ion, which is controlled by chemical speciation processes (binding to dissolved organic carbon (DOC), inorganic ligands (e.g. Cl, OH, CO32−) and the effect of pH), and are largely influenced by other cations (e.g. Na+, Ca2+, Mg2+) and H+ ions competing with trace metals for uptake at particular biological uptake sites (e.g. ion-channels and other transporters in the gills of aquatic organisms) (Hare and Tessier, 1996, Hare and Tessier, 1998, Bervoets and Blust, 2000). The latter concepts are integrated in the Free Ion Activity Model (FIAM), which states that the activity of the free metal ion is a good predictor of both metal availability and toxicity to aquatic organisms (Campbell, 1995), and has been used as the main rationale for the construction of the Biotic Ligand Model (BLM) in order to predict water-borne metal toxicity (Paquin et al., 2002, Niyogi and Wood, 2004).

Over the last decades efforts have been made to determine and predict trace metal speciation in natural waters. This has led to the construction of chemical speciation models such as the Windermere Humic Aqueous Model (WHAM), which enables calculation of the free metal ion concentration and activity in solution, based on water chemistry measurements and equilibrium binding interactions (e.g. pH, temperature, Ca2+, Mg2+, DOC) (Tipping, 1994, Tipping, 1998, Tipping et al., 1998). Although WHAM is currently incorporated in the BLM (Paquin et al., 2002, Niyogi and Wood, 2004), the speciation model has been rarely used to predict metal accumulation in aquatic insects under natural conditions (but see Hare and Tessier, 1996, Hare and Tessier, 1998, Croteau et al., 1998, Ponton and Hare, 2009, Stockdale et al., 2010). Since water chemistry and exposure scenarios can largely vary compared to conditions in the laboratory, relations between metal exposure, chemical speciation and invertebrate body burdens taking into account the influence of major ions and other metals at biological uptake sites should be assessed directly in the field. Recently, studies of Stockdale et al. (2010) and Tipping and Lofts (2013) were able to model metal levels in field-collected aquatic invertebrates using WHAM, considering organisms as humic acids, which corresponded well with measured body burdens. Since accumulated metal levels represent a time-integrated and ecologically-relevant measure of metal exposure and bioavailability, body burdens have gained increasing attention in biomonitoring studies during recent years (Hare and Tessier, 1996, Adams et al., 2011, De Jonge et al., 2013).

The aim of the current study was first to evaluate influences of chemical speciation and water chemistry (pH, DOC and major cation effects) on insect body burdens under natural field conditions, and secondly to evaluate whether WHAM-predicted free metal ion activity and other modulation factors could accurately predict the observed body burdens.

Section snippets

Study area and sampling design

In total 36 headwater streams of the Lake District, Ribbledale, Swaledale and the Howgill Fells, which are all located in the north-west part of England, were sampled as part of an extended field survey (Bass et al., 2008). Some of these sites have been severely metal contaminated from discharge of nearby abandoned mining sites. Samples for the determination of water chemistry were taken on four occasions (March 6–8, March 20–22, April 3–5 and April 17–19, 2006). Separate samples were taken for

Effect of water chemistry on Ni body burdens

Total dissolved Ni concentrations ranged from 0.002 to 1.29 μM (Table 1). WHAM-predicted free Ni ion activities were significantly positively correlated with {H+}, {K+}, {Mg2+} and all other trace metal ions (Table 2). No significant correlation was observed between {Ni2+} and both {Na+} and {Ca2+}. Nickel body burdens ranged from 0.003 (Perlodidae) to 0.68 μmol g 1 dw (Leuctra sp.) (Table 3). Ni body burdens in Leuctra sp., Simuliidae, Rhithrogena sp. and Perlodidae were generally poorly

Conclusions

Strong relations were observed between insect body burdens and WHAM-calculated free metal ion activities and the competing ions for uptake, which generally provided superior fits compared to metal accumulation as a function of total dissolved metal levels or the free ion alone. Due to the large range in pH observed in the waters of the present study, the effect of H+ ions on insect body burdens was most clearly revealed. In addition, the influence of Na+ on Cu2 + uptake was observed for

Acknowledgement

This research project was funded by the Environment Agency of England and Wales, the European Copper Institute, the European Nickel Industry Association, the International Cadmium Association, the International Zinc Association (Europe), the Rio Tinto and the Scottish Environment Protection Agency (Bass et al., 2008). We thank Edward Tipping and the CEH staff for collecting the invertebrate specimens in the field and performing the water chemistry analyses — Nicholas Kneebone, Alan Lawlor,

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