Impacts of heavy metals, polyaromatic hydrocarbons, and pesticides on freeze tolerance of the earthworm Dendrobaena octaedra

Previous studies have shown that the interactions between chemicals and climatic stressors can lead to synergistically increased mortality. In the present study, we investigated the effect of seven common environmental contaminants on survival at -6 and 15°C as well as on reproduction at 15°C in the earthworm Dendrobaena octaedra. Three classes of chemicals were considered: Heavy metals (nickel, lead, and mercury), polycyclic aromatic hydrocarbons (pyrene and phenanthrene), and pesticides (abamectin and carbendazim). Phenanthrene interacted antagonistically with freezing temperatures, whereas no interaction was observed with any of the tested pesticides. Two of the three tested metals (nickel and mercury) reduced the freeze tolerance synergistically (mercury was especially potent). This suggests that traditional laboratory studies, in which organisms are exposed to increasing concentrations of a single compound under otherwise optimal conditions, may underestimate the toxicity of some metals to field populations living in cold areas.

[1]  D. Bagchi,et al.  Oxidative mechanisms in the toxicity of metal ions. , 1995, Free radical biology & medicine.

[2]  N. M. Straalen,et al.  A Review of the Effects of Multiple Stressors on Aquatic Organisms and Analysis of Uncertainty Factors for Use in Risk Assessment , 2001, Critical reviews in toxicology.

[3]  Colin R. Janssen,et al.  Ecotoxicity of mercury to Eisenia fetida, Enchytraeus albidus and Folsomia candida , 2001, Biology and Fertility of Soils.

[4]  K. Hedlund,et al.  Cold acclimation and lipid composition in the earthworm Dendrobaena octaedra. , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[5]  E. Zvereva,et al.  Industrial barrens: extreme habitats created by non-ferrous metallurgy , 2007 .

[6]  M. Holmstrup,et al.  Synergistic interaction between 4-nonylphenol and high but not low temperatures in Dendrobaena octaedra. , 2009, Ecotoxicology and environmental safety.

[7]  J. Hazel.  Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? , 1995, Annual review of physiology.

[8]  H. Nayyar,et al.  Carbendazim alleviates effects of water stress on chickpea seedlings , 2005, Biologia Plantarum.

[9]  P. Krogh,et al.  Relative sensitivity of three terrestrial invertebrate tests to polycyclic aromatic compounds , 2002, Environmental toxicology and chemistry.

[10]  M. Depledge.  Enhanced copper toxicity resulting from environmental stress factor synergies , 1987 .

[11]  Christian Damgaard,et al.  Stress synergy between environmentally realistic levels of copper and frost in the earthworm Dendrobaena octaedra. , 2005, Environmental toxicology and chemistry.

[12]  M. Hodson,et al.  The influence of different artificial soil types on the acute toxicity of carbendazim to the earthworm Eisenia fetida in laboratory toxicity tests , 2007 .

[13]  Michael S. McLachlan,et al.  Atmospheric deposition of semivolatile organic compounds to two forest canopies , 1998 .

[14]  M. Hodson,et al.  Survival, Pb-uptake and behaviour of three species of earthworm in Pb treated soils determined using an OECD-style toxicity test and a soil avoidance test. , 2005, Environmental pollution.

[15]  D. Spurgeon,et al.  Toxicological and biochemical responses of the earthworm Lumbricus rubellus to pyrene, a non-carcinogenic polycyclic aromatic hydrocarbon. , 2004, Chemosphere.

[16]  M. Fisher,et al.  Structure and activity of avermectins and milbemycins in animal health. , 1995, Veterinary parasitology.

[17]  C. Edwards,et al.  The Effects of Toxic Chemicals on Earthworms , 1992 .

[18]  C. Damgaard,et al.  Life-history traits and population growth rate in the laboratory of the earthworm Dendrobaena octaedra cultured in copper-contaminated soil , 2007 .

[19]  H. Danks,et al.  Role of membrane transport of water and glycerol in the freeze tolerance of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae). , 2006, Journal of insect physiology.

[20]  D. T. Jones,et al.  Effects of cadmium, copper, lead and zinc on growth, reproduction and survival of the earthworm Eisenia fetida (Savigny): Assessing the environmental impact of point-source metal contamination in terrestrial ecosystems. , 1994, Environmental pollution.

[21]  M. Cronin,et al.  Metals, toxicity and oxidative stress. , 2005, Current medicinal chemistry.

[22]  Robert M Stroud,et al.  Structural basis of aquaporin inhibition by mercury. , 2007, Journal of molecular biology.

[23]  M. Holmstrup,et al.  A comparative analysis of the toxicity of eight common soil contaminants and their effects on drought tolerance in the collembolan Folsomia candida. , 2005, Ecotoxicology and environmental safety.

[24]  J. Scott-Fordsmand,et al.  Sub-lethal toxicity of the antiparasitic abamectin on earthworms and the application of neutral red retention time as a biomarker. , 2007, Chemosphere.

[25]  M. Holmstrup,et al.  Determining factors for cryoprotectant accumulation in the freeze-tolerant earthworm, Dendrobaena octaedra. , 2007, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[26]  Ari Väisänen,et al.  Effects of heavy metals on earthworms along contamination gradients in organic rich soils. , 2004, Ecotoxicology and environmental safety.

[27]  K. E. Zachariassen,et al.  Synergistic effects of an oil dispersant and low temperature on the freezing tolerance and solute concentrations of the blue mussel (Mytilus edulis L.) , 1983 .

[28]  S. O. Petersen,et al.  Drought acclimation confers cold tolerance in the soil collembolan Folsomia candida. , 2001, Journal of insect physiology.

[29]  D. Connell,et al.  The internal critical level concept of nonspecific toxicity. , 1999, Reviews of environmental contamination and toxicology.

[30]  Colin R. Janssen,et al.  Ecotoxicity of nickel to Eisenia fetida, Enchytraeus albidus and Folsomia candida. , 2002, Chemosphere.

[31]  C. A. V. van Gestel,et al.  Toxicity of abamectin and doramectin to soil invertebrates. , 2008, Environmental pollution.

[32]  A. Rukhin.  Bayes and Empirical Bayes Methods for Data Analysis , 1997 .

[33]  CHRISTIAN Damgaard,et al.  Dose-response curve modeling of excess mortality caused by two forms of stress , 2004, Environmental and Ecological Statistics.

[34]  A. Bondar,et al.  Copper Inhibits the Water and Glycerol Permeability of Aquaporin-3* , 2004, Journal of Biological Chemistry.

[35]  M. Borgnia,et al.  Cellular and molecular biology of the aquaporin water channels. , 1999, Annual review of biochemistry.