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Effects of copper fungicide residues on the microbial function of vineyard soils

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Abstract

The use of copper-based fungicides leads to an accumulation of copper (Cu) in vineyard soils, potentially causing adverse effects to the microbial function and fertility of the soil. This study used a soil microcosm approach to assess the effects of Cu accumulation on microbial function in vineyard soils. Surface soil samples were collected from 10 vineyards and a number of un-impacted reference sites in each of three different viticultural regions of Australia. The field-collected soils were transferred to microcosms and maintained for up to 93 days in the laboratory at 20–22 °C and 60 % of their maximum water-holding capacity. The microbial function of the soils was indicated by measuring phosphomonoesterase, arylsulfatase, urease, and phenol oxidase activities. In general, the vineyard soils had greater concentrations of Cu and lower enzyme activities than in the reference soils, although a weak negative relationship between Cu and enzyme activity could only be found for phosphomonoesterase activity. The results show that soil physical–chemical properties (i.e., organic carbon, pH) are greater determinants of soil enzyme activity than increased soil Cu concentration at the Cu concentrations present in vineyard soils.

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References

  • Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Poll 47:335–379

    Article  Google Scholar 

  • Brandt KK, Frandsen RJN, Holm PE, Nybroe O (2010) Development of pollution-induced community tolerance is linked to structural and functional resilience of a soil bacterial community following a five-year field exposure to copper. Soil Biol Biochem 42:748–757

    Article  CAS  Google Scholar 

  • Broos K, Warne MSJ, Heemsbergen DA, Stevens D, Barnes MB, Correll RL, McLaughlin MJ (2007) Soil factors controlling the toxicity of copper and zinc to microbial processes in Australian soils. Environ Toxicol Chem 26:583–590

    Article  CAS  Google Scholar 

  • Brussaard L, de Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agr Ecosyst Environ 121:233–244

    Article  Google Scholar 

  • Bunemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms—a review. Aus J Soil Res 44:379–406

    Article  Google Scholar 

  • Burrows LA, Edwards CA (2002) The use of integrated soil microcosms to predict effects of pesticides on soil ecosystems. Eur J Soil Biol 38:245–249

    Article  CAS  Google Scholar 

  • Chaperon S, Sauve S (2007) Toxicity interaction of metals (Ag, Cu, Hg, Zn) to urease and dehydrogenase activities in soils. Soil Biol Biochem 39:2329–2338

    Article  CAS  Google Scholar 

  • Chen SK, Edwards CA (2001) A microcosm approach to assess the effects of fungicides on soil ecological processes and plant growth: comparisons of two soil types. Soil Biol Biochem 33:1981–1991

    Article  CAS  Google Scholar 

  • Diaz-Ravina M, de Anta RC, Baath E (2007) Tolerance (PICT) of the bacterial communities to copper in vineyards soils from Spain. J Environ Qual 36:1760–1764

    Article  CAS  Google Scholar 

  • Dussault M, Becaert V, Francois M, Sauve S, Deschenes L (2008) Effect of copper on soil functional stability measured by relative soil stability index (RSSI) based on two enzyme activities. Chemosphere 72:755–762

    Article  CAS  Google Scholar 

  • Fernández-Calviño D, Nóvoa-Muñoz JC, Díaz-Raviña M, Arias-Estévez M (2009) Copper accumulation and fractionation in vineyard soils from temperate humid zone (NW Iberian Peninsula). Geoderma 153:119–129

    Article  Google Scholar 

  • Fernández-Calviño D, Soler-Rovira P, Polo A, Díaz-Raviña M, Arias-Estévez M, Plaza C (2010) Enzyme activities in vineyard soils long-term treated with copper-based fungicides. Soil Biol Biochem 42:2119–2127

    Article  Google Scholar 

  • Floch C, Alarcon-Gutierrez E, Criquet S (2009) Metal effects on phenol oxidase activities of soils. Ecotox Environ Safe 72:108–114

    Article  Google Scholar 

  • Gee GW, Bauder JW (1986) Particle-size analysis. In: Arnold K (ed) Methods of soil analysis. Part 1. Physical and mineralogical methods. American Society of Agronomy, Wisconsin

    Google Scholar 

  • Giller KE, Witter E, McGrath S (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    Article  CAS  Google Scholar 

  • Giller KE, Witter E, McGrath SP (2009) Heavy metals and soil microbes. Soil Biol Biochem 4:2031–2037

    Article  Google Scholar 

  • Komárek M, Cadková E, Chrastný V, Bordas F, Bollinger JC (2010) Contamination of vineyard soils with fungicides: a review of environmental and toxicological aspects. Environ Int 36:138–151

    Article  Google Scholar 

  • Mason HS (1948) The chemistry of melanin; mechanism of the oxidation of dihydroxyphenylalanine by tyrosinase. J Biol Chem 172:83–99

    Google Scholar 

  • Merrington G, Rogers SL, Van Zwieten L (2002) The potential impact of long-term copper fungicide usage on soil microbial biomass and microbial activity in an avocado orchard. Aus J Soil Res 40:749–759

    Article  CAS  Google Scholar 

  • Mertens J, Wakelin SA, Broos K, McLaughlin MJ, Smolders E (2010) Extent of copper tolerance and consequences for functional stability of the ammonia-oxidizing community in long-term copper-contaminated soils. Environ Toxicol Chem 29:27–37

    Article  CAS  Google Scholar 

  • Miller WP, Miller DM (1987) A micro-pippette method for soil mechanical analysis. Commun Soil Sci Plan 18:1–15

    Article  CAS  Google Scholar 

  • Nelson D, Sommers L (1996) Total carbon, organic carbon and organic matter. In: Sparks DL et al (eds) Methods of soil analysis. Part 3. Chemical methods. Soil Science Society of America/American Society of Agronomy, Madison, pp 961–1010

  • Oorts K, Bronckaers H, Smolders E (2006a) Discrepancy of the microbial response to elevated copper between freshly spiked and long-term contaminated soils. Environ Toxicol Chem 25:845–853

    Article  CAS  Google Scholar 

  • Oorts K, Ghesquiere U, Swinnen K, Smolders E (2006b) Soil properties affecting the toxicity of CuCl2 and NiCl2 for soil microbial processes in freshly spiked soils. Environ Toxicol Chem 25:836–844

    Article  CAS  Google Scholar 

  • Pietrzak U, McPhail DC (2004) Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia. Geoderma 122:151–166

    Article  CAS  Google Scholar 

  • Pind A, Freeman C, Lock MA (1994) Enzymic degradation of phenolic materials in peatlands—measurement of phenol oxidase activity. Plant Soil 159:227–231

    Article  CAS  Google Scholar 

  • Pym RVE, Milham PJ (1976) Selectivity of reaction among chlorine, ammonia, and salicylate for determination of ammonia. Anal Chem 48:1413–1415

    Article  CAS  Google Scholar 

  • Ranjard L, Echairi A, Nowak V, Lejon DPH, Nouaim R, Chaussod R (2006) Field and microcosm experiments to evaluate the effects of agricultural Cu treatment on the density and genetic structure of microbial communities in two different soils. FEMS Microbiol Ecol 58:303–315

    Article  CAS  Google Scholar 

  • Reardon J, Foreman JA, Searcy RL (1966) New reactants for the colorimetric determination of ammonia. Clin Chim Acta 14:203–205

    Article  CAS  Google Scholar 

  • Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  Google Scholar 

  • Sauve S, McBride MB, Norvell WA, Hendershot WH (1997) Copper solubility and speciation of in situ contaminated soils: effects of copper level, pH and organic matter. Water Air Soil Poll 100:133–149

    Article  CAS  Google Scholar 

  • Sauve S, Hendershot W, Allen HE (2000) Solid-solution partitioning of metals in contaminated soils: dependence on pH, total metal burden, and organic matter. Environ Sci Technol 34:1125–1131

    Article  CAS  Google Scholar 

  • Schaffer A, Van den Brink PJ, Heimbach F, Hoy S, de Jong F, Rombke J, Sousa JP, Rob-Nickoll M (2008) Semi-field methods are a useful tool for the environmental risk assessment of pesticides in soil. Environ Sci Pollut Res 15:176–177

    Article  Google Scholar 

  • Sinsabaugh RL, Reynolds H, Long TM (2000) Rapid assay for amidohydrolase (urease) activity in environmental samples. Soil Biol Biochem 32:2095–2097

    Article  CAS  Google Scholar 

  • Speir TW, Ross DJ (2002) Hydrolytic enzyme activities to assess soil degradation and recovery. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, Inc., New York, pp 403–431

    Google Scholar 

  • Speir TW, van Schaik AP, Hunter LC, Ryburn JL, Percival HJ (2007) Attempts to derive EC50 values for heavy metals from land-applied Cu-Ni-, and Zn-spiked sewage sludge. Soil Biol Biochem 39:539–549

    Article  CAS  Google Scholar 

  • Stevenson FJ, Fitch A (1981) Reactions with organic matter. In: Loneragan JF, Graham RD (eds) Copper in soils and plants. Proceedings of the Golden Jubilee International Symposium, Academic Press, Murdoch University, Perth, Western Australia, pp 69–95

  • Strawn DG, Baker LL (2008) Speciation of Cu in a contaminated agricultural soil measured by XAFS, mu-XAFS, and mu-XRF. Environ Sci Technol 42:37–42

    Article  CAS  Google Scholar 

  • Sumner ME, Miller WP (1996) Cation exchange capacity and exchange coefficients. In: Sparks DL et al (eds) Methods of soil analysis. Part 3. Chemical methods. Soil Science Society of America/American Society of Agronomy, Madison, pp 1201–1229

  • Tabatabai MA (1994) Soil enzymes. In: Weaver RW et al (eds) Methods of soil analysis. Part 2. Microbiological and biochemical properties. Soil Science Society of America, Madison

  • Tabatabai A, Dick W (2002) Enzymes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, Inc., New York

    Google Scholar 

  • Taylor JP, Wilson B, Mills MS, Burns RG (2002) Comparison of microbial numbers and enzymatic activities in surface soils and subsoils using various techniques. Soil Biol Biochem 34:387–401

    Article  CAS  Google Scholar 

  • Wang J, He W, Sun T (2007) Soil urease activity affected by copper. J Northwest A & F University - Nat Sc Ed 35:135–140

    Google Scholar 

  • Wang QY, Zhou DM, Cang L (2009) Microbial and enzyme properties of apple orchard soil as affected by long-term application of copper fungicide. Soil Biol Biochem 41:1504–1509

    Article  CAS  Google Scholar 

  • Warman PR, Munroe MD (2010) The effects of high metal concentrations in soil-compost mixtures on soil enzymes. J Environ Sci Health B 45:633–638

    Article  CAS  Google Scholar 

  • Wightwick A, Mollah M, Smith J, MacGregor A (2006) Sampling considerations for surveying copper concentrations in Australian vineyard soils. Aus J Soil Res 44:771–717

    Article  Google Scholar 

  • Wightwick A, Mollah M, Partington D, Allinson G (2008) Copper fungicide residues in Australian vineyard soils. J Agr Food Chem 56:2457–2464

    Article  CAS  Google Scholar 

  • Wightwick A, Walters R, Allinson G, Reichman SM, Menzies NW (2010a) Environmental risks of fungicides used in horticultural production systems. In: Carisse O (ed) Fungicides. InTech, Reijka, pp 273–304

  • Wightwick AM, Croatto G, Allinson G, Menzies NW (2010b) Use of reference soils in determinations of 0.01 M calcium chloride available metals. Commun Soil Sci Plan 41:2602–2612

    Article  CAS  Google Scholar 

  • Wightwick AM, Salzman SA, Reichman SM, Allinson G, Menzies NW (2010c) Inter-regional variability in environmental availability of fungicide derived copper in vineyard soils: an Australian case study. J Agr Food Chem 58:449–457

    Article  CAS  Google Scholar 

  • Williams CJ, Shingara EA, Yavitt JB (2000) Phenol oxidase activity in peatlands in New York State: response to summer drought and peat type. Wetlands 20:416–421

    Article  Google Scholar 

  • Wyszkowska J, Kucharski J, Lajszner W (2005) Enzymatic activities in different soils contaminated with copper. Pol J Environ Stud 14:659–664

    CAS  Google Scholar 

  • Young A, Young R (2001) Soils in the Australian landscape. Oxford University Press, Melbourne

    Google Scholar 

Download references

Acknowledgments

This study was supported by the Co-operative Research Centre for Contamination Assessment and Remediation of the Environment (CRC CARE) and the Department of Primary Industries Victoria, Australia (project no. 06889). We would like to thank the laboratory staff in the inorganic chemistry section at DPI Werribee, Anitha Kunhikrishnan, and Kerrie Bell (University of South Australia) for the assistance with the chemical analysis of the soil samples, as well as Andrew Brastrup for the assistance with the collection of samples in the field. We also thank the participating grape growers for so kindly enabling us to collect soil samples from their vineyards.

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Authors and Affiliations

  1. School of Agriculture and Food Sciences, The University of Queensland, St Lucia, Queensland, 4072, Australia

    Adam M. Wightwick & Neal W. Menzies

  2. Co-operative Research Centre for Contamination Assessment and Remediation of the Environment (CRC CARE), Mawson Lakes, South Australia, 5095, Australia

    Adam M. Wightwick & Neal W. Menzies

  3. Future Farming Systems Research Division, Department of Primary Industries Victoria Queenscliff Centre, P.O. Box 114, Queenscliff, Victoria, 3225, Australia

    Adam M. Wightwick & Graeme Allinson

  4. School of Information Systems, Deakin University, P.O. Box 423, Warrnambool, Victoria, 3280, Australia

    Scott A. Salzman

  5. School of Civil, Environmental and Chemical Engineering, RMIT University, Melbourne, Victoria, 3001, Australia

    Suzanne M. Reichman

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  1. Adam M. Wightwick
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  5. Neal W. Menzies
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Correspondence to Graeme Allinson.

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Responsible editor: Zhihong Xu

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Wightwick, A.M., Salzman, S.A., Reichman, S.M. et al. Effects of copper fungicide residues on the microbial function of vineyard soils. Environ Sci Pollut Res 20, 1574–1585 (2013). https://doi.org/10.1007/s11356-012-1114-7

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