Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Bioavailability of copper and zinc to poplar and microorganisms in a biosolids-amended soil

P. Jeyakumar A D , P. Loganathan A , S. Sivakumaran B , C. W. N. Anderson A and R. G. McLaren C
+ Author Affiliations
- Author Affiliations

A Soil and Earth Sciences, Institute of Natural Resources, Massey University, Palmerston North 4442, New Zealand.

B Sustainable Production–Soil Water Environment, Plant & Food Research, Palmerston North 4442, New Zealand.

C Soil and Physical Sciences Department, Agriculture and Life Sciences Faculty, Lincoln University, Lincoln 7647, New Zealand.

D Corresponding author. Email: j.jeyakumar@massey.ac.nz

Australian Journal of Soil Research 48(5) 459-469 https://doi.org/10.1071/SR09169
Submitted: 28 September 2009  Accepted: 15 March 2010   Published: 6 August 2010

Abstract

The effects of high concentrations of copper (Cu) and zinc (Zn) in a soil treated with biosolids previously spiked with these metals on poplar (Populus deltoides × yunnanensis) were investigated in a pot trial. The total soil metal concentrations in the treatments were 12, 46, 137, and 226 mg Cu/kg and 25, 141, 433, and 686 mg Zn/kg. Copper accumulation was lower in poplar leaves than Zn and the maximum bioconcentration factor was 0.8 for Cu and 10 for Zn. Copper was not found to be toxic to plants at any level of application or to mycorrhiza up to 137 mg/kg, but it was found to be toxic to soil microorganisms at all levels of Cu addition. Copper application increased mycorrhiza colonisation up to 137 mg Cu/kg and root dry matter at 226 mg Cu/kg, but had no effect on leaf dry matter. Increasing Zn rate decreased all plant and soil parameters. Lower percentages of Cu in the soil exchangeable fraction, and a lower Cu2+ concentrations in soil solution relative to Zn indicated lower bioavailability of Cu. Dehydrogenase activity was reduced by 50% at total solution-phase Cu and Zn concentrations of 0.1 and 27 mg/L, respectively, and solid-phase exchangeable Cu and Zn concentrations of 5 and 169 mg/kg, respectively.

Additional keywords: mycorrhiza, dehydrogenase activity, copper toxicity, zinc toxicity, soil copper fractions, soil zinc fractions.


Acknowledgments

We thank RST Environmental Solutions Ltd, Palmerston North, New Zealand for providing poplar cuttings, and Stéphanie Caille for measuring mycorrhizae colonized roots infection.


References


Adriano DC (2001) ‘Trace elements in terrestrial environments: biogeochemistry, bioavailability and risks of metals.’ 2nd edn. (Springer: New York)

Antonious GF, Turley ET, Sikora F, Snyder JC (2008) Heavy metal mobility in runoff water and absorption by eggplant fruits from sludge treated soil. Journal of Environmental Science and Health 43, 526–532.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Arduini I, Godbold DL, Onnis A (1995) Influence of copper on root growth and morphology of Pinus pinea L. and Pinus pinaster Ait. seedlings. Tree Physiology 15, 411–415.
PubMed |
open url image1

Borghi M, Tognetti R, Monteforti G, Sebastiani L (2007) Responses of Populus×euramericana (P. deltoides × P. nigra) clone Adda to increasing copper concentrations. Environmental and Experimental Botany 61, 66–73.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brundrett MC, Abbott LK (1994) Mycorrhizal fungus propagules in the jarrah forest. I. Seasonal Study of Inoculum Levels. New Phytologist 127, 539–546.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cancès B, Ponthieu M, Castrec-Rouelle M, Aubry E, Benedetti MF (2003) Metal ions speciation in a soil and its solution: experimental data and model results. Geoderma 113, 341–355.
Crossref | GoogleScholarGoogle Scholar | open url image1

Castiglione S, Todeschini V, Franchin C, Torrigiani P, Gastaldi D, Cicatelli A, Rinaudo C, Berta G, Biondi S, Lingua G (2009) Clonal differences in survival capacity, copper and zinc accumulation, and correlation with leaf polyamine levels in poplar: a large-scale field trial on heavily polluted soil. Environmental Pollution 157, 2108–2117.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Centre for Ecology and Hydrology (2002) ‘Windermere humic aqueous model (WHAM): Equilibrium chemical speciation for natural waters.’ (Natural Environmental Research Council: Swindon, UK)

Chander K, Brookes PC (1991) Is the dehydrogenase assay invalid as a method to estimate microbial activity in copper contaminated soils? Soil Biology & Biochemistry 23, 909–915.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chaney RL (1989) Toxic element accumulation in soils and crops: protecting soil fertility and agricultural food chains. In ‘Inorganic contaminants in the vadose zone’. (Eds B Bar-Yosef, NJ Barrow, J Goldshmid) pp. 140–158. (Springer-Verlag: Berlin)

Chaperon S, Sauve S (2007) Toxicity interaction of metals (Ag, Cu, Hg, Zn) to urease and dehydrogenase activities in soils. Soil Biology & Biochemistry 39, 2329–2338.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chaudri AM, Knight BP, Barbosa-Jefferson VL, Preston S, Paton GI, Killham K, Coad N, Nicholson FA, Chambers BJ, McGrath SP (1999) Determination of acute Zn toxicity in pore water from soils previously treated with sewage sludge using bioluminescence assays. Environmental Science & Technology 33, 1880–1885.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chaudri AM, Lawlor K, Preston S, Paton GI, Killham K, McGrath SP (2000) Response of a Rhizobium-based luminescence biosensor to Zn and Cu in soil solutions from sewage sludge treated soils. Soil Biology & Biochemistry 32, 383–388.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colpaert JV, Muller LAH, Lambaerts M, Adriaensen K, Vangronsveld J (2004) Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytologist 162, 549–559.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colpaert JV, Van Assche JA (1993) The effects of cadmium on ectomycorrhizal Pinus sylvestris L. New Phytologist 123, 325–333.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dakora FD, Phillips DA (2002) Root exudates as mediators for mineral acquisition in low-nutrient environments. Plant and Soil 245, 35–47.
Crossref | GoogleScholarGoogle Scholar | open url image1

Denny HJ, Wilkins DA (1987) Zinc tolerance in Betula spp. IV. The mechanism of ectomycorrhizal amelioration of zinc toxicity. New Phytologist 106, 545–553. open url image1

Dixon RK, Buschena CA (1988) Response of ectomycorrhizal Pinus banksiana and Picea glaucato heavy metals in soil. Plant and Soil 105, 265–271.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dos Santos Utmazian MN, Wenzel WW (2007) Cadmium and zinc accumulation in willow and poplar species grown on polluted soils. Journal of Plant Nutrition and Soil Science 170, 265–272.
Crossref | GoogleScholarGoogle Scholar | open url image1

French CJ, Dickinson NM, Putwain PD (2006) Woody biomass phytoremediation of contaminated brownfield land. Environmental Pollution 141, 387–395.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gadd GM (1993) Interactions of fungi with toxic metals. New Phytologist 124, 25–60.
Crossref | GoogleScholarGoogle Scholar | open url image1

Galli U, Schuepp H, Brunold C (1994) Heavy metal binding by mycorrhizal fungi. Physiologia Plantarum 92, 364–368.
Crossref | GoogleScholarGoogle Scholar | open url image1

Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gorge JL, Lastra O, Chueca A, Lachica M (1985) Use of photosynthetic parameters for the diagnosis of copper deficiency in Pinus radiata seedlings. Physiologia Plantarum 65, 508–512.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hartley J, Cairney JWD, Meharg AA (1997) Do ectomycorrhizal fungi exhibit adaptive tolerance to potentially toxic metals in the environment? Plant and Soil 189, 303–319.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hassinen V, Vallinkosski VM, Issakainen S, Tervahauta A, Karenlampi S (2009) Correlation of forliar MT2b expression with Cd and Zn concentrations in hybrid aspen (Populus tremula×tremuloides) grown in contaminated soil. Environmental Pollution 157, 922–930.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hewitt AE (1998) ‘New Zealand soil classification.’ Landcare Research Science Series No. 1. (Manaaki Whenua Press: Lincoln, NZ)

Horswell J, Weitz HJ, Percival HJ, Speir TW (2006) Impact of heavy metal amended sewage sludge on forest soils as assessed by bacterial and fungal biosensors. Biology and Fertility of Soils 42, 569–576.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huang Y, Tao S, Chen YJ (2005) The role of arbuscular mycorrhiza on change of heavy metal speciation in rhizosphere of maize in wastewater irrigated agriculture soil. Journal of Environmental Sciences (China) 17, 276–280.
PubMed |
open url image1

Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiologia Plantarum 109, 107–116.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jeyakumar P, Loganathan P, Sivakumaran S, Anderson CWN, McLaren RG (2008) Copper and zinc spiking of biosolids: effect of incubation period on metal fractionation and speciation and microbial activity. Environmental Chemistry 5, 347–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Joner EJ, Jakobsen I (1995) Growth and extracellular phosphatase activity of arbuscular mycorrhizal hyphae as influenced by soil organic matter. Soil Biology & Biochemistry 27, 1153–1159.
Crossref | GoogleScholarGoogle Scholar | open url image1

Joner EJ, Magid J, Gahoonia TS, Jakobsen I (1995) P depletion and activity of phosphatases in the rhizosphere of mycorrhizal and non-mycorrhizal cucumber (Cucumis sativus L.). Soil Biology & Biochemistry 27, 1145–1151.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kabata-Pendias A (1993) Behavioural properties of trace metals in soils. Applied Geochemistry 8, 3–9.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kang H, Freeman C (2007) Interactions of marsh orchid (Dactylorhiza spp.) and soil microorganisms in relation to extracellular enzyme activities in a peat soil. Pedosphere 17, 681–687.
Crossref | GoogleScholarGoogle Scholar | open url image1

Komarek M, Tlustos P, Szakova J, Chrastny V (2008) The use of poplar during a two-year induced phytoextraction of metals from contaminated agricultural soils. Environmental Pollution 151, 27–38.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kovacs B, Prokisch J, Gyori Z, Kovacs AB, Palencsar AJ (2000) Studies on soil sample preparation for inductively coupled plasma atomic Emission spectrometry analysis. Communications in Soil Science and Plant Analysis 31, 1949–1963.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krpata D, Peintner U, Langer I, Fitz W, Schweiger P (2008) Ectomycorrhizal communities associated with Populus tremula L. growing in a heavy metal contaminated site. Mycological Research 112, 1069–1079.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Laureysens I, De Temmerman L, Hastir T, Van Gysel M, Ceulemans R (2005) Clonal variation in heavy metal accumulation and biomass production in a poplar coppice culture. II. Vertical distribution and phytoextraction potential. Environmental Pollution 133, 541–551.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu Q, Loganathan P, Hedley MJ, Grace LJ (2008) Effect of mycorrhizal inoculation on rhizosphere properties, phosphorus uptake and growth of pine seedlings treated with and without a phosphate rock fertilizer. Journal of Plant Nutrition 31, 137–156.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mapanda F, Mangwayana EN, Nyamangara J, Giller KE (2007) Uptake of heavy metals by vegetables irrigated using wastewater and the subsequent risks in Harare, Zimbabwe. Physics and Chemistry of the Earth 32, 1399–1405. open url image1

Martin F, Tuskan GA, DiFazio SP, Lammers P, Newcombe G, Podila GK (2004) Symbiotic sequencing for the Populus mesocosm. New Phytologist 161, 330–335.
Crossref | GoogleScholarGoogle Scholar | open url image1

McBride MB (1994) ‘Environmental chemistry of soils.’ (Oxford University Press: New York)

McLaren RG, Clucas LM (2001) Fractionation of copper, nickel, and zinc in metal-spiked sewage sludge. Journal of Environmental Quality 30, 1968–1975.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McLaren RG, Clucas LM, Taylor MD, Hendry T (2004) Leaching of macronutrients and metals from undisturbed soils treated with metal-spiked sewage sludge. 2. Leaching of metals. Australian Journal of Soil Research 42, 459–471.
Crossref | GoogleScholarGoogle Scholar | open url image1

McLaughlin MJ, Hamon RE, McLaren RG, Speir TW, Rogers SL (2000) Review: a bioavailability-based rationale for controlling metal and metalloid contamination of agricultural land in Australia and New Zealand. Australian Journal of Soil Research 38, 1037–1086.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mills T, Arnold B, Sivakumaran S, Northcott G, Vogeler I, Robinson B, Norling C, Leonil D (2006) Phytoremediation and long-term site management of soil contaminated with pentachlorophenol (PCP) and heavy metals. Journal of Environmental Management 79, 232–241.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

NZWWA (2003) ‘Guidelines for the safe application of biosolids to land in New Zealand.’ (New Zealand Water and Wastes Association: Wellington, NZ)

Obbard JP (2001) Ecotoxicological assessment of heavy metals in sewage sludge amended soils. Applied Geochemistry 16, 1405–1411.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oburger E, Kirk GJD, Wenzel WW, Puschenreiter M, Jones DL (2009) Interactive effects of organic acids in the rhizosphere. Soil Biology & Biochemistry 41, 449–457.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oliver IW, Merrinton G, McLaughlin MJ (2004) Australian biosolids: characterization and determination of available copper. Environmental Chemistry 1, 116–124.
Crossref | GoogleScholarGoogle Scholar | open url image1

Parker DR, Pedler JF (1997) Reevaluating the free-ion activity model of trace metal availability to higher plants. Plant and Soil 196, 223–228.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pepper IL , Gerba CP , Brendecke JW (1995) ‘Environmental microbiology–A laboratory manual.’ (Academic Press: San Diego, CA)

Quoreshi AM, Khasaa DP (2008) Effectiveness of mycorrhizal inoculation in the nursery on root colonization, growth, and nutrient uptake of aspen and balsam poplar. Biomass and Bioenergy 32, 381–391.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robson AD , Reuter DJ (1981) Diagnosis of copper deficiency and toxicity. In ‘Copper in soils and plants’. (Eds JF Loneragan, AD Robson, RD Graham) pp. 287–312. (Academic Press: London)

Russell RS (1977) ‘Plant root systems: their function and interaction with the soil.’ (McGraw-Hill Book Company (UK) Limited: London)

Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527–560.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

SAS Institute Inc. (2004) ‘SAS® 9.1.2 Users’ Guide.’ (SAS Institute INC.: Cary, NC)

Sell J, Kayser A, Schulin R, Brunner I (2005) Contribution of ectomycorrhizal fungi to cadmium uptake of poplars and willows from a heavily polluted soil. Plant and Soil 277, 245–253.
Crossref | GoogleScholarGoogle Scholar | open url image1

Smith S , Read D (1997) ‘Mycorrhizal symbiosis.’ (Academic Press: London)

Stobrawa K, Lorenc-Plucinska G (2008) Thresholds of heavy-metal toxicity in cuttings of European black poplar (Populus nigra L.) determined according to antioxidant status of fine roots and morphometrical disorders. The Science of the Total Environment 390, 86–96.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Systat Software Inc. (2006) ‘SigmaPlot 10 users’ guide.’ (Systat Software Inc.: Cary, NC)

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 Biology & Biochemistry 34, 387–401.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tecator (1983) ‘Application note (AN62/83): Determination of the sum of nitrate and nitrite in water by flow injection analysis.’ (Foss North America Technology: Eden Prairie, MN)

Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry 51, 844–851.
Crossref | GoogleScholarGoogle Scholar | open url image1

Todeschini V, Franchin C, Castiglione S, Burlando B, Biondi S, Torrigiani P, Berta G, Lingua G (2007) Responses of two registered poplar clones to copper, after inoculation, or not, with arbuscular mycorrhizal fungi. Caryologia 60, 146–155. open url image1

Tomsett BA (1993) Genetic and molecular biology of metal tolerance in fungi. In ‘Stress tolerance of fungi’. (Ed. DH Jennings) pp. 69–95. (Marcel Dekker: New York)

Unterbrunner R, Puschenreiter M, Sommer P, Wieshammer G, Zupan M, Tlustos P, Wenzel WW (2007) Heavy metal accumulation in trees growing on contaminated sites in Central Europe. Environmental Pollution 148, 107–114.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vervaeke P, Luyssaerta S, Mertensa J, Meersb E, Tackb FMG, Lusta N (2003) Phytoremediation prospects of willow stands on contaminated sediment: a field trial. Environmental Pollution 126, 275–282.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wilkins DA (1991) The influence of sheathing (ecto-) mycorrhizas of trees on the uptake and toxicity of metals. Agriculture, Ecosystems & Environment 35, 245–260.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wu J, Joergensen RG, Pommeraning B, Chaussod R, Brookes PC (1990) Measurements of soil microbial biomass C by fumigation-extraction – an automated procedure. Soil Biology & Biochemistry 22, 1167–1169.
Crossref | GoogleScholarGoogle Scholar | open url image1