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Review of impacts on soil biota caused by copper residues from fungicide application

Lukas Van-Zwieten1, Graham Merrington2 and Melissa Van-Zwieten3

1NSW Department of Primary Industries, Wollongbar Agricultural Institute, Bruxner Hwy, Wollongbar NSW 2477.
Environment Agency, Chemicals Team, Science Base, Howbery Park, Wallingford, Oxfordshire, OX10 8BD, UK.
GeoLINK, Environmental Consultants, Lennox Head, NSW 2478, Australia.


Unlike most other agricultural chemicals, a significant weight of evidence exists that copper based fungicides have a long-term impact on a wide range of soil biota. Effects can occur at relatively low Cu concentrations and influence a number of soil processes including microbial activity, earthworm activity and bioturbation. In most soils, copper residues are likely to remain indefinitely, and will continue to influence the health of the soil. This manuscript reviews Australian and International data on the effects of copper based fungicides on soil health, and the implications for future land management.

Key words

Copper fungicide, earthworm avoidance, microbial activity.


The use of pesticides has long been a feature of conventional agricultural practice and their use has made it possible to increase crop yields and food production (Lee 1985). However, many of these chemicals have toxic effects that are not confined to their target species, and their application may have impacts on organisms that benefit the wider agroecosystem.

There is significant uncertainty in the prediction of impacts of external stressors such as pesticide application on the agricultural ecosystem (Liess 2004). Questions have been raised over the significance of short and even long-term population changes of soil organisms, especially where no other indicator of harm is documented. To further challenge the evaluation of impacts, there are no standard tests for soil biota, such as those found in other fields of ecotoxicology. Soils contain an extremely diverse array of microorganisms including bacteria, fungi, yeasts; photosynthetic organisms including algae, and macroorganisms such as protozoa, nematodes, mites, springtails, spiders, insects and earthworms. The functions of this complex array of biota, often referred to as the ‘soil food web,’ are diverse, and include residue decomposition, nutrient storage and release, soil structure and stability, resistance against disease and degradation or immobilisation of pesticides and other pollutants. Soil biota are measured or studied in many different ways, including direct observation under microscopes and other direct counting mechanisms, analysis of intra- and extracellular enzymes, respiration and biomass carbon, fatty acid profiles, and DNA fingerprinting.

It was not until the 1880s that copper fungicides rapidly developed due to the ‘accidental’ discovery of the Bordeaux mixture. At this time, farmers in the Bordeaux region, France were applying a paste mixture of copper sulphate and lime to grapes that were bordering the highways to deter passer-by’s. The French scientist, Millardet observed these grapes were also free of downy mildew (Copper Development Association 2003). By 1885, Millardet had completed experiments which confirmed this mixture controlled the mildew disease at very low cost. The Bordeaux mixture was the first fungicide to be used on a large scale world-wide (Schneiderhan 1933). Copper based fungicides have multi-site activity with a low risk of pathogens developing resistance.

In Australia, copper-containing sprays of various formulations (Table 1) have been used to control fungal diseases in pome and stone fruit orchards, vineyards and vegetable crops for well over 100 years (Merry et al. 1983). Over 7500 t yr-1 of Cu fungicides have been used, representing 13% of the global total (Lepp and Dickinson 1994). In stark comparison, England and Wales were estimated to use only 8 t of Cu fungicide between them in the year 2000 (Nicholson et al. 2003).

Table 1. Inorganic copper compounds used as fungicides in Australia.


Chemical formula


Cupric sulfate


Seed treatment and preparation of Bordeaux mixture

Copper dihydrazine sulfate


Powdery mildew
Black spot of roses

Copper oxychloride


Powdery mildews

Copper oxychloride sulfate

3Cu(OH)2.CuCl2 and 3Cu(OH)2.CuSO4

Many fungal diseases

Copper zinc chromates


Diseases of potato, tomato, cucurbits, peanuts and citrus

Cuprous oxide


Powdery mildews

Basic copper sulfate


Seed treatment and preparation of Bordeaux mixture

Cupric carbonate


Many fungal diseases

Copper hydroxide


Many fungal diseases

Source: Ware (1978)

Horticultural and viticultural operations with a long history of copper fungicide application have resulted in accumulations of copper in surface horizons (Gallagher et al. 2001; Chaignon et al. 2003). Prolonged use in Europe has lead to high levels in the soil (200-500 mg/kg in France, Brun et al. 1998), which has affected a large portion of agricultural land. An Australian study found up to 250mg/kg total copper in a 20-30 yr old vineyard soil, while 8-14 vineyards studied exceeded 60 mg/kg (Pietrzak and McPhail 2004). Similarly, avocado orchard soils in northern NSW were recently observed to have even greater soil Cu residues (280-340 mg/kg) (Merrington et al. 2002).

An example of an industry reliant upon copper fungicides in Australia is the avocado industry. Avocado orchards on the north coast of New South Wales have had copper oxychloride, cuprous oxide, copper hydroxide and copper ammonium acetate applied at up to 15 times per year mainly against anthracnose (Colletotrichum gloeosporoides) at recommended foliar application rates of 3-6 kg/ha (Van Zwieten et al. 2004). By contrast the use of copper-containing products in organic farming practices in Australia is restricted: Copper sulphate and hydrated lime mixtures, copper hydroxide and copper sulphates are permitted by certifying authorities but copper oxychloride is prohibited (Biological Famers of Australia 2003). Further, since 2002, the International Federation of Organic Agriculture Movements (IFOAM) has regulated total copper input on organic farms to a maximum of 8 kg/ha/yr. These restrictions applied by the organic farming industry acknowledge the potential for copper levels in orchard top-soils to accumulate with repeated application.

Impacts of copper on soil biota in an Australian study

Cu residues in avocado orchards have recently been shown to impact significantly on soil microorganisms (Merrington et al. 2002). Cu residues (280 and 340 mg/kg, respectively) in surface soils (0-2cm) of an established orchard were shown to be significantly greater than a nearby reference site under natural vegetation (13 mg/kg) (Table 2). The available fraction of Cu in these soils was also shown to be significantly greater (2.15 and 1.29 mg/kg, c. pCu2+ 8.64) than in the reference site (0.71 mg/kg, c. pCu2+ 9.2), as measured by ion-selective electrode in CaCl2 extraction. Similar trends were observed for the 2-10 cm soil profile. Data (Table 3) suggested that the Cu residues were responsible for significant reductions in biomass carbon (Cmic) even though the orchard soils had similar or elevated levels of total organic carbon (Corg). The Cmic:Corg ratio was significantly lower in all of the Cu contaminated soils. Soil respiration was elevated (6.04 and 5.57 mg CO2- C/kg/day) compared to the reference soil (3.04 mg CO2- C/kg/day), and the metabolic quotient (qCO2) was also significantly greater, indicating the microbial populations in these soils were stressed

Table 2. Free Cu as pCu2+, and expressed as free Cu concentration and percentage of CaCl2 extractable Cu in the orchard and reference soil.

Values are means ± standard error; n = 6. Significantly (*P≤ 0.05) different from respective soil layer in the reference soil

Sample site

‘Total’ Cu

CaCl2 extractable
Cu (mg/kg)


Free Cu2+ concentration (μg/L)

% Free Cu :CaCl2 extractable Cu

C (%)

(1:5 CaCl2)

Block 1,
0-2 cm

280 ± 33*

2.15 ± 0.39*

8.64 ± 0.25*



8.82 ± 0.48*

6.01 ± 0.23*

Block 1,
2-10 cm

176 ± 48*

0.76 ± 0.12*

8.89 ±0.22*



4.88 ± 0.59

4.50 ± 0.47

Block 2,
0-2 cm

345 ± 78*

1.29 ± 0.21*

9.17 ± 0.16



8.43 ± 1.00*

5.80 ± 0.20*

Block 2,
2-10 cm

301± 112*

0.71 ± 0.15*

8.90 ± 0.21*



5.37 ± 0.14

5.34 ± 0.23

Reference, 0-2 cm

13 ± 1.8

0.71 ± 0.19

9.14 ± 0.05



6.74 ± 0.14

4.43 ± 0.05

Reference, 2-10 cm

14 ± 0.1

0.24 ± 0.05

9.36 ± 0.07



4.93 ± 0.30

4.51 ± 0.13

Source: Merrington et al. (2002)

Table 3. Microbial biomass C, soil respiration, metabolic quotient (qCO2) in the orchard and reference soil.

Values are means ± standard error; n = 6. *(P≤ 0.05) significantly different from respective soil layer in the reference soil

Sample site

(mg C/kg)

(% of Organic-C)

Soil respiration
(mg CO2-C/kg/ day)

(mg CO2-C/g biomass C/ day)

Block 1,
0-2 cm

2167 ± 197*

2.48 ± 0.23*

6.04 ± 0.93*

2.85 ±0.40*

Block 1,

1021 ± 228*

2.01 ± 0.25*

1.11 ± 0.27

1.08 ± 0.21

Block 2,
0-2 cm

2023 ± 226*

2.48 ± 0.42*

5.57 ± 2.23*

2.85 ± 0.13*

Block 2,

1429 ± 170*

2.68 ± 0.47*

0.60 ± 0.13

0.48 ± 0.15

0-2 cm

2617 ± 23

3.88 ± 0.05

3.04 ± 0.26

1.17 ± 0.01


2424 ± 243

4.90 ± 0.20

3.00 ± 0.16

1.26 ± 0.13

Source: Merrington et al. (2002)

The avocado farmer from the site of the Merrington et al. 2002 study also observed that very few worms were located in the orchard. To study the impact of copper on earthworms, avoidance studies were undertaken using methods described by Yeardley et al. (1996). In these trials, worms were given the option to move between the target soil (ie, copper contaminated orchard soil), and a control soil. Various dilutions of the orchard soil were also made with the control. Results (Van Zwieten et al. 2004) showed the worms preferred non-contaminated control soils, sourced from adjacent to the orchard or an OECD standard uncontaminated soil, when Cu residues in the orchard soils reached 4-34 mg/kg. At levels of 553 mg/kg, 90% avoidance of orchard soil was observed (Figure 1).

Figure 1. Observed and predicted response of worms to copper concentration in each test soil. Note that the curves for the OECD control vs farm 1 soil and OECD control vs farm 2 soil overlap. A 50% distribution of worms indicates 50% of the worms were found in the test soil and 50% were found in the control (uncontaminated) soil (ie no avoidance found).

Source: Van Zwieten et al. (2004)

The avoidance of soils contaminated by copper was reflected in a field study. The avocado orchard was sampled using a methodology described by Kingston and Temple-Smith (1988). Ten 20 cm square holes at distances of 10 m apart were dug to a depth of 30 cm. Soil was removed and placed on a plastic sheet where it was manually broken down. All worms found at each hole, whether whole or damaged, were placed directly into a jar containing 70% ethanol in water (by volume) and returned to the laboratory. The worms were removed from the jars, counted, rolled on tissues to remove excess fluid, counted and weighed.

Copper residues of between 180-338 mg/kg resulted in very low earthworm numbers and biomass (Table 4), when compared to a reference site directly adjacent to the contaminated orchard on similar soil type. Worms found under the canopy were small hence the low biomass found, while a large individual specimen found inter-row resulted in a high biomass/ worm number.

Table 4. Earthworm number and biomass in the orchard and reference soil.

Site location


(mg kg-1)

Earthworm number m-2

Earthworm biomass (g m-2)





under canopy




Control site




Source: Van Zwieten et al. (2004)


Copper is an essential element and required by all organisms. However, elevated concentrations of copper in soils are toxic and may result in a range of effects including reduced biological activity and subsequent loss of fertility (Dumestre et al. 1999). It has been demonstrated here in Australian studies that copper residues in avocado orchards affect several soil health indicators; including microbial activity, earthworm populations and other processes such as bioturbation.

Earthworms have been suggested as useful indicators of soil health (de Bruyn 1997; Paoletti et al. 1998). Through their feeding and burrowing activity, earthworms aid in decomposition and incorporation of organic matter, increase the number of water soluble aggregates, improve water infiltration, aeration, drainage and root penetration, and increase microbial activity (Lee 1985). Earthworm casts and burrow walls exhibit higher concentrations of total and plant-available elements than surrounding soil and it has been recognised that surface feeding species horizontally and vertically disseminate micro-organisms, spores, pollen and seeds (Makeschin 1997) and can reduce plant pathogens through digestion of fungal spores (Hirst et al. 1955). Therefore practices that reduce earthworm populations in soil can lead to a reduction in soil health.

Within Australia, earthworms have been given serious consideration only in the context of temperate and Mediterranean pastures and cropping. Little relevant information had been gathered for sub-tropical agriculture. It has recently been shown (Dr. Tim Kingston, pers com) that a far greater incidence of native worms is present in sub-tropical agriculture than in many other regions in Australia. The role of native earthworms in sub-tropical agriculture is still under investigation.

Soils that contain significant copper residues have been observed to have few earthworms (Van Rhee 1967, Van Zwieten et al. 2004), reduced surface activity (fewer castings visible at the soil surface) and greater litter build-up (Ma 1984). At sites in a study on avocado orchards in northern NSW (Merrington et al. 2002) an absence of earthworms in areas of copper contamination was accompanied by a thick layer of organic matter (ca. 10-30 cm deep) that was clearly stratified on the soil surface, with little evidence of breakdown and incorporation into the sub-surface layers. This phenomenon is not seen in other sub-tropical horticultural systems where copper fungicides are not used.

A strong correlation has been observed between soil-copper concentration and the level of copper in earthworm tissues (Ma et al. 1983). It has been noted that earthworms exhibit chronic toxic responses at relatively low concentrations of copper (< 4-16 mg/kg) (Helling et al. 2000). The enchytraeid worm Cognettia sphagnetorum was shown to actively avoid copper contaminated soil (Salminen and Haimi 2001). Copper oxychloride has recently been shown to reduce populations of the earthworm Aporrectodea caliginosa in field trials six months following application of the fungicide (Maboeta et al. 2003).

Elevated Cu concentrations have been shown to reduce beneficial mycorrhizal associations (Liao et al. 2003) reduce microbial activity and function (Bogomolov et al. 1996) and impact a range of mesofauna (Böckl et al. 1998).

Thrupp (1991) found that copper arising primarily through application of Bordeaux tended to be associated with areas of high organic matter build-up in former banana plantations in Costa Rica. These soils were damaging to subsequent crops (i.e. phytotoxic). Residues ranging between 20 and 4000 mg/kg and were shown to have had a significant adverse effect on once fertile productive agricultural soils. It is likely that copper residues were toxic to soil organisms, restricting bioturbation of soil, hence resulting in accumulation of organic materials. This result is reflected in the findings of the current study where a thick layer of organic matter was found in the avocado orchard soils, however, phytotoxicity has not been evident. Phytotoxicity of copper depends on its bioavailability (Alva et al. 2000), which is controlled principally by pH, redox potential, oxide content, and clay mineral influences. However, there is limited unequivocal evidence suggesting the overriding importance of any one of these soil physico-chemical parameters. For example, Lock and Janssen (2001) noted that at relatively low organic matter content (1.5%) a soil pH increase from 4-7 reduced toxicity (14 day LC50) in the worm E. albdus from 169 to 530 mg Cu/kg. Ma (1984) observed that a pH increase over a similar range had no effect on toxicity to the earthworm Lubriculus rubellus.

Other non-target species impacted by copper include mites (Michaud and Grant 2003), entomopathic fungus (McCoy et al. 1996) and nematodes (Jaworska and Gorczyca 2002). In some instances, these species have been stimulated by copper applications and have resulted in major outbreaks of a pest and subsequent losses in production. Thus, the environmental side effects of copper-based fungicides may be more wide spread than the impacts on soil health and soil biota.

A recent study in SE QLD assessed the effects of copper fungicide on anthracnose (a fungal disease) on avocados. The study showed the use of copper significantly reduced the numbers of bacteria, filamentous fungi and yeasts on leaf and fruit surfaces. Furthermore, there was a significantly higher disease occurrence on the copper-sprayed fruit (Stirling et al. 1999). The authors attributed this to the ability of the naturally occurring microorganisms to suppress pathogenic species, while the copper based fungicides eliminated the possibility of natural predation.


The evidence reviewed in this paper demonstrates that copper residues originating from fungicide application reduce soil microbial biomass, while stressing the microorganisms that are present. In addition, copper has resulted in an elimination of earthworms in the orchard where residues averaged between 180-338 mg/kg. This has influenced soil processes by reducing bioturbation, thus potentially influencing other soil physical and chemical processes. There is a need for a better evaluation of the potential impacts of copper contamination in agricultural land, and management strategies/remediation technologies need to be developed to reduce the bioavailability of existing residues. One of the strategies that could be implemented immediately is the reduction of further inputs, through the use of alternative fungicides, of either chemical or biological origin. A recent review of alternative fungal control agents has recent been published (Van Zwieten et al. 2004b), with products including: Selected biological control agents; Compost; Inoculated compost; Surfactants and biosurfactants; Antifungal compounds; Compost tea; pH modifiers and bicarbonates; Foliar calcium and silicone; Milk products and other organic amendments (eg. molasses); Essential oils (eg. tea tree) and Polymer coatings all showing promise as alternatives to copper for disease control.


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