Cover crops influence soil microorganisms and phytoextraction of copper from a moderately contaminated vineyard
Introduction
Due to the long history of application and continued use of copper containing fungicides in agriculture, copper (Cu) has accumulated within these topsoils (McBride et al., 1981, Mackie et al., 2012). Moderate levels of Cu have been shown to negatively affect macro-organisms, such as earthworms and plants, specifically in biomass and seed set, as well as organic matter decomposition (Moolenaar, 1998, Paoletti et al., 1998, Brun et al., 2003, Hinojosa et al., 2010). It severely decreases the functional diversity of the soil microbial community, impairs specific pathways of nutrient cycling and impacts soil fertility indicators at amounts as low as 140 mg Cu kg− 1 (Kandeler et al., 1996, Fernández-Calviño et al., 2010, Hinojosa et al., 2010, Mackie et al., 2013). For these reasons, the European Union has set a limit on the amount of copper fungicide permitted for use in agriculture at 6 kg ha− 1 y− 1 (European Commission, 2007). However, as there are currently no viable alternatives in organic agriculture (Heibertshausen et al., 2006, La Torre et al., 2007) and as the potential for infection from plant pathogens increases with climate change (Salinari et al., 2006), Cu fungicides have not been prohibited and may even increase in the future.
In response to these negative effects, one possible solution is Cu removal through in situ accumulation by plants. Phytoextraction is the use of (hyper) accumulator plants to remove metals/metalloids from the environment by taking them up into their shoots and subsequently removing them from the contaminated area (Wenzel, 2009). It is a low cost, environmentally sensitive method, which displaces Cu from the environment, but does not require full soil removal impractical in perennial agriculture and/or large tracts of land (Gómez-Sagasti et al., 2012, Meier et al., 2012a).
Particular microorganisms prefer specific plants and plant species support and encourage associated microorganisms (Terry and Bañuelos, 2000, Wardle et al., 2004, Castaldi et al., 2009, Narula et al., 2009, Epelde et al., 2010, Haferburg and Kothe, 2010). The most recent mechanism for enhancing phytoextraction is inoculating the soil with bacteria producing siderophores, which assist in chelating Cu, suggesting that microorganisms may play a significant role in successful phytoextraction (Haferburg and Kothe, 2010, Rajkumar et al., 2010). Phytoextraction, with and without inoculated microbial assistance, has been successfully investigated in laboratories and greenhouses (Poschenrieder et al., 2001, Brun et al., 2003, Kos and Leštan, 2004, Song et al., 2004, Chen et al., 2006, Meier et al., 2012b, Ma et al., 2009, Zeremski-Škorić et al., 2010, Andreazza et al., 2011). However, phytoextraction of Cu has seldom been monitored in the field (Poschenrieder et al., 2001, Clemente et al., 2005, Brej and Fabiszewski, 2006).
The aims of this study were to investigate the in situ relationship between microorganisms and plants within Cu contaminated topsoil, and identify the practicability of phytoextraction and monitor ecosystem services, such as soil health and nutrient mineralization, using microbial biomass, enzyme activity and phospholipid fatty acids (PLFAs) (Epelde et al., 2014). Enzyme activities are consistent biological indicators of heavy metal pollution and PLFA patterns have been seen to change quickly with changing soil metal concentration in as little as two weeks (Frostegård et al., 1996, Hinojosa et al., 2010, Ge and Zhang, 2011). Additionally, PLFAs identify microbial groups, which may indicate whether such groups naturally support increased phytoextraction of specific plants in situ. This project focused particularly on vineyards, a representative system of fruit production where Cu is most often applied. In vineyards with sufficient water, i.e. central Europe, cover crops grown between the vine rows have been observed to increase desirable properties in soil and vine performance (Morlat and Jacquet, 2003, Guerra and Steenwerth, 2012). Therefore, phytoextraction has the potential to improve grape production and soil fertility in vineyards, while removing Cu from the topsoil. We investigated whether (i) the efficiency of phytoextraction depends on plant species, plant community composition, distance from vine row, and growing season, (ii) if effective phytoextraction is associated with a microbial community structure, and (iii) if diverse plant communities will mitigate the negative influence of Cu on soil microorganisms.
The plants chosen within the present study were a mixture of Cu adapted plant species with high biomass production known from laboratory research as well as common vineyard cover crop species in central Europe not yet researched for Cu removal potential (Poschenrieder et al., 2001, Kos and Leštan, 2004, Andreazza et al., 2010, Haferburg and Kothe, 2010). Moreover, diverse plant systems, in comparison to monoculture systems, have been seen to reduce the impact of pollution by increasing microbial diversity and activity (Yang et al., 2007). Therefore, a treatment consisting of a mixture of plant species has also been added.
Section snippets
Study site and experimental setup
This field experiment was designed specifically to understand the in situ potential of cover crop plant species to accumulate Cu and was established at the Ithaka Institute in Canton Wallis, Switzerland (46°16′N, 7°24′E) in the spring of 2012. The study site is a vineyard planted with Pinot noir (Vitis vinifera L.) with a southeastern exposure at an elevation of 760–780 m a.s.l. The site has a mean annual precipitation of 550 mm and an average temperature of 11.4 °C. The soil is predominately
Plant copper content
Plant shoots contained varying concentrations of Cu, ranging in mean from 8.4 to 14.3 mg Cu kg− 1 DM between June 2012 and August 2012 (Fig. 1a). Treatment was highly significant (Table 1). Clover shoots had the highest Cu content (14.3 mg Cu kg− 1 DM), which was significantly more than summer mix, oat and Chenopodium. Summer mix shoots had the second highest Cu content (11.8 mg Cu kg− 1 DM), significantly more than Chenopodium. Plant Cu content increased significantly from June 2012 to August 2012.
Plant shoot biomass and plant copper removal
Plant
Copper uptake
This study is one of few that have sampled plants growing in situ for phytoextraction purposes (Clemente et al., 2005, Clemente et al., 2006, Brej and Fabiszewski, 2006). Although there is a clear distinction between the maximum plant shoot Cu content, the amount of Cu accumulated per plant shoot DM, achievable by the treatments, the quantities suggested in the literature were much higher than the quantities observed in this study. Oat has been previously researched by Andreazza et al. (2010)
Conclusion
When considering overall Cu removal capabilities, the plants with the most potential in a Wallisian vineyard were oat, hairy vetch and rye. However, the maximum removal rate, at 120 cm from the vine row, was 0.033 kg Cu ha− 1 DM y− 1. These quantities were achievable because of the plants' high biomass production and not their shoot Cu content. Winter cover crops, in particular, achieved the highest removal rates because more water was available, more nutrients were accessible and microorganisms were
Acknowledgments
We would like to thank Till Haas, Zorica Kauf, Matti Hanisch, Runa Boeddinghaus, Richard Ebner, Lisa Ebner, Felix Hegwein, and Silke Grünewald for their assistance in the field as well as Claudio Niggli for managing the field site and providing beneficial cover crop information. Thank you especially to Ibrahim Köran for his assistance in the field and in the lab and Juan Carlos Laso Bayas from the Department of Bioinformatics for his statistical consultations and assistance. We would also like
References (69)
- et al.
Bacterial stimulation of copper phytoaccumulation by bioaugmentation with rhizosphere bacteria
Chemosphere
(2010) - et al.
Approaches for enhanced phytoextraction of heavy metals
J Environ Manage
(2012) - et al.
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
(2010) - et al.
Relationships between extractable copper, soil properties and copper uptake by wild plants in vineyard soils
Environ Pollut
(1998) - et al.
Effects of elevated soil copper on phenology, growth and reproduction of five ruderal plant species
Environ Pollut
(2003) - et al.
Influence of pea and wheat growth on Pb, Cd, and Zn mobility and soil biological status in a polluted amended soil
Geoderma
(2009) - et al.
Dynamics of water and nitrogen stress along the grapevine cycle as affected by cover cropping
Eur J Agron
(2013) - et al.
Impacts of chelate-assisted phytoremediation on microbial community composition in the rhizosphere of a copper accumulator and non-accumulator
Sci Total Environ
(2006) - et al.
Uptake of heavy metals and As by Brassica juncea grown in a contaminated soil in Aznalcóllar (Spain): the effect of soil amendments
Environ Pollut
(2005) - et al.
A remediation strategy based on active phytoremediation followed by natural attenuation in a soil contaminated by pyrite waste
Environ Pollut
(2006)
Interactions between plant and rhizosphere microbial communities in a metalliferous soil
Environ Pollut
Assessment of single extractions for the determination of mobile forms of metals in highly polluted soils and sediments—analytical and thermodynamic approaches
Anal Chim Acta
Enzyme activities in vineyard soils long-term treated with copper-based fungicides
Soil Biol Biochem
Microbial biomass measured as total lipid phosphate in soils of different organic content
J Microbiol Methods
Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals
Soil Biol Biochem
Microbial community structure and enzyme activities in a sequence of copper-polluted soils
Pedosphere
Seasonal changes in the soil microbial community in a grassland plant diversity gradient four years after establishment
Soil Biol Biochem
The fumigation–extraction method to estimate soil microbial biomass: calibration of the kEC value
Soil Biol Biochem
Transient elevation of carbon dioxide modifies the microbial community composition in a semi-arid grassland
Soil Biol Biochem
Grassland plants affect dissolved organic carbon and nitrogen dynamics in soil
Soil Biol Biochem
Trace element behaviour at the root–soil interface: implications in phytoremediation
Environ Exp Bot
Chelator induced phytoextraction and in situ soil washing of Cu
Environ Pollut
Long-term plant growth legacies overwhelm short-term plant growth effects on soil microbial community structure
Soil Biol Biochem
Inoculation of plant growth promoting bacterium Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea
J Environ Manage
Remediation of copper in vineyards — a mini review
Environ Pollut
Long-term copper application in an organic vineyard modifies spatial distribution of soil micro-organisms
Soil Biol Biochem
Effects of arbuscular mycorrhizal inoculation on metallophyte and agricultural plants growing at increasing copper levels
Appl Soil Ecol
Estimation of soil microbial biomass C in the presence of living roots by fumigation–extraction
Soil Biol Biochem
Earthworms as useful bioindicators of agroecosystem sustainability in orchards and vineyards with different inputs
Appl Soil Ecol
Potential of siderophore-producing bacteria for improving heavy metal phytoextraction
Trends Biotechnol
Seasonal controls on grassland microbial biogeography: are they governed by plants, abiotic properties or both?
Soil Biol Biochem
Copper uptake by Elsholtzia splendens and Silene vulgaris and assessment of copper phytoavailability in contaminated soils
Environ Pollut
Cover crops and cultivation: impacts on soil N dynamics and microbiological function in a Mediterranean vineyard agroecosystem
Appl Soil Ecol
An extraction method for measuring soil microbial biomass C
Soil Biol Biochem
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