Impact of organic and conventional farming systems on wheat grain uptake and soil bioavailability of zinc and cadmium
Graphical abstract
Introduction
Increasing zinc (Zn) in edible plant parts is a strategic aim in agricultural systems to combat widespread Zn deficiency in human nutrition (Cakmak, 2008; Cakmak and Kutman, 2017; White and Broadley, 2011). The HarvestPlus program has set a target concentration of 38 mg kg−1 Zn in wheat grains (Bouis and Welch, 2010). In agricultural soils, the availability of soil Zn for uptake by crop plants is limited by its solubility, which is governed primarily by adsorption to mineral surfaces, complexation with organic matter and formation of precipitates (Baird and Cann, 2005; Smolders and Mertens, 2013). Due to its chemical similarity with Zn, the availability of soil cadmium (Cd) is affected in a similar manner by the same soil factors (Hart et al., 2002). However, Cd threatens human health and the environment and, thus, interactions between Zn and Cd availability and uptake should be carefully monitored. In particular, the availability of Zn and Cd in the soil is dependent on soil organic matter (SOM), oxides, clay particles, and pH (Schulin et al., 2009; Smolders and Mertens, 2013). The affinity of Zn and Cd for sorption on soil particles can be >10 times higher on organic matter than on mineral particles (Lair et al., 2007b). As agricultural practises can have a major impact on SOM and soil pH (Bolan et al., 2001; Six et al., 2000), it is important to understand how they influence available Zn and Cd concentrations in agricultural soils. For food safety reasons it is especially important to relate soil Zn and Cd to their uptake by wheat grains to determine how availability translates into the edible parts of crop plants. Previous studies showed that for some cultivars the Zn and Cd accumulation in grains might be more strongly affected by soil properties than others (Gao et al., 2011) whereas the different soil properties of sites had a higher impact than crop cultivars (Oliver et al., 1995; Wångstrand et al., 2007).
Various studies investigated how organic compounds affect Zn and Cd uptake by crop plants. In a hydroponic experiment, the addition of citrate and histidine increased Zn uptake of wheat due to soluble complex formation of Zn with these organic acids, comparing nutrient solutions with the same free Zn concentration (Gramlich et al., 2013). Soil microorganisms can increase soil Zn availability by exuding organic ligands (Altomare and Tringovska, 2011). Mycorrhizal plants were observed to have more Zn available, while Cd toxicity was reduced due to a potential discrimination of the arbuscular mycorrhiza between Zn and Cd (Janoušková et al., 2006). These greenhouse and pot experiments provided important insights, however, the impact of SOM management on Zn and Cd availability remains elusive in real farm environments.
In addition to the complexation by organic ligands and sorption at organic matter surfaces, Zn and Cd can also be sorbed and complexed at mineral surfaces like clay minerals or (hydr-)oxides (Fonseca et al., 2011; Sipos et al., 2008). Organo-mineral associations were shown to provide important interfaces for the binding of heavy metals and can be prominent factors for the binding and mobilisation of soil Zn and Cd (Arias et al., 2005; Leinweber et al., 1995).
The addition of fertilisers or amendments containing organic matter can enrich soils with heavy metals due to metal contents of the applied materials exceeding natural inputs (Facchinelli et al., 2001). Animal feed is supplemented with Zn to improve animal health and livestock productivity and the majority of the supplemented Zn is not retained by the animals and excreted (Bolan et al., 2004; Gubler et al., 2015; Schultheiß et al., 2004). The heavy metal concentrations in manure vary depending on the farming system and the feed and supplements used (Keller et al., 2002; Menzi and Kessler, 1998; Menzi et al., 1999; Möller and Schultheiß, 2015). In German dairy production, on-farm grown fodder introduced 39% of the added Zn and 71% of the Cd into cow sheds, whereas protein-rich external feed accounted for a similar range of Zn and much less Cd (Schultheiß et al., 2004). In addition, the recycling of plant residues and land management was found to influence metal dynamics and plant uptake (Düring et al., 2003; Mench, 1998; Oliver et al., 1993). While many studies have looked at the on-farm flows of heavy metals in livestock production, only a few studies have investigated to what extent heavy metals are retained and mobilised in agricultural soils (Helfenstein et al., 2016).
In this study, we investigated how agricultural cropping and livestock production systems influence Zn and Cd concentrations in wheat grains and how these effects relate to soil Zn and Cd availability and other soil factors. We sampled soils and wheat grains on farms in northern Switzerland categorised in three differing farming systems, with and without livestock production: organic farms with compost use, organic farms without compost use, and conventional farms without compost use. The objectives of the study were (i) to relate total and available soil Zn and Cd concentrations to wheat grain Zn and Cd concentrations and (ii) to assess the role of management practices and soil properties in these relationships.
Section snippets
Study site and farm characteristics
The 28 farms included in this survey were located at elevations between 340 and 954 m above sea level around Zurich in northern Switzerland (Fig. 1). The sampled soils were Cambisols (WRB) with an average clay-sized particle content of 25 ± 1.2% and a range of 16–41%. The sampled soils did not significantly differ in texture, cation exchange capacity (CEC), pH, and bulk density between the three farming systems we distinguished in this study. The climate is temperate and humid. The annual mean
Farm system properties
The conventional farms showed a more intense livestock production on average, as indicated by a tendency towards higher livestock density and concentrate feed density (Table 1). The organic C input on the organic farms with compost use averaged 4.8 times that of conventional farms during the analysed wheat year (Table 1). Over the whole crop rotation, the average input of organic C increased in the order CON < ORG < COMP but there was no significant difference between the farming systems (Table
Soil concentrations of Zn and Cd
The positive correlations of total soil Zn and Cd with SOC concentration and CEC suggest that organic matter was a major factor in providing binding capacity for Zn and Cd retention in the analysed agricultural fields, which is in line with previous sorption experiments (Lair et al., 2006). The clay content also correlated positively with CEC but had a lower correlation coefficient with total soil Zn and Cd so the clay content was probably less important for total soil Zn and Cd than organic
Conclusion
Organic matter mainly mediated the soil Zn and Cd concentrations in the analysed Swiss wheat farms. Accordingly, organic farms with compost use with a raised SOC concentration and CEC revealed higher soil and grain Cd contents than conventional farms explained by a combination of compost application, livestock production, and a cultivar effect. This increased Cd binding sites, biocycling of Cd within the farm and potentially also available Cd inputs that were taken up by wheat grain. The soil
Acknowledgements
We thank the Mercator foundation and the World Food System Center for financial support for the project “Zinc Biofortification of Wheat through Organic Matter Management in Sustainable Agriculture” (ZOMM) of which this was part. MvdH and BS acknowledge funding from the Mercator foundation for the project 2015-0393 “Carbon Storage and Resource Use Efficiency for a Sustainable Agriculture”. We are also very thankful to the participating farmers for their great cooperation and Roman Grüter for his
References (64)
- et al.
Adsorption and desorption of copper and zinc in the surface layer of acid soils
J. Colloid Interface Sci.
(2005) - et al.
Total and available soil trace element concentrations in two Mediterranean agricultural systems treated with municipal waste compost or conventional mineral fertilizers
Chemosphere
(2010) - et al.
An inventory of trace elements inputs to French agricultural soils
Sci. Total Environ.
(2012) - et al.
Sorption and bioavailability of heavy metals in long-term differently tilled soils amended with organic wastes
Sci. Total Environ.
(2003) - et al.
Multivariate statistical and GIS-based approach to identify heavy metal sources in soils
Environ. Pollut.
(2001) - et al.
Mobility of Cr, Pb, Cd, Cu and Zn in a loamy sand soil: a comparative study
Geoderma
(2011) - et al.
Grain cadmium and zinc concentrations in wheat as affected by genotypic variation and potassium chloride fertilization
Field Crop Res.
(2011) - et al.
Green manure and long-term fertilization effects on soil zinc and cadmium availability and uptake by wheat (Triticum aestivum L.) at different growth stages
Sci. Total Environ.
(2017) - et al.
Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil
Chemosphere
(2006) - et al.
Heavy metals in source-separated compost and digestates
Waste Manag.
(2014)
Monitoring of cadmium in the chain from soil via crops and feed to pig blood and kidney
Ecotoxicol. Environ. Saf.
Cadmium availability to plants in relation to major long-term changes in agronomy systems
Agric. Ecosyst. Environ.
Competitive sorption of cadmium and zinc in contrasting soils
Geoderma
Heavy metal contents of livestock feeds and animal manures in England and Wales
Bioresour. Technol.
The transportation and accumulation of arsenic, cadmium, and phosphorus in 12 wheat cultivars and their relationships with each other
J. Hazard. Mater.
Cadmium and zinc accumulation in soybean: a threat to food safety?
Sci. Total Environ.
Sorption of copper, zinc and lead on soil mineral phases
Chemosphere
Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture
Soil Biol. Biochem.
Cadmium concentration in winter wheat as affected by nitrogen fertilization
Eur. J. Agron.
Green manure addition to soil increases grain zinc concentration in bread wheat
PLoS One
Beneficial soil microorganisms, an ecological alternative for soil fertility management
Levels of cd and some other trace elements in soils and crops as influenced by lime and fertilizer level
Acta Agric. Scand.
Associations of cadmium, zinc, and lead in soils from a lead and zinc mining area as studied by single and sequential extractions
Environ. Monit. Assess.
Environmental Chemistry
Trace element changes in soil after long-term cattle manure applications
J. Environ. Qual.
Soil acidification and liming interactions with nutrientand heavy metal transformationand bioavailability
Adv. Agron.
Distribution and bioavailability of trace elements in livestock and poultry manure by-products
Crit. Rev. Environ. Sci. Technol.
Biofortification—a sustainable agricultural strategy for reducing micronutrient malnutrition in the global south
Crop Sci.
Enrichment of cereal grains with zinc: agronomic or genetic biofortification?
Plant Soil
Agronomic biofortification of cereals with zinc: a review
Eur. J. Soil Sci.
Molecular mechanisms of plant metal tolerance and homeostasis
Planta
Competitive adsorption of heavy metals by soils
J. Environ. Qual.
Cited by (28)
Cadmium, zinc, and copper leaching rates determined in large monolith lysimeters
2024, Science of the Total EnvironmentCadmium-tolerant facultative endophytic Rhizobium larrymoorei S28 reduces cadmium availability and accumulation in rice in cadmium-polluted soil
2022, Environmental Technology and InnovationCitation Excerpt :Cd uptake and transport in rice is an ecological issue of global concern. Metal bioavailability in soil affects metal accumulation in plants (Schweizer et al., 2018). In situ metal immobilization is an effective method for contaminated soil remediation (Li et al., 2016; Etesami, 2018; Xiong et al., 2019).
Soil organic carbon is affected by organic amendments, conservation tillage, and cover cropping in organic farming systems: A meta-analysis
2021, Agriculture, Ecosystems and EnvironmentLong-term effects of intensive application of manure on heavy metal pollution risk in protected-field vegetable production
2020, Environmental PollutionCitation Excerpt :Continuous and high application rates of manure increased soil available Cd, Zn, and Cu in comparison with lower manure application rates (Fig. 2). This is similar to a previous study conducted on an organic farm that used manures, where in total soil and available Cd concentrations were found to be significantly higher than those on conventional farms (Schweizer et al., 2018). Additionally, it was also found that soil available Cd and Zn increased by the application of aerobically composted farmyard manure and slurry in a long-term experiment (Grüter et al., 2019).
The presence of zinc reduced cadmium uptake and translocation in Cosmos bipinnatus seedlings under cadmium/zinc combined stress
2020, Plant Physiology and Biochemistry
- 1
Present address: Sustainable Agricultural Sciences North Wyke, Rothamsted Research, North Wyke, Devon, EX20 2SB, United Kingdom.