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Article

The Content, Uptake and Bioaccumulation Factor of Copper and Nickel in Grass Depending on Zinc Application and Organic Fertilization

by
Beata Kuziemska
*,
Andrzej Wysokinski
and
Paulina Klej
Faculty of Agrobioengineering and Animal Husbandry, Institute of Agriculture and Horticulture, Siedlce University of Natural Sciences and Humanities, 08110 Siedlce, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(9), 1676; https://doi.org/10.3390/agriculture13091676
Submission received: 3 July 2023 / Revised: 25 July 2023 / Accepted: 23 August 2023 / Published: 25 August 2023
(This article belongs to the Special Issue Agricultural Environmental Pollution, Risk Assessment, and Control)
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Versions Notes

Abstract

:
Different content of Zn in the soil and organic fertilization can affect micronutrient uptake by plants. A pot experiment was carried out to determine the impact of increasing Zn application rates, i.e., 200, 400 and 600 Zn mg·kg−1, in combination with bovine and chicken manures and mushroom substrate on Cu and Ni content, uptake and bioaccumulation factor in cocksfoot (Dactylis glomerata L.). Control objects without Zn and organic fertilizers and after application of only different Zn doses and only organic fertilizers were also tested. Application of Zn at 400 and 600 mg·kg−1 significantly decreased the content, uptake and value of bioaccumulation factor of Cu in the grass. Different Zn doses were not found to influence the content and bioaccumulation factor of Ni in cocksfoot, but application at 200 Zn mg·kg−1 increased Ni uptake. Chicken manure increased the content and bioaccumulation factor of Cu and Ni in the test plant, and all the organic fertilizers increased their uptake. Cocksfoot showed no tendency to excessive bioaccumulation of Cu and Ni.

1. Introduction

To obtain high yields of good quality in agricultural production, it is necessary not only to provide an adequate supply of macroelements to crop plants, but to meet their demand for microelements as well. Essential microelements in plant nutrition include Zn, Cu, Ni and others (e.g., B, Fe, Mn, Mo) [1,2,3]. Their source for plants can be mineral and organic fertilizers or waste substances used in fertilization and industrial human activity [4]. However, taken up by plants in excessive amounts, these metals can have toxic effects, disturbing metabolic processes and decreasing yields [5,6,7,8].
Zn is a catalytic and structural cofactor of many enzymes, influencing the activity of enzymes such as hydrogenase and carbonic anhydrase [9,10]. It also performs crucial structural functions in the domains of proteins which interact with other molecules [11,12]. In addition, Zn increases crop resistance to drought [13]. Zn deficiency inhibits the activity of enzymes involved in photosynthesis [14] and also reduces accumulation of amino acids and protein synthesis. An excessive amount of this metal inhibits photosynthesis and chlorophyll biosynthesis, resulting in reduced whole mass of plants [15,16].
Cu is a catalyst in respiration and photosynthesis and plays an important role in hormonal signalling and cell wall metabolism [17,18]. Cu ions are cofactors in many enzymes, e.g., cytochrome c oxidase, Cu/Zn superoxide dismutase (SOD), amine oxidase, polyphenol oxidase, plastocyanin and laccase [19]. Cu deficiency disturbs metabolism, reduces stress resistance, damages enzyme systems and, in effect, reduces yields [20]. At high concentrations in tissues, Cu inhibits plant growth, disturbs photosynthetic electron transport and causes chlorosis, necrosis and dwarfism [21,22].
Ni is an element that activates urease, which catalyses hydrolysis of urea in plants [23,24]. It is also a component of other metalloenzymes, such as NiFe hydrogenase, superoxide dismutase, carbon monoxide dehydrogenase, methyl-coenzyme M reductase, hydrogenase and RNase A, acetyl-coenzyme-A synthase. Ni deficiency reduces urease activity, disturbs N assimilation and limits scavenging of superoxide free radicals. Excessive amounts of this metal adversely affect nutrient absorption by the roots, disturb plant metabolism, and inhibit photosynthesis and transpiration [25,26].
The uptake of heavy metals into plants’ roots occurs mainly through two pathways: the apoplastic pathway (passive diffusion) and the symplastic pathway (active transport against electrochemical potential gradients and concentrations across the plasma membrane [27]. Uptake of Zn, Ni and Cu by plants depends on numerous soil factors, including pH, content of organic matter, redox conditions and the antagonistic or synergistic interactions between these elements [28,29].
Studies carried out by many researchers have shown that nearly half of the arable soils in the world have a low content of available Zn, resulting in a deficiency of this element in crop plants [2,28,30,31,32,33]. Application of this microelement in the form of mineral and organic fertilizer is the most practical means of preventing the effects of its deficiencies [34]. However, a high content of Zn in the soil may reduce its biological activity and cause the accumulation of this metal in plants [8]. At the same time, it can reduce the uptake of other elements by plants, in relation to which it is an antagonist. In such conditions, the organic fertilizers used may be a source of, e.g., Cu and Ni for plants.
The presented studies show that the content of zinc in Polish soils may range from 12 to 632 mg Zn·kg−1 of soil, which was taken into account when determining its doses in the experiment [35]. Therefore, a study was undertaken to determine the impact of varied levels of Zn applied together with organic materials, e.g., bovine and chicken manures or mushroom substrate, on the content, uptake and bioaccumulation factor of Cu and Ni in cocksfoot.
Grasses occupy a special place among fodder crops. When adequately fertilized, they have high yield potential for dry matter, protein and carbohydrates. Cocksfoot is one of the most important fodder crops in Europe and in the world [36,37]. It attains high yields and is disease-resistant [36], as well as highly resistant to drought [38]. Due to its high quality as fodder, it is used for production of hay and silage and for grazing [36]. The National List of varieties in Poland includes eight cocksfoot cultivars: Amera, Bepra, Berta, Crown Royale, Dika, Minora, Trerano and Tukan [39]. The Amera cultivar, the test plant in the present study, is the earliest variety of cocksfoot, with early onset of growth, a high rate of spring growth and rapid regrowth. It produces high yields of palatable and digestible biomass.
It was hypothesized that increasing doses of Zn reduce the content and bioaccumulation factor of Cu and Ni in cocksfoot, while organic fertilization causes their increase.

2. Materials and Methods

2.1. Experimental Design

A pot experiment was carried out in the years 2014–2016 in a greenhouse in Siedlce (52°10′ N, 22°17′ E, 155 m a.s.l.).
Pots with a capacity of 10 L were filled with 12 kg of soil. The soil was Luvisols consisting of 71% sand, 24% silt and 5% clay.
The experiment was planned in a randomized design in triplicate, with two factors:
I—Zn application amount
II—organic fertilizer.
The experimental design is shown in Table 1.
Zn and organic fertilizer were applied once, only in the first year of the study, two weeks before sowing of the grass. Zn was applied as an aqueous solution of ZnSO4·5H2O. Organic fertilizers were applied in amounts that introduced 2 g Corg·kg−1 to the soil. In three years of the study, the test plant was the grass cocksfoot (Dactylis glomerata L.), the Amera cultivar, which was sown in the first decade of May of each year. The green parts of the grass were collected every 30 days, four times a year. During the growing period, the soil moisture in the pots was kept at 60–70% of the total water capacity.

2.2. Laboratory Analyses

2.2.1. Soil

Before starting the experiment, the soil was analysed for pH by potentiometric titration in 1 mol·dm−3 of KCl solution [40]; organic C by a modification of the Tyurin method [41]; total N content by CHNS (automatic CHN analyser with an IDC detector, Series II 2400, Perkin-Elmer, Valencia, CA, USA); and content of total K, P, Zn, Cu and Ni by ACP-AES (Optima 3200 RL spectrometer, Perkin-Elmer, Waltham, MA, USA), following wet mineralization in a mixture of concentrated HCl and HNO3 (3:1 ratio) [42]. Available K and P were determined by the Egner–Riehm method [43]. Selected properties of soil are shown in Table 2.

2.2.2. Organic Fertilizers

The organic materials used in the experiment (bovine and chicken manures and mushroom substrate) were analysed for dry matter (DW at 105 °C) organic C by the Tyurin method [41]; total N content by CHNS; and content of P, K, Zn, Cu and Ni by ICP-AES following dry mineralization of the samples at 500 °C [42]. The results of the chemical analyses are given in Table 3.
The contents of dry matter, total N and K were highest in the mushroom substrate, organic C content was highest in the bovine manure, and the contents of P, Zn, Cu and Ni were highest in chicken manure.

2.2.3. Plant Material

The aerial parts of cocksfoot were analysed for content of Cu and Ni by inductively coupled plasma atomic emission spectroscopy (ICP-AES). Prior to the analysis, the samples were subjected to dry mineralization at 450 °C and dissolved in 10% HCl solution [44].

2.3. Calculations

Uptake of Cu and Ni by cocksfoot was calculated according to the formulas given by Bokhari et al. [45]:
CuUP = Y × Cuplant/1000,
where:
CuUP—Cu uptake by grass (accumulation), Cu mg·pot−1
Y—yield of grass, g·pot−1
Cuplant—Cu content in grass, Cu mg·kg−1.
NiUP = Y × Niplant/1000,
where:
NiUP—Ni uptake by grass (accumulation), Ni mg·pot−1
Y—yield of grass, g·pot−1
Niplan—Ni content in grass, Ni mg·kg−1.
In addition, the bioaccumulation factor of Cu and Ni [46,47] was calculated according to the following formulas:
BFCu = Cuplant/Cusoil,
where:
BFCu—Bioaccumulation factor of Cu
Cuplant—Cu content in grass, Cu mg·kg−1
Cusoil—total Cu content in the soil, Cu mg·kg−1
BFNi = Niplant/Nisoil,
where:
BFNi—Bioaccumulation factor of Ni
Niplant—Ni content in grass, Ni mg·kg−1
Nisoil—total Ni content in the soil, Ni mg·kg−1.

2.4. Statistical Analysis

The content, uptake and bioaccumulation factor obtained in subsequent years of the experiment were analysed by analysis of variance using Statistica 13 PL software (ver. 13.1, StatSoft, Tulsa, OK, USA).
yijk = µ + ai + bj + ck + abij +acik + bcjk + abcijk + eijkp
where µ—mean from all treatments; ai—effect of Zn level; bj—effect of organic fertilizer type; ck—effect of year (third source of variation); abij—interaction of Zn level and fertilizer type; acik—interaction of Zn level and year; bcjk—interaction of fertilizer type and year; abcijd—interaction of Zn level and fertilizer type and year; eijkp—sampling error.
The total Cu and Ni uptake over a period of 3 years was also calculated in this application according to the equation:
yijk = µ + ai + bj + abij + eijp
where µ—mean from all treatments; ai—effect of Zn level; bj—effect of organic fertilizer type; abij—interaction of Zn level and fertilizer type; eijp—sampling error.
The significance of the experimental factors was determined on the basis of the Fisher–Snedecor distribution. Least significant difference (LSD) values were calculated by Tukey’s test. The calculations were performed for a significance level of p = 0.05. In addition, Pearson’s linear correlation coefficient was calculated.

3. Results

The content of Cu in the biomass of cocksfoot ranged from 2.35 to 5.24 mg·kg−1 DM (on average, 3.34 Cu mg·kg−1 DM) (Table 4). It was significantly reduced by application of Zn at 400 and 600 mg·kg−1, by 10.6% and 12.0%, respectively, relative to the control. The content of Cu in the grass was not significantly affected by application of 200 Zn mg·kg−1, bovine manure or mushroom substrate. The highest content of this metal was noted in the cocksfoot fertilized with chicken manure; it was 32.5% higher than in the plants from the control treatment and 24.2% and 28.2% higher, respectively, than following application of mushroom substrate and bovine manure. The Cu content in the biomass of the grass significantly decreased in successive years of the experiment. In the second and third years, it was 7.8% and 31.7% lower, respectively, than in the first year of the experiment.
All experimental factors also significantly influenced Cu uptake by cocksfoot, calculated as the mean from the three years of the experiment (Table 5) and the total for the 3-year cycle (Figure 1 and Figure 2). In the first year of the study, Cu accumulation was highest following application of 200 Zn mg·kg−1 and lowest following application of 600 Zn mg·kg−1. In the subsequent years of the experiment, increasing application of Zn did not significantly affect Cu uptake by the test plant. The organic fertilizers, irrespective of their origin, increased Cu uptake by cocksfoot. In all years of the study, its accumulation by the plants was significantly the highest following application of chicken manure. Cu uptake by the grass decreased in successive years. In the second and third years of the experiment, it was 57.0% and 31.4%, respectively, of the amount taken up in the first year.
Ni content in tested grass ranged from 1.34 to 6.40 Ni mg·kg−1 DM (on average, 3.20 Ni mg·kg−1 DM) and did not depend on the amount of Zn applied to the soil (Table 6). It was significantly increased by application of chicken manure, but only in the first year of the study. Mushroom substrate and bovine manure were not shown to significantly influence this parameter. The content of Ni in grass significantly decreased in successive years of the experiment. In the second and third years of the experiment, it was 43.1% and 62.7% lower, respectively, than in the first year.
Uptake of Ni by cocksfoot, calculated as the mean from the 3 years of the study (Table 7) and the total for the 3-year cycle (Figure 3 and Figure 4), was significantly dependent on the level of Zn applied to the soil, organic fertilizer, and the year of the experiment. In the 3-year cycle, following application of Zn at 200 mg·kg−1 of soil, the plants accumulated 13.7% more Ni than the plants from the control treatment and 14.4% and 27.5% more, respectively, than following application of 400 and 600 Zn mg·kg−1. No significant differences were noted in accumulation of Ni in the plants from the treatments without Zn application or with application at 400 and 600 Zn mg·kg−1. Bovine and chicken manures and mushroom substrate increased uptake of nickel by the grass by 63.2%, 107.2% and 39.6%, respectively, relative to the control treatment. Significantly, the highest uptake of this metal was noted following application of chicken manure. It was 105.5% higher than in the control plants and 20.4% and 42.7% higher, respectively, than following application of bovine manure and mushroom substrate. During the three years of the experiment, Ni uptake by grass was highest in the first year and lowest in the third year. Uptake in the second and third year was 34.5% and 15.0%, respectively, of the level of uptake in the first year.
The application of 400 and 600 Zn mg·kg−1 reduced the factor of Cu bioaccumulation in cocksfoot (Figure 5). There was no significant effect of all doses of Zn on the bioaccumulation factor of Ni in this grass.
Mushroom substrate and bovine manure did not significantly change the bioaccumulation factor of Cu and Ni, whereas chicken manure increased its value (Figure 6).
In the subsequent years of the study, the bioaccumulation factor of Cu and Ni decreased (Figure 7).
The correlation coefficients showed no clear effect of increasing Zn application (200, 400 and 600 Zn mg·kg−1) on the content and uptake of Cu and Ni by grass (Table 8). They also showed no significant relationship between the content of these two metals and the content of Zn in the grass given by Kuziemska et al. [48]. At the same time, they indicated a significant relationship between the uptake and content of Cu and Ni and the yield of this plant reported in the study cited above.

4. Discussion

The biological value of crops is influenced not only by their content of macronutrients and microelements, but also by their proportions. Interactions between elements in crops occur when the supply of one element affects the absorption and use of other elements. Interaction of this type is most common when one element is present in the soil in excessive amounts. Antagonistic and synergistic relationships between plant nutrients cause disturbances in their chemical composition. According to Rietra et al. [49], knowledge of the interactions between nutrients can help to optimize fertilization strategies to achieve high yields of good biological value.
In the present study, the average Cu content in the cocksfoot biomass was 3.34 Cu mg·kg−1 DM. Łukowski et al. [50] reported content of this metal ranging from 2.2 to 21 Cu mg·kg−1 DM in various grass species cultivated in Poland. In a study by Gawryluk et al. [51], the average Cu content in grasses ranged from 8.6 to 16.2 Cu mg·kg−1 DM. Zn application at 400 and 600 mg·kg−1 reduced Cu content, uptake and bioaccumulation factor in cocksfoot. Decreases in Cu content is indicative of antagonistic relationships between these metals. Chaudhry et al. [52] investigated the effect of various levels of application of Zn and Cu on their uptake by rice (Oryza sativa L.) and rice yield. They showed that Zn application reduced the content of Cu in the biomass of the plant. Similar tendencies were obtained by Imtiaz et al. [53] for the relationship between Zn and Cu. In a pot experiment, they tested the effect of increasing Zn application (0, 5, 10, 15 and 20 Zn mg·ml−1) on the content of Cu in wheat. The authors found that Zn, irrespective of the rate of application, decreased the content of Cu in the test plant. Zhao et al. [54] tested the effect of Zn, Mn and Cu on plant growth and accumulation of these elements in Phytolacca americana. They showed that excessive Zn application leads to chlorosis, disturbs elemental homeostasis and reduces the Cu concentration in the plant. Antagonistic relationships between Zn and Cu have also been reported by Abou Seeda et al. [3], Mousavi et al. [55] and Liščáková et al. [56].
Contrasting results for the interrelationships between Zn and Cu were obtained by Malinowska et al. [57], who tested the content of these metals in selected plants growing along a motorway. They found no significant correlations between their content in the plants. The results obtained by the cited authors and the results of our own research indicate that the relationship between the content of Zn and Cu in plants probably depends on their species.
The present study showed no significant effect of bovine manure or mushroom substrate on the content and bioaccumulation factor of Cu by cocksfoot. Application of chicken manure, with which the largest quantity of this metal was applied to the soil, significantly increased its content in the biomass of the grass. In addition, all of the organic fertilizers increased Cu uptake by the test plant. Sumner [58] and Wuana and Okieimen [59] described bovine manure and chicken manure as potential sources of Cu for plants. At the same time, Wuana and Okieimen [59] reported that Cu is added to livestock fodder as a growth promoter, which may result in an increase in its content in animal waste and in the biomass of fertilized crops. Velusami et al. [60] tested the fertilizer value of mushroom substrates and showed that they are a valuable source of macro- and microelements, including Cu, for plants. The correlation coefficients indicate that the increase in Cu accumulation by cocksfoot under the influence of chicken manure, bovine manure and mushroom substrate is associated with stimulation of yield by these fertilizers, discussed in a previous paper [48].
The average content of Ni in cocksfoot was 3.20 Ni mg·kg−1 DM. Wowkowicz et al. [61] tested the content of heavy metals in crops grown on permanent grassland in the vicinity of Warsaw. The Ni content in the grasses ranged from 0.8 to 2.28 Ni mg·kg−1 DM. Contrasting results were presented by Łukowski et al. [50], who found highly varied content of this metal in fodder grasses, ranging from 4.55 to 39.60 Ni mg·kg−1 DM.
The present study showed no significant effect of increasing soil application of Zn (200, 400 and 600 Zn mg·kg−1) on the content and bioaccumulation factor of Ni in the biomass of cocksfoot. The results do not indicate an interaction between Zn and Ni. Previous studies also showed no antagonistic or synergistic relationships between these metals in cocksfoot cultivation [62,63]. Contrasting results were obtained by Dalir et al. [64], who studied the relationship between the uptake of Zn and Ni by spring wheat grown in a water medium containing varied concentrations of both metals. The authors found that the interactions were dependent on their content in the medium. Zn at low concentrations did not affect Ni uptake, but higher Zn content in the medium reduced Ni uptake by wheat. Antagonistic relationships between Zn and Ni in cultivation of Arabidopsis thaliana (L.) were also reported by Nishida et al. [65]. At the same time, application of 200 Zn mg·kg−1 soil caused a significant increase in the uptake of Ni in the test plant. Analysis of the correlation coefficients indicates that this is linked to the increase in the yield of cocksfoot.
In our study, the highest amount of Ni was applied to the soil with chicken manure, which caused a significant increase in its content and bioaccumulation factor in the cocksfoot biomass. Earlier research on the chemical composition of selected organic fertilizers (pig, bovine and chicken manure) showed that chicken manure was the best source of Ni for plants [66]. The organic fertilizers, irrespective of their origin, increased uptake of this metal by the test plant. Analysis of the correlation coefficients indicates that this is directly linked to their positive effect on the yield of cocksfoot. The values of the bioaccumulation factor provide information about the ability of plants to absorb elements from the soil. In research conducted by Łukowski et al. [50], the average bioaccumulation factor of Cu and Ni in Polish grasses was 0.8 and 1.8, respectively. Small values (much lower than 1) of this factor for Cu and Ni obtained in our own research indicate that cocksfoot does not tend to excessive accumulation of these heavy metals [46].

5. Conclusions

Zn applied to the soil at 200 mg·kg−1 did not influence the content, uptake and bioaccumulation factor of Cu in cocksfoot, whereas higher application rates—400 and 600 Zn mg·kg−1—significantly reduced them. Decrease in the copper content indicates antagonistic relationships between Zn and Cu. Application of Zn, irrespective of the application rate, did not affect the content and bioaccumulation factor of Ni in the grass, but it increased its uptake at 200 Zn mg·kg−1, as a result of increasing the yield. Bovine manure and mushroom substrate did not affect the contents and bioaccumulation factor of Cu or Ni in the grass. The chicken manure application, with which the largest amount of Cu and Ni was introduced, resulted in a significant increase in their content and bioaccumulation coefficient in tested grass. All of the organic fertilizers increased the uptake of Ni and Cu by the biomass of the test grass. Uptake of both of these metals was highest in the grass fertilized with chicken manure. Low values of bioaccumulation factors of Cu and Ni indicate a low potential of cocksfoot for their excessive accumulation.

Author Contributions

Conceptualization, B.K., A.W. and P.K.; methodology, B.K., P.K. and A.W.; resources, B.K., P.K. and A.W.; writing—original draft preparation, B.K. and A.W.; writing—review and editing, B.K. and A.W.; visualization, A.W. and B.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Polish Ministry of Science and Higher Education, grant numbers 314/12/S, 105/14/MN and 158/23/B.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Agriculture 13 01676 g001
Figure 1. Total Cu uptake by grass in three years (Cu mg·pot–1)—variability caused by different organic fertilizers. CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c,d—means investigated factors with different letters are significantly different.
Figure 1. Total Cu uptake by grass in three years (Cu mg·pot–1)—variability caused by different organic fertilizers. CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c,d—means investigated factors with different letters are significantly different.
Agriculture 13 01676 g001
Agriculture 13 01676 g002
Figure 2. Total Cu uptake by grass in three years (Cu mg·pot–1)—variability caused by different zinc doses. a,b—means investigated factors with different letters are significantly different.
Figure 2. Total Cu uptake by grass in three years (Cu mg·pot–1)—variability caused by different zinc doses. a,b—means investigated factors with different letters are significantly different.
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Agriculture 13 01676 g003
Figure 3. Total Ni uptake by grass in three years (Ni mg·pot–1)—variability caused by different organic fertilizers. CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c,d—means investigated factors with different letters are significantly different.
Figure 3. Total Ni uptake by grass in three years (Ni mg·pot–1)—variability caused by different organic fertilizers. CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c,d—means investigated factors with different letters are significantly different.
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Agriculture 13 01676 g004
Figure 4. Total Ni uptake by grass in three years (Ni mg·pot–1)—variability caused by different zinc doses. a,b—means investigated factors with different letters are significantly different.
Figure 4. Total Ni uptake by grass in three years (Ni mg·pot–1)—variability caused by different zinc doses. a,b—means investigated factors with different letters are significantly different.
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Agriculture 13 01676 g005
Figure 5. Bioaccumulation factor of Cu and Ni in grass—variability caused by different zinc doses. a,b for Cu—means investigated factors with different letters are significantly different.
Figure 5. Bioaccumulation factor of Cu and Ni in grass—variability caused by different zinc doses. a,b for Cu—means investigated factors with different letters are significantly different.
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Agriculture 13 01676 g006
Figure 6. Bioaccumulation factor of Cu and Ni in grass—variability caused by different organic fertilizers. CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b for Cu and A,B for Ni—means investigated factors with different letters are significantly different.
Figure 6. Bioaccumulation factor of Cu and Ni in grass—variability caused by different organic fertilizers. CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b for Cu and A,B for Ni—means investigated factors with different letters are significantly different.
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Agriculture 13 01676 g007
Figure 7. Bioaccumulation factor of Cu and Ni in grass—variability caused by years of study. a,b,c for Cu and A,B,C for Ni—means investigated factors with different letters are significantly different.
Figure 7. Bioaccumulation factor of Cu and Ni in grass—variability caused by years of study. a,b,c for Cu and A,B,C for Ni—means investigated factors with different letters are significantly different.
Agriculture 13 01676 g007
Table 1. Design of the pot experiment.
Table 1. Design of the pot experiment.
Organic FertilizerDose of Zn [mg∙kg−1 of Soil]
0200400600
Without organic fertilization (CO)1234
Bovine manure (BM)5678
Chicken manure (ChM)9101112
Mushroom substrate (MS)13141516
1—no organic fertilizer and without Zn applied; 2—200 mg Zn; 3—400 mg Zn; 4—600 mg Zn; 5—only BM; 6—BM + 200 mg Zn; 7—BM + 400 mg Zn; 8—BM + 600 mg Zn; 9—only ChM; 10—ChM + 200 mg Zn; 11—ChM + 400 mg Zn; 12—ChM + 600 mg Zn; 13—only MS; 14—MS + 200 mg Zn; 15—MS + 400 mg Zn; 16—MS + 600 mg Zn.
Table 2. Some soil properties before the start of the experiment.
Table 2. Some soil properties before the start of the experiment.
pHKClCorganicNtotalPtotalKtotalPavailableKavailableCutotalZntotalNitotal
g∙kg−1mg∙kg−1
6.6516.401.520.521.2217610813.5056.609.85
Table 3. Chemical composition of organic fertilizers.
Table 3. Chemical composition of organic fertilizers.
Organic FertilizersDry Matter (%)CorganicNPKCuZnNi
g∙kg−1 DMmg∙kg−1 DM
BM19.6405.123.905.3815.285.9760.2811.16
ChM27.8167.313.508.449.3242.98190.8032.15
MS30.4319.324.206.2217.4815.61117.5011.20
BM—bovine manure, ChM—chicken manure, MS—mushroom substrate.
Table 4. Cu content in grass biomass (Cu mg·kg−1 DM).
Table 4. Cu content in grass biomass (Cu mg·kg−1 DM).
Organic FertilizersYearsDoses of Zn [mg∙kg−1]Means
0200400600
CO1st3.683.443.243.433.44
2nd3.423.293.153.013.22
3rd2.462.432.352.352.40
means3.183.052.912.933.02 a
BM1st4.123.983.753.363.80
2nd3.663.383.253.233.38
3rd2.542.502.402.462.48
means3.443.293.133.023.22 a
ChM1st5.244.964.144.084.61
2nd4.724.264.083.864.23
3rd3.383.123.003.153.16
means4.454.113.743.704.00 b
MS1st3.853.613.413.283.54
2nd3.573.403.263.183.35
3rd2.502.492.452.472.48
means3.313.173.042.983.12 a
Means for Zn dose3.59 b3.41 ab3.21 a3.16 a3.34
Means for years1st4.224.003.643.543.85 c
2nd3.843.583.443.323.55 b
3rd2.722.642.552.612.63 a
CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c—means investigated factors with different letters (in the columns for organic fertilization and for years but in the row for Zn doses) are significantly different.
Table 5. Cu uptake by grass (Cu mg·pot−1).
Table 5. Cu uptake by grass (Cu mg·pot−1).
Organic FertilizersYearsDoses of Zn [mg∙kg−1 ]Means
0200400600
CO1st0.0560.0630.0420.0400.050 C
2nd0.0420.0370.0280.0380.036 B
3rd0.0220.0200.0180.0190.020 A
means0.0400.0400.0290.0320.035 a
BM1st0.1040.1160.0990.0710.098 C
2nd0.0530.0510.0420.0410.047 B
3rd0.0320.0300.0250.0280.029 A
means0.0630.0660.0560.0470.058 c
ChM1st0.1410.1420.1100.0930.122 C
2nd0.0770.0720.0610.0570.067 B
3rd0.0340.0360.0260.0300.032 A
means0.0840.0840.0660.0600.073 d
MS1st0.0830.0910.0750.0580.076 C
2nd0.0470.0380.0520.0460.046 B
3rd0.0270.0280.0240.0250.026 A
means0.0520.0520.0500.0430.049 b
Means for Zn dose0.060 b0.060 b0.050 a0.0454 a0.054
Means for years1st0.096 C0.103 D0.081 B0.065 A0.086 c
2nd0.055 A0.050 A0.046 A0.045 A0.049 b
3rd0.029 A0.029 A0.023 A0.026 A0.027 a
CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c—means investigated factors with different letters (in the columns for organic fertilization and for years but in the row for Zn doses) are significantly different. A,B,C,D—means the interaction with different letters in the rows of the table are significantly different.
Table 6. Ni content in grass biomass (Ni mg·kg−1 DM).
Table 6. Ni content in grass biomass (Ni mg·kg−1 DM).
Organic FertilizersYearsDoses of Zn [mg∙kg−1]Means
0200400600
CO1st4.674.384.314.514.47 A
2nd2.462.953.193.122.93 A
3rd1.541.421.441.341.44 A
means2.892.922.982.992.95 a
BM1st4.804.894.875.124.92 A
2nd2.893.082.642.792.85 A
3rd1,701.771.991.891.84 A
means3.133.253.173.273.20 a
ChM1st6.136.405.795.525.96 B
2nd2.912.983.213.263.09 A
3rd1.652.042.011.721.86 A
means3.563.813.673.503.63 b
MS1st4.784.895.014.974.91 A
2nd2.052.802.862.802.63 A
3rd1.591.501.521.471.52 A
means2.803.063.133.083.02 a
Means for Zn dose3.103.263.243.213.20
Means for years1st5.095.144.995.035.06 c
2nd2.582.952.982.992.88 b
3rd1.621.681.741.611.66 a
CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c—means investigated factors with different letters (in the columns for organic fertilization and for years but in the row for Zn doses) are significantly different. A,B—means the interaction with different letters in the rows of the table are significantly different.
Table 7. Ni uptake by grass (Ni mg·pot−1).
Table 7. Ni uptake by grass (Ni mg·pot−1).
Organic FertilizersYearsDoses of Zn [mg∙kg−1]Means
0200400600
CO1st0.0710.0790.0560.0520.065 A
2nd0.0310.0330.0280.0390.033 A
3rd0.0140.0120.0110.0110.012 A
means0.0380.0410.0320.0340.036 a
BM1st0.1220.1440.1290.1080.126 C
2nd0.0410.0470.0340.0350.039 AB
3rd0.0200.0210.0210.0220.021 A
means0.0610.0710.0610.0550.062 c
ChM1st0.1640.1830.1540.1270.157 D
2nd0.0480.0500.0480.0480.048 B
3rd0.0170.0240.0170.0160.019 A
means0.0760.0850.0730.0640.075 d
MS1st0.1020.1230.1090.0870.105 B
2nd0.0270.0310.0460.0400.036 A
3rd0.0170.0170.0150.0150.016 A
means0.0490.0570.0570.0470.052 b
Means for Zn dose0.056 a0.064 b0.055 a0.050 a0.056
Means for years1st0.115 B0.132 C0.112 B0.094 A0.113 c
2nd0.037 A0.040 A0.039 A0.041 A0.039 b
3rd0.017 A0.018 A0.016 A0.016 A0.017 a
CO—without organic fertilization, BM—bovine manure, ChM—chicken manure, MS—mushroom substrate. a,b,c,d—means investigated factors with different letters (in the columns for organic fertilization and for years but in the row for Zn doses) are significantly different. A,B,C,D—means the interaction with different letters in the rows of the table are significantly different.
Table 8. Linear correlation coefficients between some properties of cultivated grass.
Table 8. Linear correlation coefficients between some properties of cultivated grass.
PropertiesCockfoot YieldZn_ContentZn_UptakeCu_ContentCu_UptakeNi_ContentNi_Uptake
Zn dosens0.946 *0.851 *nsnsnsns
Cockfoot yield-nsns0.645 *0.908 *0.6620.944 *
Zn_contentns-0.837 *nsnsnsns
Zn_uptakens0.837 *-nsnsnsns
Cu_content0.645 *nsns-0.901 *0.792 *0.798 *
Cu_uptake0.908 *nsns0.901 *-0.801 *0.963 *
Ni_content0.662 *nsns0.792 *0.801 *-0.862 *
Ni_uptake0.944nsns0.798 *0.963 *0.862-
*—is important, p < 0.05. ns—not significant.
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Kuziemska, B.; Wysokinski, A.; Klej, P. The Content, Uptake and Bioaccumulation Factor of Copper and Nickel in Grass Depending on Zinc Application and Organic Fertilization. Agriculture 2023, 13, 1676. https://doi.org/10.3390/agriculture13091676

AMA Style

Kuziemska B, Wysokinski A, Klej P. The Content, Uptake and Bioaccumulation Factor of Copper and Nickel in Grass Depending on Zinc Application and Organic Fertilization. Agriculture. 2023; 13(9):1676. https://doi.org/10.3390/agriculture13091676

Chicago/Turabian Style

Kuziemska, Beata, Andrzej Wysokinski, and Paulina Klej. 2023. "The Content, Uptake and Bioaccumulation Factor of Copper and Nickel in Grass Depending on Zinc Application and Organic Fertilization" Agriculture 13, no. 9: 1676. https://doi.org/10.3390/agriculture13091676

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