Nickel Toxicity Effects on Crop and Soil: Comparison
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Low or moderate nickel concentrations in soils can cause environmental problems. The main effects of this potentially toxic element on the soil biota and the most common crop species are addressed.

  • nickel
  • agricultural soils
  • bioremediation

1. Introduction

Ni is an essential micronutrient for several biological functions in plants [20,21][1][2] and for selected microorganisms where it participates in various cellular processes [22][3].
The essentiality of this element for the animal kingdom is debated, as deficiencies rarely occur because it takes little to meet the biological functions; moreover, a metalloenzyme containing Ni has yet to be recovered [23][4].
Phipps et al. reported that there are no studies on the essentiality of Ni in invertebrates, but it probably acts as an enzymatic cofactor, as observed in vertebrates [24][5].
This element’s potential toxicity depends on many factors, such as its speciations, the way and time of exposure and concentrations. Different effects could occur at cellular and population levels when it exceeds the optimum intake level in organisms [25][6].

2. Effects on Crop

Nickel metabolism in plants is essential for some enzyme activities [26][7], maintaining the proper cellular redox state and various physiological [27][8] and growth responses [28][9].
Ni is considered an essential element for the growth of the majority of plant species with low concentrations (0.05–10 mg kg−1 d.w.) [29][10]; it is involved mainly in nitrogen metabolism, iron uptake and specific enzymatic activities such as urease, hydrogenase and superoxide dismutase [28][9].
Many authors [30,31,32,33][11][12][13][14] have studied Ni deficiency in plants, as reported in a recent review [34][15], but actually, cases of Ni deficiency are unusual in agricultural soils [35][16].
The critical level of Ni toxicity is higher than 10 mg kg−1 dry mass in sensitive species [36][17], more than 50 mg kg−1 dry mass in moderately tolerant species [37][18] and above 1000 mg kg−1 dry mass in Ni-hyperaccumulator plants [38][19]. Ni above certain limits can induce phytotoxicity at multiple levels [39][20], altering plants’ structural and anatomical dynamics [21][2]. However, it is difficult to establish a threshold of Ni concentration in soils that can be potentially toxic for cultivated plants.
Numerous authors have studied the effects of Ni on European crops such as tomato, spinach, oats, barley, wheat and corn. From the experiment conducted in Poland by Matraszek et al. [40][21] on cherry tomato (Lycopersicon esculentum), it was found that the plant yield (expressed in dry biomass) does not vary at low Ni concentrations (40 mg kg−1), while it decreased significantly at 100 mg kg−1. In another study on tomatoes, 40 mg kg−1 of Ni in the soil affected the plants’ development and yield [41][22].
Other authors found a strong decrease in cherry tomato yield at lower Ni doses caused by this PTE in plant nutrient media (from 5 to 30 mg L−1). Ni probably causes disturbances and imbalances in the absorption and accumulation of other nutrients [42][23]. More recently, the impact of Ni on Solanum lycopersicum was measured throughout the antioxidative enzyme ascorbate peroxidase (APX) when Ni was applied at 50 µM and 15 mg L−1 [43,44][24][25]. The augmented Ni doses caused a significant increase in APX activity. This effect was also observed in other plants subjected to Ni treatments, such as wheat [45][26], rice [46][27] and corn [47][28].
Poulik [48][29] studied the toxic effects of Ni on Avena sativa. Ni concentrations of 100 mg kg−1 resulted in yield depression, while doses higher than 150 mg kg−1 caused phytotoxicity and plant mortality. Kumar et al. [49][30] found that Ni applied to the soil at 10 mg kg−1 increased Hordeum vulgare yield parameters, but a significant reduction was observed beyond this level. Gupta et al. [50][31] found similar results in three cereal species (wheat, barley and oats) subjected to doses of 0, 2.5, 5, 10, 20 and 40 mg Ni kg−1. These authors found that the yield of all cereals increased significantly at 2.5–5.0 mg Ni kg−1 but decreased at higher levels. In corn plants, Amjad et al. [51][32] evaluated the mechanisms influencing the growth, physiology and nutrient dynamics after exposure to Ni treatments (0, 20 and 40 mg L−1) in hydroponic conditions. This experiment showed that all the antioxidant enzyme activity tested (SOD, CAT, GR, APX and POX) increased significantly compared to the control after Ni treatments.
Additional experiments [52,53][33][34] to test the activity of the antioxidant system in the cells of the spinach plant have shown that Ni doses applied at 50–100 and >25 mg kg−1 caused oxidative stress via increased synthesis of ascorbic acid in plant biomass. The author has suggested that ascorbic acid plays a defensive role in Ni stress.
Works regarding Ni toxicity on plant physiological processes almost always refer to laboratory studies with a contaminated solution at different concentrations [51,54[32][35][36],55], but only a few use contaminated soils, so it is difficult to establish when the soil concentration of Ni could be toxic for cultivated plants.

3. Effects on Soil Microorganisms and Earthworms

Exposure to excessive Ni concentration in soils could strongly affect living organisms such as microorganisms and soil invertebrates. Until now, the responses of soil organisms to long-term Ni pollution under field conditions has remained largely unknown.
Many microbial processes in the soil are altered by Ni presence at different concentrations, and such alterations are often identified by studying the soil enzymatic activities by the microorganisms that inhabit it. For example, in the study by Helaoui et al. [56][37], the enzymatic activities of the soil (urease, dehydrogenase, β-glucosidase, arylsulfatase, alkaline phosphatase and FDA) significantly decreased compared to the control at a Ni dose of 50 mg kg−1. However, the most negative effect appears at the high concentration of 500 mg kg−1. Similar results regarding enzymatic activities were previously found by Wyszkowska et al. [57][38], with maximum doses of 400 mg kg−1 of Ni applied.
Regarding the effect of Ni on soil microbial biomass, some studies showed a strong decrease at Ni doses of 100 and 200 mg kg−1 [58,59][39][40]. A similar trend was observed up to 250 mg kg−1, although an increase in microbial biomass at the higher dose of 500 mg kg−1 probably indicates an integrated defence system was observed [56][37].
Several authors have found that soil microbial respiration is stimulated at low Ni concentrations (50–150 mg kg−1) but declines with increasing Ni levels (> 200 mg kg−1) [58,60,61][39][41][42]. This tendency reflects a mechanism of “hormesis”, in which a small concentration of xenobiotics stimulates certain bodily functions [61][42].
In some neocaledonian soils with high levels of Ni (from 800 to 5000 mg kg−1), Héry et al. [62][43] found different Ni-resistant bacteria that adapted due to the long-time exposure to these high concentrations. The addition of NiCl2 at 30,000 mg kg−1 to these soils and a reference soil (20 mg kg−1 Ni) had an initial negative effect on bacterial growth, regardless of the soil or population considered, and this result was surprising, as the Caledonian soils had adapted to long-term exposure to high concentrations of Ni. However, the bacterial community of the reference soil was highly disturbed by the addition of Ni, while only a few changes occurred in the bacterial structure (shifts in the genetic profiles) of the neocaledonian soils, suggesting a good adaptation to Ni of these microorganisms.
In recent decades, some studies have been reported the effect of Ni concentrations (low, medium and high) on soil invertebrates such as earthworms. Scott-Fordsmand et al. [63][44] reported the toxic effects of Ni on the earthworm Eisenia veneta, in sandy-clay soil, at a concentration above 85 mg kg−1. Reproduction and lysosomal membrane stability showed a dose–response relationship and were already altered at 85 mg kg−1, while adult survival was reduced only at concentrations above 245 mg kg−1.
Lock and Janssen [64][45] examined the chronic toxicity of this metal at different concentrations, in OECD soil, for three soil invertebrates: Eisenia fetida, Folsomia candida and Enchytraesus albidus. At the highest Ni concentration of 1000 mg kg−1, no mortality occurred in E.fetida, while F.candida showed a mortality of 10%, and all E.albidus died. The reproduction test showed a significant effect on cocoons, and juvenile production in E.fetida started to be evident from a concentration of 320 mg kg−1.
E.fetida did not show an increased tolerance toward Ni despite being exposed to elevated levels for more than ten generations: worms exposed to Ni for several years showed an increased sensitivity towards this element [65][46].
Other authors [66][47] analysed the effects of the addition of nickel at concentrations ranging from 0 to 1000 mg kg−1 to 13 Chinese soils on growth, cocoon and juvenile production in the earthworm E.fetida. The body weight of E.fetida was insensitive to Ni until 320 mg kg−1, while a significant decrease in growth was observed at 560 and 1000 mg kg−1. Juvenile production, compared to cocoon output, was a more sensitive end-point for Ni, and the two parameters did not show a significant correlation with the properties of the 13 soils studied, probably due to the narrow range of properties of the selected soils.
More recently, a study examined the toxic effect of Ni-spiked farmland at concentrations from 0 to 800 mg kg−1 on E.fetida. A low mortality rate (10%) was observed only in earthworms exposed to the higher dose (800 mg kg−1) on day 14, while the avoidance response reached 100% at this concentration [67][48].
Depending on the end-point and substrate type, there is a broad range of Ni limit values, evidencing that the soil and substrate characteristics greatly influence Ni’s availability and toxicity [59[40][49][50],68,69], as well as those of other PTEs [70][51].

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