Cadmium pollution from phosphate fertilizers in arable soils and crops: an overview

Abstract

The application of mineral and organic phosphorus fertilizers to arable land has greatly increased crop yield to meet the world food demand. On the other hand, impurities in these fertilizers, such as heavy metals, are being added to agricultural soils, resulting both from the raw materials themselves and the processes used to obtain the final product. Cadmium, a non-essential and toxic heavy metal, has been found in relatively high amounts in common P fertilizers obtained from sediments. This metal poses a high risk for soil fertility, crop cultivation, and plants in general. Furthermore, human health might be compromised by the cadmium concentrations in agricultural and livestock products, due to the bioaccumulation effect in the food web. The accumulation in the different matrixes is the result of the high mobility and flexible availability of this harmful metal. This review summarizes risks to human health, the factors influencing cadmium movement in soils and crop uptake, as well as common plant responses to its toxicity. In addition, it summarizes cadmium balances in soils, trends, long-term experiments, and further studies. Cadmium inputs and outputs in arable soil, together with their calculated concentrations, are compared between two different regions: the European countries (in particular Germany) and China. The comparison appears useful because of the different proportions in the inputs and outputs of cadmium, and the diverse geographical, environmental and social factors. Moreover, these variables and their influences on cadmium contamination improve the understanding of the pollution from phosphate fertilizers and will help to establish future mitigation policies.

Keywords

soil pollution / arable land / crop production / cadmium balance / P fertilizer / cadmium toxicity

1 Introduction

Phosphorus is a scarce essential element for plant, animal and human life. It forms part of the sugar phosphates in the structures of DNA and RNA, as well as component of other biomolecules including ATP and phospholipids^[1]. Thus, the element is involved in virtually all metabolic processes. The availability of this scarce macronutrient is the product of its cycle and its pools. The soil pools include P in solution (available for plants in organic or orthophos-phate form), active (depending on soil pH bound as Ca-, Fe-, Al-phosphate, metal hydroxides or as organic phosphate, but potentially mobilized by biogenic activity) and fixed (in deposits or sediments)^[2].

Due to its deficiency in many soils and the human need for higher crop yields, mineral phosphorus fertilizers are produced via the treatment of phosphate rock (PR) from sedimentary or igneous origin^[3,4]. The final products of the process include phosphoric acid, superphosphate (SP) and triple superphosphate (TSP)^[4]. Other common P fertilizers include monoammonium (MAP) and diammonium (DAP) phosphate, the result of nitrogen addition in ammonium form to phosphoric acid^[5].

The production and consumption of P fertilizers have been rising and will rise further to meet the food demand of the increasing global population (Tab.1)^[9]. Phosphorus slowly accumulates in P mineral deposits, which are renewed over a time-scale of thousands to millions of years. The intense mining activity for agricultural purposes is rapidly decreasing these high-quality rock phosphate deposits, leading to a probable scarcity or depletion in the next 50–100 years, although other studies claim that the actual reserves will last for 400 years or more^[1,10,11]. According to the most recent survey by the Geological Survey in 2018^[12], the world P reserves will last around 260 years, taking into account the phosphate mine production (270 kt·yr⁻¹) and reserves (70000 kt).

Beside potentially exhausting P stocks, another problem is the presence of toxic heavy metals in the fertilizer input added to otherwise uncontaminated arable soils^[9,13–15]. These non-essential heavy metals, including cadmium, may disturb human, animal and plant life even at low concentrations^[9,16,17].

Tab.1 Phosphate rock production and reserves (kt; data from US Geological Survey[6,7]), and production and demand of P fertilizers (kt; data from International Fertilizer Industry Association[8])

Year	Country	Phosphate Rock USGS 2019				IFAData 2019
		Production	Reservesa	P2O5 content		Production (P2O5)	Demand (P2O5)
2010	All countries	181000	65000000	56000		42532	41663
	China	68000	3700000	20400		15998	13092
	Germany	–	–	–		3	286
	Morocco and Western Sahara	26600	50000000	8800		1875	191
	United States	25800	1400000	7400		6297	3890
2015	All countries	223000	69000000	73900		44139	43912
	China	120000	3700000	36000		17224	12111
	Germany	–	–	–		25	225
	Morocco and Western Sahara	30000	50000000	9100		2169	221
	United States	27600	1100000	7710		5257	4302
2018	All countries	270000	70000000	–		–	–
	China	140000	3200000	–		–	–
	Germany	–	–	–		–	–
	Morocco and Western Sahara	33000	50000000	–		–	–
	United States	27000	1000000	–		–	–

Note: a The estimated reserves correspond to the survey done the year after 2011, 2016 and 2019.

2 Cadmium in the environment and its health risks

2.1 Health risks by cadmium consumption

Cadmium is known as a toxic heavy metal with high mobility and hazardous effects for human life and the environment (Fig.1)^[16–20]. For human health, the tolerable weekly intake given by the World Health Organization is 7.00 µg·kg⁻¹ bodyweight^[20–22]. However, an intake above 75.00 µg·d⁻¹ Cd by an average adult person is considered a hazardous consumption, since cadmium has a half-life about 20 years in the human body^[17,22].

Cadmium can cause damage to DNA and disturbances to enzyme activities. As a consequence, cadmium can trigger failure or cancer in different organ systems, including the reproductive system, muscles, bones (by demineralization and Ca replacement), heart, lungs, liver, and kidneys. The kidneys accumulate most of the cadmium and it often binds to proteins, due to its affinity for sulfhydryl and phosphate groups^{[17,18,20,23,24]}.

Fig.1 General scheme of cadmium balance in an air-soil-crop system

Full size|PPT slide

2.2 Cadmium in soil

In general, cadmium concentrations in surface soils range from 0.06 to 1.10 mg·kg⁻¹ with an average of 0.41 mg·kg^−1[17]. The cadmium concentrations in arable land in Germany are on average 0.31 mg·kg⁻¹ (0.30– 1.20 mg·kg⁻¹)^[25,26], with concentrations varying with the soil type. Arable soils in China contain an average concentration of 0.27 mg·kg⁻¹ Cd, with higher amounts in soils near areas of mining and industrial activity, where the values can reach 150.00 mg·kg^−1[25].

The bioavailability of heavy metals (including Cd) via plant roots depends on various factors: abiotic factors include the metal concentration in soil and the physicochemical characteristics (pH, clay content, salinity, humidity, mineral, and organic matter); and biotic factors including the presence of metal-releasing microorganisms and the substances (enzymes, organic acids and hydrogen ions) released into the rhizosphere^[20,26–28].

Due to its high mobility, cadmium can be transferred from soil to plants including crops, thereby increasing the risk of bioaccumulation along the food chain^[23]. Cadmium solubility and bioavailability in soils is strongly dependent on pH^{[17,20,26,29–33]}. Lower mobility is observed when the pH is above 7.5, and a higher availability under lower pH conditions. The critical pH range is between 4.0 and 4.5 where a decrease of 0.2 pH units can cause up to five times higher mobilization and bioavailability^[16,30]. However, cadmium uptake by plants can be reduced or suppressed regardless of the suitability of the pH for mobilization by simultaneous competition with other metallic cations (Ca²⁺, Mg²⁺, Zn²⁺) and hydrogen ions^[34].

Other physicochemical characteristics of soil, such as the high organic matter content in arable soils (for instance crop residues or input of farmyard manure) may form insoluble organic complexes with cadmium, diminishing its phytoavailability and increasing crop yield^{[20,26,35,36]}.

In general, the processes of sorption-desorption, precipitation, and complexation reactions control the retention of metals in soils. The sorption-desorption equilibrium is the predominant process if heavy metals (such as Cd) are present at a low concentration. In contrast, when heavy metal concentrations are relatively high, or the pH is low, the precipitation-dissolution reactions are likely to regulate availability of heavy metal in the soil solutions^[5,31].

In addition, cadmium behavior in acidic soils can be controlled by the amount of soluble organic matter. In alkaline soils, however, cadmium mobility is dominated by precipitation processes involving phosphates and carbonates^[17].

The biotic factors influencing cadmium bioavailability include organic acids in the rhizosphere, which can form complexes with cadmium, facilitating plant uptake^[27]. Further biotic factors are the microorganisms. For example, mycorrhizal fungi can decrease cadmium phytoavailability by adsorbing cadmium in their hyphae, and bacteria can take up metallic cations and release them in a less mobile form^[27]. However, according to Vig et al.^[37], many studies regarding plant-microbe-metal interactions are based on soils amended with sewage sludge (SS) or on polluted sites after bioremediation. In such cases, high concentrations of cadmium, as well as other heavy metals and organic pollutants, are employed. Furthermore, the role of microbes is focused on augmenting tolerance to heavy metals in plants or reducing cadmium uptake by plants^[37]. In another review related to soil microorganisms, Wyszkowska et al.^[38] point out that cadmium and other heavy metals can affect the microbial community, especially bacteria, by damaging cellular structure (protein or lipid bonding structures), denaturalization of proteins or affecting enzyme activity, and thereby, influence the microbial population and its interactions with plants.

2.3 Cadmium and fertilizers

The fertilizer type, the fertilization rate, the quantity per application, crop rotation, crop residues management and liming, along with the plant species and genotype, as well as changes in pH and plant growth, can all affect the cadmium concentration and availability in soils^[20,26]. To illustrate this, chloride ions (e.g., from KCl fertilizers) may form soluble Cd-Cl complexes, reducing cadmium sorption in soils and thus increasing the Cd mobilization and bioavailability^[31,35].

The combination of high pH and high fertilization rates with nitrate compounds, such as Ca(NO₃)_2, can enhance the cadmium concentration in soil solution, since calcium in solution competes with Cd²⁺ for adsorption by soil particles, thus increasing cadmium phytoavailability^[32].

Mineral P fertilizers are considered the main input source of cadmium in arable soils in Europe^[39]. The cadmium comes from the raw materials used to produce the fertilizers, i.e., PR, which is often sourced from materials of sedimentary (with higher Cd concentration), rather than igneous origin (with lower Cd concentration). Unfortunately, only 13% of the global P sources is found in igneous rock^[3,5,31]. Dependent on their origin, the cadmium concentrations in PR range from 0.10 to 60.00 mg·kg⁻¹, with the highest values found in PR from North Africa (~60.00 mg·kg⁻¹)^[40]. However, other studies have found cadmium concentrations above 500.00 mg·kg⁻¹ in PR from Morocco (Tab.2)^[14].

In Europe cadmium concentrations in P fertilizers generally range from trace amounts to 300.00 mg·kg⁻¹, with an average of 7.40 mg·kg^−1[50], and 36.00 mg Cd per kg P₂O₅ considering the phosphate content^[51]. The current permitted limit for cadmium in fertilizers in Germany is 50.00 mg·kg⁻¹ P₂O₅ according to the German Fertilizer Ordinance^[48]. Nevertheless, P fertilizers including PR, SP and TSP might exceed this value^[14,40,48].

Tab.2 Cadmium concentrations (mg·kg−1) in inorganic and organic P fertilizers from different countries

Inorganic P fertilizers	China	Brazil (sold)	Germany (sold)	Morocco	Russia	South Africa	USA
PR	5.00 [31]	20.00[41]	19.00b[42]	30.00–60.00 [40]	0.25a[39]	1.00[20]	60.00–340.00[31]
	<2.00[20]	–	–	12.00–38.00[20,31]	1.00[20]	–	6.00–92.00[20]
	4.48a[43]	–	–	46.00–120.00a[39]	0.15[14]	–	1.45–199.00[14]
	2.60b[28]	–	–	507.00[14]	–	–	–
DAP	5.10a[39]	–	28.10a[44]	29.50–68.00a[39]	2.10a[39]	2.20a[39]	18.20–185.40[39]
	2.20[45]	–	61.00a[44]	9.36[45]	0.84[46]	–	–
MAP	5.30a[39]	17.12[41]	–	30.60–70.60a[39]	2.20a[39]	2.20a[39]	18.8–192.4a[39]
	–	–	–	–	0.14[45]	–	50.92[45]
NPK	0.60–1.51[45]	5.80[41]	15.80b[47]	0.80–11.45[45]	3.23–3.66[45]	–	–
	–	–	2.30[48]	–	–	–	–
PK	–	–	55.60b[47]	–	–	–	–
SP	0.22b[49]	8.50[41]	34.00[48]	–	–	–	–
TSP	–	–	24.40[48]	31.50–72.70a[39]	2.30a[39]	2.30a[39]	13.30–198.10a[39]
	–	–	62.00b[42]	–	–	–	–
	–	–	36.70–73.10b[47]	–	–	–	–
	–	–	28.10b[44]	–	–	–	–

Note: a Given in mg·kg−1 P2O5; b given in mg·kg−1 dry mass. PR, phosphate rock; DAP, diammonium; MAP, monoammonium; NPK, nitrogen, phosphorus, potassium; SP, superphosphate; TSP, triple superphosphate.

P fertilizers containing ammonium, such as MAP and DAP, can temporally acidify soils as a consequence of the natural process of nitrification, thereby, releasing hydrogen ions^[5,31,32]. However, the acidification of soils caused by nitrate is only relevant when this is lost by leaching^[52].

${\mathrm{NH}}_2{\mathrm{H}}_2{\mathrm{PO}}_4\to {\mathrm{NH}}_{\mathrm{4}}^{+}+{\mathrm{H}}_2{\mathrm{PO}}_{\mathrm{4}}^{-}$

${\mathrm{NH}}_{\mathrm{4}}^{+}\to \mathrm{conversion\; of\; ammonia\; to\; nitrate}\to {\mathrm{NO}}_{\mathrm{3}}^{-}+{\mathrm{2H}}^{+}\to \mathrm{decreased\; pH\; and\; soil\; acidification}$

Another effect of ammonium fertilizer may be rhizosphere acidification when ammonium is taken up directly by the plant root, which may compensate this cation uptake by proton release. If ammonia is taken up, the proton release by conversion of ammonium to ammonia also acidifies the rhizosphere. In the case of neutral or alkaline soil solution pH, both these variants mobilize phosphate and cadmium in the rhizosphere.

In contrast, P fertilizers, such as TSP and PR, can induce changes in pH and cadmium allocation into less available compartments after several applications^[30,53]. These fertilizers can enhance the formation of insoluble cadmium-phosphate compounds, e.g., Cd₃PO₄, in soils, thus immobilizing cadmium and reducing plant uptake^[36], due to the shift in soluble-exchangeable Cd distribution toward more stable bound phosphate forms^[5,32,54].

2.4 Cadmium in plants

Cadmium can have detrimental effects on enzyme activity in plants, leading to lower photosynthesis. As a result, plant growth and development including germination, root elongation, and leaf expansion can be affected by cadmium^[17,55,56]. Under higher concentrations in soils, this metal can also produce phytotoxicity symptoms such as chlorosis, and reduced vigor and performance (for instance, water and nutrient uptake)^[16,56,57]. Reduced growth and proliferation is also a consequence of the additional C skeletons required for defense and repair, which usually causes the size of the most tolerant plants to be very small (e.g., hyperaccumulators such as Arabidopsis halleri^[58]). Therefore, in agricultural production cadmium can be responsible for damage to crop, decreasing yield and protein content in seeds^[55,56].

Plants have developed resistance mechanisms against heavy metal pollution, and some species are hyperaccumulators of certain heavy metals. Even in non- accumulating species, such as maize, responses can be detected. For example, when this crop is grown under cadmium presence, phytochelatins (Cd binding polypeptides) are released as a detoxification response to avoid cadmium binding to important enzymes or proteins^[26,59]. Another reaction is the storage of cadmium binding peptides in the vacuole, removing the cadmium from essential and sensitive metabolic activities^[2,55].

Several environmental factors can activate an increased production of reactive oxygen species (ROS) in plants, including stress by heat, drought, air pollutants, organic chemicals or heavy metals. These compounds include hydroxyl radicals, hydrogen peroxide, singlet oxygen and, superoxide radicals, which are highly reactive products of an incomplete reduction of O₂ to H₂O for energy production^[9,32,55,60]. The oxidative stress triggered by high ROS concentrations impacts negatively on plant metabolism, including potential DNA damage, inhibition of enzyme activity, protein oxidation, lipid peroxidation and cell membrane damage^[55].

Thus, a further plant defense mechanism against elevated ROS production derived from heavy metal stress is the production of antioxidants. For example, some studies have detected an increased enzyme production with antioxidant activity in some maize cultivars under high cadmium concentrations, such as peroxidase, catalase, ascorbate peroxidase and superoxide dismutase^[60].

3 Cadmium balance in arable soil

The cadmium balance in surface soils as well as the bioaccumulation along the food chain involving crop production, are determined by the inputs and the outputs in arable land. Currently, the main cadmium input into European arable soils derives from mineral P fertilizers^[13,15,61]. Nonetheless, other cadmium contributions from animal manure, SS, lime, and atmospheric deposition also need to be considered (Tab.3)^[31,39,70].

For atmospheric deposition, cadmium can be present in the air as particulate matter, facilitating its mobility through the atmosphere and to other parts of the ecosphere^[17]. However, this input has been reduced since 2002 in European countries through environmental policies^[70], while in China atmospheric deposition still has a larger cadmium contribution compared to P fertilizers (Tab.3)^[5,71].

Tab.3 Atmospheric cadmium deposition (g·ha−1·yr−1) in different regions of China

Location in China	Cadmium deposition	Reference
Heilongjiang, Northeast	1.46	[62]
Mongolian Plateau, Northwest	1.04	[63]
Beijing, North China	4.75	[64]
Tianjin, North China	5.30	[64]
Hebei, North China	5.57	[64]
Henan, North China	4.93	[65]
Shanxi, North China	2.04	[65]
Fujian, South-east	0.91	[65]
Lianyuan, Southeast	17.00	[66]
Shenzhen, Southeast	7.42	[66]
Guizhou, Southwest	2.01	[65]
Jiaozhou Bay, Central Yellow Sea	1.30	[67]
Daya Bay, South China Sea	1.60	[68]
East China Sea	1.78	[69]
Southern Yellow Sea	1.80	[69]

Another important source of cadmium inputs to the soil are recycled P fertilizers. Due to the decline of PR reservoirs^[1] and the increase of organic farming, the development and use of non-mineral fertilizers had intensified^[42]. These fertilizers include animal manure, dewatered SS, chemical and thermally treated SS and anaerobically digested wastes^[42].

Manure and SS, which offer a large number of benefits to agricultural soils, are also important for the cadmium pathway through the P cycle in crop production, since cadmium is still found in these fertilizers, especially in regions of China (Tab.4). Cadmium concentrations in manure usually differ according to the animal origin, with higher amounts in swine manure regardless of the region^[44,51,74]. As a consequence of its nature, the nutrient concentration in manure is lower and more variable compared to mineral P fertilizer, leading to a higher field application rate^[5], and thereby, a higher cadmium input rates. For SS in Germany, the cadmium concentration in dewatered and stabilized SS should not exceed 1.00 mg·kg^−1[77]. Due to this reasonably low cadmium concentration in SS and the controlled application rate^[78], the estimated input through SS to arable land in Europe is relatively low^[70].

Tab.4 Cadmium concentrations (mg·kg−1) in organic P fertilizers from China, European region and Germany

Organic P fertilizers	China	Europe	Germany
Manure	0.67a[72]	0.20[70]	0.30a[44]
Swine manure	1.30[73]	–	–
	12.05[74]	0.46[70]	0.74[44]
	0.64–21.02[75]	–	–
Cattle manure	0.92[73]	–	0.43a[44]
	5.61[76]	–	0.80[42]
Poultry manure	1.48[73]	–	0.25a [44]
	15.38[74]	–	–
Sewage sludge	1.65[77]	1.80[70]	1.00a[42,77]
	–	0.30–5.10[77]	1.50–4.50[78]

Note: a Given in mg·kg−1 dry mass.

Another cadmium input to soils is the addition of lime, given that it can contain cadmium as an impurity. Usually liming of soils increases pH and reduces cadmium availability in acidic soils, thus the uptake by plants is reduced^{[26,32,79–81]}. Several studies have found that 50%–70% less cadmium accumulates in maize and some vegetables (amaranth, cabbage, and lettuce), most likely due to the supply of calcium from lime and its absorption competition with cadmium^[80–82]. However, this lime addition might not diminish cadmium uptake in alkaline soils, under deeper rooting or due to the antagonism with Ca⁺ in the soil solution^[26].

When calculating the cadmium outputs from the soil, crop uptake and leaching must be considered (Tab.5)^[15,44,61]. While crop harvest contributes to the output, leaching most likely represents a significant output from agricultural soils^[70]. Several factors influence cadmium leaching, including the sorption-desorption processes, which, as specified in Section 2.2, regulate the cadmium retention in soils. One of the most important sorption types is non-specific sorption. This occurs when cadmium is weakly bound to negatively charged surfaces by electrostatic attraction, and can be easily replaced by other ions (exchangeable) and predisposed to leaching and bioavailability^[31,91]. Another influencing factor is the pH, which could cause increased leaching when the value is lower, while higher pH values decrease this variable^[92]. For instance, data obtained by He et al.^[93] indicate that the cadmium quantity adsorbed in soils was higher, the more acidic these became. This is due to the likely release of hydrogen ions from adsorption sites and their replacement with cadmium^[93]. Paradoxically, as mentioned before, a lower pH can increase the cadmium leaching to deeper layers. Furthermore, periods with elevated precipitation (water surplus or excess of precipitation) contribute to leaching to deeper layers since cadmium leaching is coupled to water leaching^[94]. Other factors such as soil density, total cadmium concentration in the soil, temperature, distribution coefficient ($K_D$), cation exchange capacity (CEC), which is influenced by organic matter and clay content, are known to influence cadmium leaching^{[61,70,93,95]}. Thus, leaching rates are usually modeled or calculated^[15]. In 2014, Six and Smolders^[70] calculated a relatively high leaching rate for European soils, which represents the main output from arable soils (Tab.5). This agrees with some Chinese studies, in which leaching has been found to be the main output mechanism rather than crop harvesting^[15,87]. However, another recent study has indicated that the high value for leaching for European soils could be an overestimation due to the equation used^[61] since lower rates of cadmium leaching were measured or calculated in other studies done in soils from Europe and New Zealand^[19,94,95]. Furthermore, soils in Europe are usually limed^[70], which should be sufficient to buffer soil and avoid cadmium leaching.

Tab.5 Cadmium inputs and outputs (g·kg−1·yr−1) in arable land from studies in Europe and China

Type	Europe								China
	Finland[83]	Austria[84]	Germany[44]	Northern Sweden[85]	Europe[70]	Central Europe[42]	France[61]		China[86]	Heilongjiang[87]	Hunan[88]	Yangtze River delta[89]	Hainan Island[90]
Cadmium inputs
Atm. Dep.	0.30	2.10	1.70	0.34	0.35	0.35	0.20		4.04	0.36	6.85–40.25	2.66	0.91
P fertilizers	0.025	0.79	5.60	–	0.80	3.40	2.84		0.20	0.40	0.06–2.39	0.11	3.20
Manure	0.32	0.46	0.64	0.47	0.06–0.14	1.40	0.25		6.38
Sewage sludge/Irrigation watera	0.023	0.04	–	–	0.05	0.30	–		1.80	<0.10	0.002–8.19	5.65	0.11
Lime	0.035	–	–	–	0.02–0.09	0.15	0.02		–	–	–	–	–
Total input	0.71	3.39	7.94	0.81	1.43	5.60	3.31		12.42	0.76	6.91–50.83	8.42	4.22
Cadmium outputs
Crop offtake	0.14	0.13	0.68	0.17	0.20	–	0.99		–	0.20	15.66–61.45	0.61	0.41
Leaching	0.06	0.26	0.28	0.61	2.56	–	3.00, 0.56 and 0.28		–	–	0.033–0.412	1.11	0.64
Total output	0.20	0.39	0.96	0.78	2.76	0.50	3.99, 1.55 and 1.28		1.46	0.20	15.66-61.66	1.72	1.05

Note: a Sewage sludge is banned for arable use in China. The input from irrigation water is considered instead of sewage sludge.

4 Long-term studies

4.1 Field studies

One single application of fertilizer may not cause a significant accumulation of heavy metals in arable land. However, repeated fertilizer application over the long-term can result in harmful heavy metal concentrations for crops and for bioaccumulation potential in the food chain, thus representing a health risk^[76,96,97]. Nevertheless, contrasting studies reviewed by Jiao et al.^[28] indicate that cadmium concentrations in soils might not be affected by P fertilization addition in the long term.

Long-term studies by Gray et al.^[96] in pastures of New Zealand indicated that after 44 years of P mineral fertilization, an increase in total soil cadmium had occurred. The P fertilizer used (single SP) had relatively high concentrations of cadmium, ranging between 34.00 and 69.00 mg·kg⁻¹. However, after the long period of fertilization, a higher proportion of cadmium was in the residual soil fraction, which represents the residual and least mobile fraction from the sequential extraction method used, indicating that cadmium moves to less plant-available forms with time^[96].

Results from other long-term fertilization experiments (>22 years) suggest that animal manure could cause cadmium accumulation in soils as a consequence of the mixture of mineral and non-mineral fertilizers^[33,97]. In one of these studies, cadmium concentrations were 10 to 25 times higher than prior to fertilization with manure. However, the manure decreased the uptake of cadmium by the maize crop^[97], while in other field experiments under swine manure and NPK fertilization, the plant-available cadmium fraction in soils decreased compared to the total concentration^[33]. This may be due to the formation of insoluble cadmium-complexes with organic compounds originating from the manure^[26,35]. In other words, the application of amendments, namely manure and SS, does not decrease (or increase) the total cadmium concentration, but their application can reduce its bioavailability for crops^[23].

In another long-term experiment (17 years) by Wu et al.^[76], the application of pig manure together with mineral fertilizer (NPK) increased the total cadmium concentration in different soil types: ‘black’ soils, which have a higher quality humus and a moderate to high organic matter content^[98,99], and ‘red’ soils, which have high contents of Al-and Fe-oxides, and a lower CEC^[98]. In this long-term experiment, the cadmium bioavailability (reducible and exchangeable fractions) was determined by the soil type: the ‘red’ soil had a lower cadmium bioavailability and a higher residual fraction, while the ‘black’ soil had a higher cadmium percentage in the exchangeable and reducible fraction. This is likely due to the mineral differences between both soils. Still, for mineral P fertilizer, application in the form of calcium superphosphate did not result in any difference in cadmium concentration compared to the unfertilized soils^[76].

4.2 Models and trends

The problem of relatively high cadmium concentrations in fertilizers is not just a recent concern and several papers have approached this challenging situation in the past.

Cupit et al.^[100] studied the economic aspects, concluding that the lowest cost option for decreasing cadmium risks was to use low-cadmium phosphate rock, since taxing the fertilizers with high cadmium concentrations would impact largely on the farmer. Another suggested option was to the limit concentration gradually from 60.00 mg Cd per kg P₂O₅ by 2006 to 20.00 mg Cd per kg P₂O₅ by 2015^[20,100]. However, a lower threshold would affect important producers and exporters^[39,101], for instance, producers from Morocco, where cadmium concentrations in PR are usually higher than 20.00 mg Cd per kg P₂O₅^[14,39,40], and in 2018 the flexible limit was still 60.00 mg Cd per kg P₂O₅^[102].

In a study by Smolders and Six^[51], European soils with different P fertilizers concentrations (with 0, 40.00, 60.00 and 80.00 mg Cd per kg P₂O₅) were modeled. It was predicted that soil cadmium will stay constant over the long-term (100 years), even if fertilizers with the highest concentrations of cadmium were to be applied. Additionally, under low or medium fertilizer application, the cadmium concentrations in the soil will decrease in most of the scenarios after 100 years of P fertilizers application. This prediction was based on lower P fertilization rates, leaching rates, the K_D models used and the strong reduction in atmospheric deposition of cadmium in European countries, compared to other mass balances done previously.

Another mass balance model, for accumulation of cadmium and other hazardous substances after 200 years of different P fertilizer application, was developed by Weissengruber et al.^[42]. The authors assumed two different pH values and different rainfall scenarios to test the influence of diverse fertilizers on hazardous substances accumulation. These fertilizers included mineral fertilizers (e.g., TSP), recycled P fertilizers allowed in organic farming (e.g., compost), and other emerging options (e.g., treated biosolid ashes). The results indicated that there is likely to be a decline in cadmium accumulation in soils even when high cadmium concentration fertilizers are applied, which agrees with the study of Six and Smolders^[70]. However, there is a probability of cadmium output by leaching and crop harvests, which is higher under TSP, PR and compost application. Recycled fertilizer had a higher probability of cadmium output than struvite or biosolids ashes, as the result of the fertilizer application rate, which is dominated by the P concentration in the fertilizers. In other words, if the P concentration is lower, such as in green compost, the application frequency will increase to meet the crop P demand, as will the addition of hazardous substances as a consequence. Meanwhile, if the P concentration is relatively high, as in struvite or biosolid ashes, the P fertilization rate decreases and therefore the pollutant input to soils will also decrease, despite cadmium concentration of these fertilizers being higher^[5,15,42].

In contrast to these results, Qian et al.^[103] indicated that cadmium concentrations in Chinese soils will increase, reaching the acceptable threshold for agricultural soils in 50 years. This is the result of the cadmium background concentrations in soil, the atmospheric deposition and the continuous application of animal manure to fields, which are the main heavy metal inputs to arable soils in China^[15,71], especially from swine manure, which has higher cadmium concentrations than the current approved limit (Cd<3.00 mg·kg⁻¹ DM)^[74].

Another mass balance model for actual P fertilizer application rates in soils in France was developed by Sterckeman et al.^[61]. In their study, the authors indicated that under high leaching rates (using the equation from Six and Smolders^[70]), the cadmium concentration in the soil would decrease in the long-term (100 years) from 0.31 to 0.29 mg·kg⁻¹. Meanwhile, considering a medium and low leaching rate, cadmium would increase from 0.31 to 0.35 and 0.36 mg·kg⁻¹, respectively. In addition, the increase of cadmium in soils under the actual P rates would lead to proportionally higher crop uptake, increasing the cadmium exposure of animals and humans through dietary intake^[61].

There are numerous model studies, however, the results of these cadmium accumulation models can be imprecise, due to the many assumptions and generalizations that are made to simplify the complexity of reality, including social, agricultural, climatic and regional factors^[102]. Moreover, the lack of consistency in the leaching rate estimates indicates that its determination in different regions and environmental variables should be a priority to eliminate further uncertainties around this factor.

5 Conclusions and outlooks

Cadmium input from phosphate fertilizers represents an environmental and health risk due to soil pollution, crop uptake, and bioaccumulation along the food chain. A decrease in mineral P fertilizer dependence, along with the use of non-polluted recycled fertilizers could alleviate the gap in the P cycle and the cadmium pollution of arable land, in countries such as Germany, where atmospheric deposition does not represent an important cadmium contribution to the soil. In countries like China, however, where atmospheric deposition and the manure application are the main cadmium inputs to agricultural land, environmental policies, and trace metals limits in animal waste could be used to decrease the pollution of arable land.

Future work should focus on cadmium balances in arable land, considering the soil properties (e.g., pH and CEC), crop and soil management (e.g., liming) and therefore the potential leaching, which seems to be an important but also inconsistent output regarding cadmium balance models. The social, climatic and economic differences and circumstances among countries should also be taken into account. Furthermore, there is a lack of knowledge about the potential accumulation of cadmium from P fertilizers via crops in the various elements of the food chain and in the P cycle. Hopefully, an improved, highly efficient P input and a more closed P cycling can mitigate the problem of cadmium pollution, due to a higher recycling and a lower dependency on mineral P fertilizer from sedimentary origin, but this remains to be investigated.

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Acknowledgements

This review was carried out as part of the project “Adaptation of Maize-based Food-feed-energy Systems to Limited Phosphate Resources” from the German-Chinese International Research Training Group 2366. The authors gratefully acknowledge the support for this project provided by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)–328017493/GRK 2366 and Ten-Thousand Talent Program of China (Xuejun Liu).

Compliance with ethics guidelines

ƒAndrea Giovanna Niño-savala, Zhong Zhuang, Xin Ma, Andreas Fangmeier, Huafen Li, Aohan Tang, and Xuejun Liu declare that they have no conflicts of interest or financial conflicts to disclose.ƒThis article is a review and does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2019. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)