INTRODUCTION
Reconciling the need for producing sufficient high-quality, health-enhancing food for the world's expanding population with conserving biodiversity will be achieved through scientific and technological advances. Probably, two aspects of biology, namely breeding improved cultivars and enhancing the efficiency of nutrient uptake in partnership with soil microbes (Wissuwa et al. Reference Wissuwa, Mazzola and Picard2009), will be prominent among these advances. Artificially supplementing nutrient supplies, especially nitrogen, has previously made major contributions in raising crop yields. For example, Bell et al. (Reference Bell, Fischer, Byerlee and Sayre1995) showed from long-term studies of cereal farming in the Yaqui Valley of Mexico that breeding improved wheat cultivars accounted for 0·28 of the overall farm yield progress and 0·48 came from increased use of nitrogenous fertilizers. This supports observations by Greenwood (Reference Greenwood1982) who showed that “… in West Europe … wheat yields are almost directly proportional to the level of N-fertilizer applied”. It is now appreciated, however, that use of nitrogenous fertilizers must not produce undesirable side-effects such as nitrate pollution into river catchment areas (Sieling & Kage Reference Sieling and Kage2010; Roy Reference Roy2015). Ideally, fertilizers should act in concert with soil-borne microbial populations as part of sustainable integrated pest management (IPM) strategies. The current review suggests that calcium cyanamide, a specialized fertilizer, which until recently has been used predominantly for intensive horticultural crops, has properties that could contribute to these IPM strategies including minimizing nitrate release into groundwater and encouraging benign soil-borne microbes (Brochado-Miranda Reference Brochado-Miranda1975; Dixon Reference Dixon2012a ). In support of that contention, the current review examines the background to calcium cyanamide manufacture, the advantages and disadvantages of practical use, its presence as a natural metabolite, relationships with soil microorganisms and in particular capabilities for reducing the impact of soil-borne pathogens such as Plasmodiophora brassicae Wor., which causes clubroot disease.
THE NITROGEN PROBLEM
Sir William Crookes, an eminent chemist in the late 19th century, highlighted the original ‘nitrogen problem’, identifying that “… the (artificial) fixation of nitrogen is vital to the progress of civilized humanity…” (Crookes Reference Crookes1900). For most of mankind's history, soil nitrogen was obtained from two natural sources: rainwater containing nitrous oxides derived from atmospheric electrical storms, forming nitric acid and the activities of soil-borne bacteria, either those in symbiotic relationships with legumes and other plants or those which exist as free-living forms. Farmers supplemented these sources with animal faeces either deposited directly onto pastures or as manure collected from farmyards. Other more minor sources included nitrogen-bearing rocks in India and Chile plus deposits of guano, accumulated bird droppings and waste materials such as shoddy, from some manufacturing processes. As Europe's Agricultural Revolution led on to its Industrial Revolution, finding new supplies of nitrogen that would boost food supplies became crucially important (this is reviewed in detail in the textbook series by Broughton Reference Broughton1981, Reference Broughton1982, Reference Broughton1983, Reference Broughton1986). Research and industrial progress, particularly in Germany, developed at least six processes that artificially fixed atmospheric di-nitrogen (N2) into stable forms in the late 19th and early 20th centuries. Three processes were economically feasible and commercialized: the Norwegian Arc, the Haber-Bosch and Cyanamide (Mellor Reference Mellor1925; Ernst Reference Ernst1928; Leigh Reference Leigh and Leigh2004). Of these, the Haber-Bosch process has dominated nitrogen fertilizer manufacture for over a century. Production of calcium cyanamide has, however, continued predominantly for some specialized applications.
CALCIUM CYANAMIDE
From 1895 onwards, Adolph Frank (1834–1916) and Nikodemus Caro (1871–1935) researched chemical methods of nitrogen fixation as a means for making artificial fertilizers. Eventually working with F. Rothe of Beringer Söhne, they jointly discovered that calcium cyanamide could be made by the addition of pure di-nitrogen, prepared by air liquefaction (Linde Reference Linde1916), to calcium carbide at temperatures in excess of 1000 °C (Frank Reference Frank1908). In 1908, Frank and Caro established a factory near Trostberg, Bavaria, powered by hydroelectricity generated from the river Alz, where they produced 30 000 tonnes per annum of calcium cyanamide by 1912. This is now the most commonly used derivative of the cyanamide group of organic compounds, with the general formula CN2H2. The molecule contains nitrile and amino groups. Hall (Reference Hall1905), working at Rothamsted Experiment Station Harpenden (now Rothamsted Research), recognized calcium cyanamide as “… the first attempt on a commercial scale to bring atmospheric nitrogen into a state of combination, to manufacture infact an artificial manure containing N derived from the air”. The physical, chemical and industrial properties of the cyanamide group of compounds are discussed by Güthner & Mertschenk (Reference Güthner, Mertschenk and Elvers2006).
FERTILIZER VALUE
Originally this fertilizer was named Kalkstickstoff (nitrogen-chalk) and is also referred to as lime-nitrogen and nitrolime. It is now formulated as a granular dust-free product resulting from combination with calcium nitrate suspension, calcium carbonate and a surface treatment with wax. Calcium cyanamide (CASE Registry no: 420–02–4) contains approximately 0·20 nitrogen and 0·50 calcium (expressed as calcium oxide, CaO). Albert Frank, son of Adolph Frank, demonstrated that in soil calcium cyanamide is converted into ammonium ions, offering a form of artificial fertilizer nitrogen, which plants could utilize (Anon 2008a ; Dixon Reference Dixon2009a ). In the UK, studies at Rothamsted demonstrated that soil microbial activity increases in the presence of calcium cyanamide (Ashby Reference Ashby1905) and in the USA by Jacob et al. (Reference Jacob, Allison and Braham1924). Soil microbes slowly change calcium cyanamide in a step-wise process through cyanamide to urea to ammonia to nitrate (Bjälfve Reference Bjälfve1957). Alternatively, and more rapidly, carbonic acid from the atmosphere converts calcium cyanamide into cyanamide ions and calcium carbonate. Subsequent hydrolysis of cyanamide forms urea. In moist soils, a proportion of cyanamide (0·06–0·11) dimerises into dicyandiamide (cyanoguanidin) (H4C2N4) (Cornforth Reference Cornforth1971; Dixon & Williamson Reference Dixon, Williamson, Macfarlane Smith and Hodgkin1985).
Dicyandiamide (DCD) is classed by the European Union (EU)-Fertilizer Directive 02003/2003 (Amendment of 8 November 2008; European Union 2008) as a nitrification inhibitor. The initial DCD content of calcium cyanamide and additional amounts resulting from the effects of soil moisture and activities of microbes slows the rate of soil nitrification and reduces the leaching of nitrates into groundwater (Rathsack Reference Rathsack1978; Vilsmeier & Amberger Reference Vilsmeier and Amberger1978). Recent Japanese research (Yamamoto et al. Reference Yamamoto, Akiyama, Naokawa and Yagi2012, Reference Yamamoto, Akiyama, Naokawa and Yagi2013) demonstrated that calcium cyanamide reduces the emissions of nitrous oxide from soils. It is notable that nitrous oxide is a greenhouse gas, which is estimated to be approximately 300 times more damaging for the environment than carbon dioxide (Solomon et al. Reference Solomon, Qin, Manning, Chen, Marquis, Avery, Tignor and Miller2007). Recent studies of spring applications of nitrogen fertilizers to winter wheat crops in eastern England emphasized the value of DCD in reducing nitrous oxide emissions (Thorman et al. Reference Thorman, Williams, Musselbrook, Rollett, Bowden, Shrosbree, Chambers and Cordovil2014). In Germany, there is official recognition of DCD's properties (Nõmmik Reference Nõmmik1958; Anon 1996; Güthner & Mertschenk Reference Güthner, Mertschenk and Elvers2006).
Calcium cyanamide production in the Western world is limited to one factory in Bavaria, Germany. There are two factories in Japan and several in China. Limits on German production capacity mean that this fertilizer is available in modest quantities (~100 000 t/year) for European users compared with the 450 Mt/year of ammoniacal fertilizers produced by the Haber-Bosch process in factories worldwide as reported by Smil (Reference Smil2004). This author identifies that artificial nitrogen production uses large amounts of energy. The Haber-Bosch process requires up to 0·02 of the world's annual energy supply, while calcium cyanamide manufacture is one of the larger users of Germany's annual energy production (AlzChem, personal communication, February 2015). The scale of calcium cyanamide production is also limited by the two-stage nature of chemical manufacture, which initially involves carefully forming calcium carbide. After manufacture, the finely ground product is compacted by a granulation process resulting in very hard fertilizer granules. Treating the surface of these granules with a wax ensures that the fertilizer product is a dust-free formulation. In this state, the product has an unlimited storage life (Güthner & Mertschenk Reference Güthner, Mertschenk and Elvers2006) and may be transported without restriction, packed in polyethylene valve or multilayer paper bags.
The relatively modest scale of production means that the cost of calcium cyanamide is proportionately higher than ammonia-based products. But since this fertilizer combines nitrogen and calcium, the latter reducing the need for applications of lime and helping to diminish the impact of soil-borne pathogens, it eliminates the need to purchase other resources. The agronomic value of calcium cyanamide is increased by repeated use over several seasons, which further increases yields and crop health (Crowther & Richardson Reference Crowther and Richardson1932; Verona Reference Verona1970).
Predominantly, calcium cyanamide has been used as a fertilizer for field vegetable and salad crops in Europe, Asia and North America. Use in other crops has risen recently because of increased applications on oilseed rape crops in Northern Europe, where clubroot disease (P. brassicae) is becoming a limiting factor (Dixon Reference Dixon2009b ). Demand in China is also increasing for similar reasons, because of their substantial problems with clubroot (P. brassicae) on oilseed rape and vegetable brassica (Brassica rapa), crops which are a staple part of the diet (Chai et al. Reference Chai, Xie, Shi and Li2014). The properties of calcium cynamide for inhibiting seed germination (Sturkie Reference Sturkie1937) resulted in recommendations for a 14-day interval between application and drilling. This restriction is less necesary for transplanted crops: recommendations, for example in Harling & Oxley (Reference Harling and Oxley2007), suggest applying split applications of 500 kg/ha as a base dressing followed by a further 500 kg/ha 14–21 days after transplanting modules. Recent technological advances in crop husbandry permitting between-row, in-row and deep-placement of fertilizers have led to further relaxation of these restrictions because the volumes of fertilizers applied per unit area are greatly reduced, while nutrient-use efficiency increases (Burns et al. Reference Burns, Hammond and White2010). In Australia, Donald et al. (Reference Donald, Lawrence and Porter2004) demonstrated the usefulness of banding techniques for the application of calcium cyanamide, which reduced clubroot incidence and costs. This technique is especially useful in Asian vegetable brassica crops grown on soils with high organic matter contents, where clubroot disease can be particularly devastating (McDonald et al. Reference McDonald, Kornatowska and McKeown2004).
Stability in soil
Long-term studies in Portugal (1958–74) compared the effects of applying ammonium nitrate, ammonium sulphate, calcium cyanamide, calcium nitrate and urea to land in a warm temperate region with an annual average rainfall exceeding 1100 mm (Brochado-Miranda Reference Brochado-Miranda1975). The pH of calcium cyanamide-treated plots increased slightly, while the other treatments decreased it. Additionally, the use of calcium cyanamide resulted in greater retention of exchangeable calcium, while other fertilizers reduced it. The phosphate and potash content of soil treated with calcium cyanamide remained stable, with increased availability of these nutrients.
Subsequent research in a tropical environment subjected coarse-textured kaolinitic ultisol placed in soil columns and treated with calcium cyanamide, urea or calcium ammonium nitrate to the equivalent of 2420 mm rainfall over 42 days (Pleysier et al. Reference Pleysier, Arora and Juo1987). Lowest leaching losses (0·03 of the nitrogen applied) were recorded where calcium cyanamide was used; the highest losses were found with calcium ammonium nitrate, while urea produced intermediate effects. These results indicated that calcium cyanamide is retained in soils and not leached, even where rainfall or irrigation is substantial. These are valuable properties in relation to the use of irrigation and spread of plant pathogens (Dixon Reference Dixon2015).
The nitrate content of soils treated with calcium cyanamide was lower than those of untreated controls (Nõmmik Reference Nõmmik1958). It was shown that conversion to nitrate took longer where calcium cyanamide was used compared with ammonium sulphate (Nõmmik Reference Nõmmik1958). Soil texture influenced the rate of conversion, with coarse sandy soils retaining nitrate longer. In soil samples incubated for 3 months, >0·90 of the nitrogen was retained in the calcium cyanamide treatments. Lowering the temperature slowed nitrification still further. The conversion of calcium cyanamide to ammonia was stopped in sterilized soil, indicating that this process requires microbially derived enzymes. Earlier research by Jacob et al. (Reference Jacob, Allison and Braham1924) produced broadly comparable results.
The fertilizer properties of calcium cyanamide were reviewed by Rieder (Reference Rieder1981) and more recently by Dixon (Reference Dixon2009a ; Reference Dixon2012a ). These workers identified that granulating calcium cyanamide increased its stability and environmental value. Granulation of calcium cyanamide improved its fertilizer-use-efficiency and availability for roots (Vilsmeier & Amberger Reference Vilsmeier and Amberger1978). Amberger (Reference Amberger1986, Reference Amberger1989) also demonstrated that when DCD inhibits the initial step in nitrification, this conserves nitrogen as ammonium (NH+ 4) ions. Dicyandiamide ultimately is decomposed by biotic and abiotic processes in soils into ammonium ions, carbon dioxide and water, while nitrogen is slowly released.
NATURAL OCCURRENCE AND UTILIZATION OF CYANAMIDE
Hairy vetch (Vicia villosa), which originates from Europe and Western Asia, is used as a cover crop in the USA as a means of protecting land from wind and water erosion during fallow periods (Hartwig & Ammon Reference Hartwig and Ammon2002). This legume adds nitrogen into the soil and is also antagonistic to weed growth, suggesting that it may produce naturally growth-inhibitory compounds. Analyses by Kamo et al. (Reference Kamo, Hiradate and Fujii2003) showed that hairy vetch produces cyanamide, which has allelo-chemical activity against lettuce (Lactuca sativa) seedlings used as test plants. Germinated seedlings of hairy vetch contained 40-fold greater concentrations of cyanamide compared with the content of dry seed, illustrating that this plant generates cyanamide during its early growth. In hairy vetch seedlings, concentrations of cyanamide as high as 130 µg/g fresh weight were found. This illustrates that cyanamide, which was previously considered solely as a product of industrial manufacturing, is also a naturally occurring metabolite. Later studies by Kamo et al. (Reference Kamo, Sato, Kato, Hiradate, Nakajima, Fujii and Hirota2006, Reference Kamo, Takemura, Wasano, Fujii and Hiradate2012) indicated that young leaves of V. villosa, V. cracca, V. benghalensis and Robinia pseudo-acacia contained cyanamide (NH2CN) in the range of 190–645 µg/g fresh weight, determined by gas chromatography-mass spectrometry (GC-MS).
Some Aspergillus and Penicillium spp. can reportedly utilize the cyanamide molecule as a source of nitrogen for decomposing cellulose (Klasse Reference Klasse2002). Consequently, calcium cyanamide is considered as an environmentally benign product as it is broken down to harmless products by microbes (Harling & Oxley Reference Harling and Oxley2007). The soil-borne fungus Myrothecium verrucaria is capable of degrading fertilizer calcium cyanamide by the action of a single soluble enzyme that hydrolyses cyanamide to urea (Stransky & Amberger Reference Stransky and Amberger1973). Cyanamide hydratase is produced by this fungus in combination with a urease (Maier-Greiner et al. Reference Maier-Greiner, Obermaier-Skrobranek, Estermaier, Kammerloher, Freund, Wülfing, Burkert, Matern, Breuer and Eulitz1991; Lehtovirta-Morley et al. Reference Lehtovirta-Morley, Stoecker, Vilcinskas, Prosser and Nicol2011; Tourna et al. Reference Tourna, Steiglmeier, Spang, Könneke, Schintlmeister, Urich, Engel, Schloter, Wagner, Richter and Schleper2011). The discovery of this highly substrate-specific cyanamide hydratase, the elucidation of its structure as a homo-hexameric polypeptide, and the isolation of its gene (cah) offers the possibility that transformed plants could carry out these reactions. That would allow calcium cyanamide fertilizer to be applied before sowing without risking seedling growth inhibition. This could reduce the amount of fertilizer calcium cyanamide required while retaining its effectiveness as a source of nitrogen. Other suggestions that would improve the efficacy of calcium cyanamide fertilizer applications have been the incorporation of the cah gene into crop plants so that they could directly utilize cyanamide as opposed to requiring its initial conversion to urea (Wood Reference Wood1998).
SOIL HEALTH AND FERTILIZER VALUE
Sustainable agriculture aims at developing healthy soils, as discussed by Lehmann & Kleber (Reference Lehmann and Kleber2015) and Wall et al. (Reference Wall, Nielsen and Six2015). Healthy soils are stable systems in which there are high levels of biological diversity, activity, internal nutrient cycling and resilience to disturbance (Doran et al. Reference Doran, Sarrantonio and Liebig1996; Doran & Zeiss Reference Doran and Zeiss2000; Eveillard Reference Eveillard2005; van Bruggen et al. Reference van Bruggen, Semenov, van Diepeningen, de Vos and Blok2006). Soil health is defined in detail by Pankhurst et al. (Reference Pankhurst, Doube, Gupta, Pankhurst, Doube and Gupta1997) and by the United Nations Food and Agriculture Organization (Anon 2008b ). Retaining the diversity of microbes in soil is critical for maintaining soil health and quality and the wide range of microbes involved in soil functioning (Liesack et al. Reference Liesack, Janssen, Rainey, Ward-Rainey, Stackebrandt, van Elsas, Trevors and Wellington1997; Garbeva et al. Reference Garbeva, van Veen and van Elsas2004). This preserves the huge genotypic and phenotypic diversity, heterogeneity and crypticity in soil microbial populations. The top layer of soil may contain up to 109 microbe cells per gram (Torsvik & Ovreas Reference Torsvik and Ovreas2002). As yet, knowledge concerning many of these organisms and their interactions is limited. The fraction of cells making up the general microbial biomass that have been cultured and studied is very small, probably <0·05 (Torsvik et al. Reference Torsvik, Goksoyr and Daae1990; Borneman & Triplett Reference Borneman and Triplett1997). An added difficulty is that microbe populations may change quite rapidly, especially during cropping, where soluble nutrients such as ammonium-nitrogen are used and soil acidity increases (Kirkby Reference Kirkby1968). Consequently, practical fertilizer strategies should aim where possible, at encouraging beneficial microbes, especially those that are antagonists against soil-borne pathogens (such as P. brasicae) (Lahlali & Peng Reference Lahlali and Peng2014; Yu et al. Reference Yu, Zhao, Cheng and Wang2015).
Müller (Reference Müller1955) was one of the first pathologists who associated calcium cyanamide with reductions in diseases caused by soil-borne microbes and also recorded its effects in stimulating the growth of non-pathogenic microbes. Earlier interactions between calcium cyanamide and soil microbe populations had been reported by Allison (Reference Allison1924); Kuhn & Drechsel (Reference Kuhn and Drechsel1928); Wolfe & Wolfe (Reference Wolfe and Wolfe1930) and Haenseler & Moyer (Reference Haenseler and Moyer1937). The detailed studies by Haenseler & Moyer (Reference Haenseler and Moyer1937) demonstrated that bacteria and actinomyce populations in soil decreased initially and then accelerated rapidly for about 30 days after application of calcium cyanamide. Thereafter numbers dropped, returning to the values present before the fertilizer was applied. At their peak, however, the numbers of microbes in these two groups were 90-fold greater compared with normal soil content. Similar results have been reported more recently by Klasse (Reference Klasse1996). Applications of calcium cyanamide are associated with increased extracellular enzyme activity in soil, which is indicative of enhanced microbial activity (Bosch & Amberger Reference Bosch and Amberger1983). These included increases in: biomass, amylase, protease, alkaline phosphatase and dehydrogenase activities, exceeding that achieved by applications of farmyard manure and ammonium sulphate. This implies that for organic husbandry systems, the use of calcium cyanamide is superior in its effects to those obtained from animal manure (Zhu et al. Reference Zhu, Ma, Ye and Xia2001).
The practical advantages of calcium cyanamide in relation to disease suppression were highlighted by Cornforth (Reference Cornforth1971); Rieder (Reference Rieder1981) and Klasse (Reference Klasse, Anac and Martin-Prével1999). Evidence for the benefits of fertilizers such as calcium cyanamide in developing healthy soils is accumulating. In China, for example, large areas of land are now devoted to the production of protected vegetables, especially aubergines, cucumbers and tomatoes. This has led to a rise in crop losses caused by soil-borne pathogens, especially fungi such as Verticillium spp. Calcium cyanamide applications increased the biological health of these soils and resulted in improved crop growth by inducing shifts in the composition of microbial communities (Tian et al. Reference Tian, Zhang, Liu, Chen and Gao2009). This reduced the damage from Verticillium spp. Calcium cyanamide increased mineral nitrogen, followed by increased microbial biomass, especially in the autumn periods. Similar findings were reported by Shi et al. (Reference Shi, Wang, Zhou, Yu and Yu2009), where calcium cyanamide applications increased soil bacterial populations and decreased the pathogen Fusarium oxysporum f. sp. cucurbitae (cucurbit wilt). Subsequently, reduction of activity by the soil pathogen F. solani f. sp. cucurbitae (stem rot) affecting cucumber was ascribed by Bourbos et al. (Reference Bourbos, Skoudridakis, Darakis and Koulizakis1997) to soil enrichment with nitrogen and calcium. Bletsos (Reference Bletsos2006) suggested that calcium cyanamide can form an effective component of an integrated management system, which eliminates the need for using the environmentally damaging sterilant methyl bromide (Klasse Reference Klasse2002).
Recent research reported by Ma et al. (Reference Ma, Sun, Hu, Yu, Wang and Fu2013) demonstrated that the numbers of bacteria increased in soil treated with calcium cyanamide, while those of fungi decreased in the 30 days after application. Ma et al. (Reference Ma, Sun, Hu, Yu, Wang and Fu2013) claim that this restored the microbial community balance to a healthy status favourable for vegetable cropping. Use of polymerase chain reaction–denaturing gradient gel electrophoresis (PCR-DGGE) fingerprinting indicated that the bacterial populations following calcium cyanamide application changed, with the appearance of new species and increased biodiversity. The diversity and richness indices 20 days after calcium cyanamide was applied increased substantially. The dimer product DCD produced similar effects, improving diversity and richness in bacterial populations. Ma et al. (Reference Ma, Sun, Hu, Yu, Wang and Fu2013) suggested that such effects are principal mechanisms by which the cyanamide fertilizer reduced the impact of soil-borne pathogens. Greater knowledge of the interaction of fertilizers and microbes might also solve some of the problems highlighted by Walters et al. (Reference Walters, Ratsep and Havis2013) regarding the use of induced resistance as an ingredient in integrated disease management strategies. Since calcium cyanamide provides a readily available source of calcium for plants, this may potentially help up-regulate aspects of general and specific resistance, as suggested by Takahashi et al. (Reference Takahashi, Takita, Kishimoto, Mitsui and Hori2002). In the Takahashi et al. (Reference Takahashi, Takita, Kishimoto, Mitsui and Hori2002) studies, an influx of calcium into turnip cells increased the formation of phenylalanine ammonia-lyase (PAL) activity, which appeared necessary for the expression of resistance to Plasmodiophora brassicae. As Dixon & Tilston (Reference Dixon, Tilston, Dixon and Tilston2010) suggest, knowledge of the properties of fertilizers such as calcium cyanamide might help redirect agronomists towards enhancing soil and plant health.
CALCIUM CYANAMIDE AND THE SUPPRESSION OF CLUBROOT DISEASE
Clubroot disease is caused by the protist member of the Rhizaria (Burki et al. Reference Burki, Kudryavtsev, Matz, Aglyamova, Bulman, Fiers, Keeling and Pawlowski2010; Neuhauser et al. Reference Neuhauser, Kirchmair and Gleason2011; Schwelm et al. Reference Schwelm, Fogelqvist, Knaust, Jülke, Lilja, Bonilla-Rosso, Karlsson, Shevchenko, Dhandapani, Choi, Kim, Park, Lim, Ludwig-Müller and Dixelius2015) Plasmodiophora brasicae, a microbe which attacks members of the Brassicaceae family. Clubroot is an intractable disease affecting this group of crops, which are vitally important sources of fresh and processed vegetables and oil seeds. These crops contain chemicals that are associated with significant improvements in human health. They also provide cooking oils and fats, industrial lubricants, lighting fuels, condiments and flavourings, animal fodder and forage, improved soil fertility and bio-control, while also including ornamental decorative annuals and perennials. Arabidopsis thaliana (thale cress), which is the molecular biologists’ main model species and the first plant whose genome was sequenced, is also included in this family (Dixon Reference Dixon2007) and suffers from clubroot disease, making it a valuable source of information on host–parasite relationships and potentially increasing the pool of resistance genes (Alix et al. Reference Alix, Lariagon, Delourme and Manzanares-Dauleux2007). Advances in understanding the biology of this host–pathogen relationship were described by Dixon (Reference Dixon2006, Reference Dixon2014). The economic significance, impact and biology of this pathogen are reviewed by Dixon (Reference Dixon2009b , Reference Dixon c ; Reference Dixon2014).
Disease incidence
It is evident from the very earliest scientific studies of clubroot and its causal organism P. brassicae in the 19th century by Woronin (Reference Woronin1878, translated by Chupp Reference Chupp1934) that there were associations between fertilizer-use and the incidence and suppession of disease. Woronin, however, could not verify these assertions scientifically. Calcium cyanamide has gained an association for reducing the impact of clubroot disease over the past 100 years. Early studies of the relationship between soil-borne pathogenic microbes and calcium cyanamide showed that regular applications of the fertilizer were associated with reductions in the occurrence and severity of clubroot. Research by Martin (Reference Martin1933) reported considerable reductions in clubroot disease following applications of calcium cyanamide. Subsequently, Walker & Larson (Reference Walker and Larson1935) emphasized the influence of soil conditions in moderating its efficacy, but demonstrated that weight-for-weight, the effect of calcium cyanamide exceeded that of lime (calcium carbonate) by a factor of two. Haenseler & Moyer (Reference Haenseler and Moyer1937) showed in both field and laboratory studies that applications of calcium cyanamide were associated with reductions in the incidence of clubroot disease, and that it had a 2·5-fold greater impact in reducing clubroot compared with hydrated lime. Importantly, Haenseler & Moyer (Reference Hall1937) identified that the effects of calcium cyanamide were affected by the soil environment. Small changes in pH values, soil moisture content, structure and texture affected the level of disease reduction. This served to underline the importance of Crowther & Richardson's (Reference Crowther and Richardson1932) findings that hydrogen-ion concentration in soil regulated the breakdown reactions of calcium cyanamide. The importance of interactions between soil environments, modes of application and the incidence of clubroot disease and its severity were discussed by Colhoun (Reference Colhoun1958) and Karling (Reference Karling1968) in their respective monographs. In farming practice, calcium cyanamide was used regularly for vegetable crops in Great Britain during the 1920s and 1930s (Smith Reference Smith and Smith1961; Elizabeth Gray, personal communication 12 August 1985).
Following World War II, scientific interest in interactions between fertilizers and the reduced severity of soil-borne diseases was largely overtaken by the invention of numerous synthetic agrochemical molecules. These eliminated specific pathogens by inhibiting single enzyme-driven reactions. Attempts at control of clubroot followed this route, with reports of extensive testing of synthetic chemicals, for example Buczacki & Cadd (Reference Buczacki and Cadd1976). More environmentally sensitive approaches returned in the 1980s. Researchers, farmers and growers began recognizing that reducing clubroot disease would be achieved only by IPM. This combined genetic resistance with the manipulation of soil environments, host nutritional status and, where possible, use of synthetic agrochemicals. In the period between 1945 and the early 1980s, practical use of calcium cyanamide as a specialized fertilizer in horticulture continued, particularly in north-western Europe. Here, it was associated with higher crop health status and increased soil fertility (Rieder Reference Rieder1981). Studies restarted in Great Britain in the early 1980s, when it was demonstrated that calcium cyanamide is associated with reductions in the severity of clubroot disease (Dixon & Brokenshire Reference Dixon, Brokenshire and Williams1981; Dixon & Wilson Reference Dixon and Wilson1983; Dixon Reference Dixon2009a , Reference Dixon2012a ).
An evaluation of calcium cyanamide by Williamson & Dyce (Reference Williamson and Dyce1989) studied its effects in swede (B. napus) cultivars of differing resistance to P. brassicae. Disease severity was reduced progressively when increasing amounts of calcium cyanamide were applied. Disease threshold was related to the viable inoculum density, cultivar resistance and the use of calcium cyanamide. The integrated use of calcium cyanamide with boron and forms of nitrogen resulted in the lessening of clubroot severity (Dixon et al. Reference Dixon, Naiki, Webster, Wilson and Williams1987). Calcium cyanamide is reported by Horiuchi et al. (Reference Horiuchi, Hori, Takashi and Shimizu1983) as a useful component when integrated with solarization as a means of reducing inoculum load in P. brassicae-infested land. Similarly, Dixon & Wilson (Reference Dixon and Wilson1983) reported on the successful use of calcium cyanamide in reducing the impact of clubroot on cabbage and Brussels sprouts. This was followed by detailed multi-site and multi-seasonal studies that estimated the reduction in clubroot disease following the use of calcium cyanamide fertilizer, achieving a minimum of 30% improvement in yields (Humpherson-Jones et al. Reference Humpherson-Jones, Dixon, Craig, Ann and Russell1992). At the same time, calcium cyanamide was associated by Naiki & Dixon (Reference Naiki and Dixon1987) with the diminution of disease severity caused by P. brassicae when examined in controlled environment and glasshouse experiments. Reductions in disease severity were related to the interval between application of the fertilizer and planting of susceptible Chinese cabbage (B. rapa spp. pekinensis cvar Granaat) seedlings in pathogen infested soil. Calcium cyanamide also stimulated host growth at all the treatment concentrations used. Subsequently, associations between the use of calcium cyanamide and reductions in the incidence of clubroot disease (P. brassicae) of brassicas has been reviewed by Dixon (Reference Dixon2009a , Reference Dixon2010, Reference Dixon2012a ).
Clubroot developed in the late 1980s and into the 1990s as a significant disease of the Australian vegetable brassica industry, most notably cauliflower and calabrese (green broccoli) crops in Victoria and Western Australia. A system of integrated control was developed that included the use of calcium cyanamide. Applying the fertilizer by banded applications directed into the crop rows planted on raised beds significantly reduced cost through cutting application rates by 66% and reduced the level of disease incidence. The marketable yield of calabrese receiving calcium cyanamide was double that of untreated controls in both 1996 and 1997 in Victoria, indicating that crop growth was improved. This followed earlier work that studied the particle size and application methods for calcium cyanamide used in Australian vegetable production (Donald et al. Reference Donald, Lawrence and Porter2004). These studies showed that calcium cyanamide used with other treatments, especially rapidly acting forms of lime, successfully reduced the intensity of clubroot disease in the field (Donald et al. Reference Donald, Porter, Faggian and Lancaster2006). Subsequent British studies (Harling et al. Reference Harling, Stewart and Gladders2007; Stewart Reference Stewart2008) indicated that combining calcium cyanamide with other bio-fertilizers and formulations of calcium was associated with reductions in clubroot disease on several sites over four seasons.
Donald et al. (Reference Donald, Porter, Faggian and Lancaster2006) also developed a real-time PCR test that quantified inoculum loads and allowed predictions of yield losses. Naiki et al. (Reference Naiki, Kageyama and Ikegami1978) suggested that there is a minimum viable spore density of between 103 and 104 spores per gm of dry soil before root hair infection by P. brassicae leads to consistent disease expression. This result agrees with Garrett's (Reference Garrett1958) theories of minimal inoculum potential being required before there is successful disease development caused by soil-borne pathogens.
Integrated use of calcium cyanamide with lime is advocated by Belec et al. (Reference Belec, Trembaly and Coulombe2004) in Canada and, with the addition of resistant cultivars into an integrated system, was recommended for vegetable brassicas (Anon 2012). Similar reports come from other centres in Canada (McDonald Reference McDonald2002). Working on highly organic muck soils in Ontario, McDonald (Reference McDonald2002) found that calcium cyanamide applications were strongly associated with reductions in clubroot severity, especially when used in combination with applications of boron. The need for coherent means of controlling clubroot disease is highlighted by information now coming from China. Reportedly 0·70–0·80 of land used for brassica crops, which are of major culinary and industrial significance in the provinces of Guangdong, Shandong, Zhejiang, Jiangsu, Hangzhou, Jinhua and Nongbo district of Zhejiang province, is infested with P. brassicae (Chai et al. Reference Chai, Xie, Shi and Li2014). This poses a problem of great urgency for Chinese agriculture. Lime-nitrogen (calcium cyanamide) applications were associated with substantial reductions of clubroot disease in Chinese cabbage, increased yield and grower's income (Benyue Reference Benyue1995).
Clubroot severely limits brassica crop production worldwide and has now gained major footholds in the oilseed rape crops of Canada, China and northern Europe, threatening the viability of one of the world's most significant internationally traded crops (Strelkov & Dixon Reference Strelkov and Dixon2014). Management of P. brassicae is limited by the factors discussed by Dixon (Reference Dixon2014). The distribution of this pathogen seems to be increasing, since disease reports are now coming from countries, which previously had no or very limited occurrence of clubroot, such as Turkey (Apaydin et al. Reference Apaydin, Deligöz, Kar, Kibar and Karaagac2010).
Mode of action
The association of calcium, in the form of lime, with the suppression of clubroot (finger and toe) disease was well established even before the causal organism was identified (Anderson Reference Anderson1855). Thereafter calcium as limes or, to a lesser extent, fertilizers such as calcium cyanamide were recommended as practical means for reducing the progress of clubroot disease (Colhoun Reference Colhoun1958; Karling Reference Karling1968). The mode of action of calcium and associated effects on soil pH has, however, been elucidated only relatively recently. Fletcher et al. (Reference Fletcher, Hims, Archer and Brown1982) recognized that although pH influenced the progress of clubroot disease, this was affected by the concentrations of calcium ions in the soil solution. In California, USA, Campbell et al. (Reference Campbell, Greathead, Myers and de Boer1985) concluded that there was an interaction between pH, extractable calcium and magnesium, which must exceed approximately 14 meq/100 mg of soil from native minerals or with fertilizers, such as calcium cyanamide or lime treatments. These relationships were studied by Dixon & Webster (Reference Dixon and Webster1988) and by Webster & Dixon (Reference Webster and Dixon1991a , Reference Webster and Dixon b ), who demonstrated details of the stages in the life-cycle of P. brassicae and the associated development of pathogenesis that are regulated by calcium ions, pH values and host factors. Each of these components, while affected by the others, has independent effects. These operate throughout the pathogen life-cycle from the germination of motile primary zoospores, penetration and colonization of root hairs through the formation of primary plasmodia, sporangia and then onto the infection of cortical cells and the secondary stages of pathogenesis, which culminate in gall formation. Increasing soil calcium or alkalinity reduces the rate of maturation of P. brassicae in root hairs, retarding its speed and the quantities of plasmodia that form sporangia. But as Myers & Campbell (Reference Myers and Campbell1985) demonstrated, calcium has little impact on the dormant resting spores. Previously, Macfarlane (Reference Macfarlane1958) had demonstrated that in controlled experiments, pH values of 5–6 had little influence on the level of successful infection by primary zoospores penetrating root hairs. Successful infection diminished greatly as pH increased and reached 8·0. This effect was further explained by Donald & Porter (Reference Donald and Porter2004), who showed that at acidic pH values the progress of infection into root hairs was only delayed by the presence of significant amounts of calcium (20 mM). As pH became increasingly alkaline, the amount of calcium required to reduce root hair infection lessened. Subsequently, Takahashi et al. (Reference Takahashi, Ishikawa, Kaido, Takita, Hayakawa, Okazaki, Itoh, Mitsui and Hori2006) found that when P. brassicae encounters resistant cultivars, there is an alkalization of the environment in the rhizosphere that retards the capacity of the pathogen for invasion. Takahashi et al. (Reference Takahashi, Ishikawa, Kaido, Takita, Hayakawa, Okazaki, Itoh, Mitsui and Hori2006) found that cell death in Arabidopsis thaliana-resistant to P. brassicae was associated with increasing alkalization of the root environment and that this did not occur in cultures of susceptible plants. These suggestions were taken further by Niwa et al. (Reference Niwa, Kumei, Nomura, Yoshida, Osaki and Ezawa2007), who emphasized the role of pH in moderating the development of clubroot disease in field experiments. Soils which suppressed P. brassicae had elevated calcium contents, alkaline pH and considerable microbial activity. Webster (Reference Webster1986) found that nitrate-nitrogen could also be associated with reduced root hair invasion by P. brassicae. This might, at least in part, be explained by findings that on root surfaces there is a localized increase in pH associated with nitrate-nitrogen and a decline in pH around root hairs when ammonium is the source of nitrogen (Marschner et al. Reference Marschner, Römheld, Horst and Martin1986).
Primary stages in the interaction of calcium with P. brassicae and the development of clubroot disease are being increasingly understood. Research by Yano et al. (Reference Yano, Tanaka, Kameya-Iwaki and Katumoto1991) for example, quantitatively investigated the relationships between calcium in spore suspensions and effects of inoculation in culture solutions with resting spores; their results suggested that the presence of calcium (as Ca2+ ions) promoted the germination of P. brassicae resting spores. That exposes the resultant delicate primary zoospores to predation by soil-borne bacteria and may also reduce their motility. By analogy with the water moulds (Oomyces), that also rely on flagella for motility, calcium ions in solution adversely affect the movement of zoospores (Donaldson & Deacon Reference Donaldson and Deacon1993). Yano's research offered a clue to the manner by which microbial populations antagonistic towards P. brassicae might be stimulated by the presence of calcium (Yano et al. Reference Yano, Tanaka, Kameya-Iwaki and Katumoto1991).
Suppressive soils
The volume of soil where P. brassicae most probably encounters the greatest numbers of anatagonistic microorganisms is the rhizosphere. This is because the primary zoospores are <1·5 µm in diameter (Cook Reference Cook1933), hence will have limited supplies of energy and not be capable of moving far in soil moisture films from the resting spore to the host root surface (Dixon Reference Dixon2014) in response to host root exudates (Mattey & Dixon Reference Mattey and Dixon2015). It is the suppressive or conducive environment in the rhizosphere, which P. brassicae zoospores encounter as they attempt penetration of the root hairs that determines the success or failure of subsequent invasion and disease development. A generalized description of the rhizosphere was provided by Hinsinger et al. (Reference Hinsinger, Gobran, Gregory and Wenzel2005). This emphasized its complexity, since it is occupied by beneficial as well as pathogenic organisms and plant root systems. Further, the rhizoplane (root surface) and surrounding rhizosphere were noted by Newton et al. (Reference Newton, Fitt, Atkins, Walters and Daniell2010) as “support(ing) complex microbial communities that can influence nutrient availability and the ability of pathogens to colonize roots”. This complexity in the microbial community and resultant suppressibility or conduciveness is influenced by agricultural practices as discussed by Raaijamkers et al. (Reference Raaijmakers, Paulitz, Steinberg, Alabouvette, Moëmme-Loccoz, Dessaux, Hinsinger and Lemanceau2009) and Raaijmakers & Mazzola (Reference Raaijmakers and Mazzola2016). This encourages beneficial rhizosphere microorganisms such as the bacteria Pseudomonas, Burkholderia and Bacillus that adversely affect the population density, dynamics and metabolic activities of soil-borne pathogens (Raaijmakers et al. Reference Raaijmakers, Paulitz, Steinberg, Alabouvette, Moëmme-Loccoz, Dessaux, Hinsinger and Lemanceau2009). Increasing the activities of microorganisms capable of suppressing pathogens is a route by which sustainable husbandry may be achieved, as advocated by Mazzola (Reference Mazzola2004) particularly in relation to take-all disease of cereals (Gaeumannomyces graminis). Research with various soil amendments indicates that stimulation of soil microbial populations encourages chitinolytic bacteria that are capable of degrading the resting spores of P. brassicae because they contain chitin in the cell wall (Buczacki & Moxham Reference Buczacki and Moxham1983). The stimulation of chitinolytic bacteria resulting in the inhibition of diseases caused by soil-borne pathogens is discussed by Dixon & Walsh (Reference Dixon and Walsh1998).
The indirect effects of calcium cyanamide, of stimulating antagonistic microbe populations, which then results in reduced incidence of soil-borne pathogens and the diseases that they incite, was identified for Verticillium albo-atrum, Pythium ultimum and Thielaviopsis basicola by Verona (Reference Verona1970). Applications of calcium cyanamide were demonstrated by Huang & Sun (Reference Huang and Sun1991), to be associated with encouraging bacterial populations in treated soil and in reductions in populations of some other plant pathogenic fungi such as Sclerotinia sclerotiorum, a cause of white rot in a wide range of crops (Jones & Gray Reference Jones and Gray1973). Applying calcium cyanamide to soil also encouraged suppression of F. oxysporum f. sp. cucumerinum (cucumber wilt) (Shi et al. Reference Shi, Wang, Zhou, Yu and Yu2009). It was suggested by Horiuchi et al. (Reference Horiuchi, Hori, Takashi and Shimizu1983) that calcium cyanamide enhanced the suppression of clubroot in association with the use of soil solarization.
Studies of soil-borne bacteria such as Bacillus subtilis established that they are antagonists of P. brassicae (Einhorn et al. Reference Einhorn, Bochow, Huber and Krebs1991). In the 1980s in Taiwan, Hsieh & Wang (Reference Hsieh and Wang1986) examined the components of clubroot-suppressive soils and concluded that while calcium and pH were important factors, the stimulation of populations of antagonistic microbes was also essential. In Taiwan, clubroot-suppressive soils were associated with pH values >7·4 and with a calcium content >1210 ppm. The local irrigation water was found by Hsieh & Wang (Reference Hsieh and Wang1986) to be highly calcareous but they contended that suppressivity was partially related to soil physico-chemical factors such as texture, pH, organic matter content and exchangeable potassium, sodium, magnesium and calcium. However, acidifying soils, which is a means of removing bacteria, was shown by Wang & Hsieh (Reference Wang and Hsieh1986) to reduce their suppressive properties.
Applications of calcium cyanamide were associated with increased numbers of microbes in soil (Allison Reference Allison1924; Mukerji Reference Mukerji1932). Soil biological health, as measured by the amount of amylase and protease activity, increased where calcium cyanamide was used, whereas the opposite effects were obtained with applications of ammonium sulphate (Bosch & Amberger Reference Bosch and Amberger1983). Calcium hydroxide may be released from calcium cyanamide, which then raises alkaline soil pH, further encouraging microbial activity and benefiting soil fertility (Verona Reference Verona1970). The subsequent release of nitrogen via DCD encourages populations of heterotrophic microbes (Nõmmik Reference Nõmmik1958). Overall, the breakdown of calcium cyanamide increases the heterogeneity of soil microbe populations and in turn this raises fertility. This finding supports the early results of Crowther & Richardson (Reference Crowther and Richardson1932) showing that calcium cyanamide is most effective when applied as routine annual applications thereby maintaining environments conducive for increased microbial activity.
More recently, studies of conducive and suppressive soils in Brittany, France, by Rouxel et al. (Reference Rouxel, Briard, Lejeune, Cavalloro and Pelerents1988) established a relationship between pH values, soil moisture, inoculum load and clubroot disease. Rouxel et al. (Reference Rouxel, Briard, Lejeune, Cavalloro and Pelerents1988) also speculated on the role, which microbial biological control agents might play and their interaction with physical characteristics of soil. Page (Reference Page2001) clearly demonstrated that applications of calcium in various forms of lime could be associated with the development of soil suppressivity towards P. brassicae; her Scottish field studies identified the development of soil suppressiveness towards P. brassicae resulting from the interactions between calcium and benign soil microbes. This relationship was explored further by Murakami et al. (Reference Murakami, Tsushima, Kuroyanagi and Shishido2002), who identifed the effects of reducing inoculum load as suppressiveness increased, resulting in reduced disease expression associated with exchangeable soil calcium. A link between calcium and increased microbial activity was developed by Niwa et al. (Reference Niwa, Kumei, Nomura, Yoshida, Osaki and Ezawa2007, Reference Niwa, Nomura, Osaki and Ezawa2008) in relation to suppressive and conducive soils; they demonstrated that calcium is associated with increased microbial activity and reduced germination of P. brassciae resting spores, and in turn this suppresses the development of clubroot disease. Niwa et al. (Reference Niwa, Kumei, Nomura, Yoshida, Osaki and Ezawa2007, Reference Niwa, Nomura, Osaki and Ezawa2008) demonstrated that soil-borne microbes may change their metabolic activities when calcium cyanamide is present. The diversity and species richness of soil populations of beneficial bacteria was enhanced by calcium cyanamide, as Niwa et al. (Reference Niwa, Nomura, Osaki and Ezawa2008) demonstrated by increasing amounts of rRNA fragments. Subsequently, Ma et al. (Reference Ma, Sun, Hu, Yu, Wang and Fu2013) reported that applications of calcium cyanamide encourage soil bacterial community diversity and richness. This could potentially increase soil suppressiveness and probably result in a decline in soil-borne plant pathogens. If suppressiveness is accepted as a component of soil health, then that also implies promoting a broader spectrum of soil inhabitants such as earthworms. A report by Bauchhenb (Reference Bauchhenb1994) then becomes relevant; this work demonstrated that applications of calcium cyanamide caused no adverse effects on populations of several earthworm species and ultimately resulted in increased numbers of these animals. It is also noted that beneficial bacteria such as nitrogen-fixing bradyrhizobia are increased by the presence of calcium cyanamide. Nitrogen fixation, for example, was 50% greater in soybean crops receiving this fertilizer (Tewari et al. Reference Tewari, Suganuma, Fuijikake, Ohtake, Sueyoshi, Takahashi and Ohyama2004).
DISCUSSION AND CONCLUSIONS
Immense challenges will face scientists, farmers and growers over the next 50 years in ensuring food security as human populations expand, land areas for cropping diminish and water supplies for irrigation become more restricted (Dixon Reference Dixon and Letcher2009d ; Reference Dixon2012b ). Confronting these challenges requires larger crop yields without accelerating climate change, soil degradation, water shortages or the further impoverishment of natural biodiversity. Currently, agricultural productivity increases by about 2% annually as a result of scientific improvements, this must rise to 3% if food security worldwide is to be maximized (Dixon Reference Dixon and Letcher2009d , Reference Dixon2012b ; von Braun Reference von Braun2010). Raising the intensity of production should be linked with the protection of the environment (Tollefson Reference Tollefson2010), in which soil management will be of particular importance (Schutter et al. Reference Schutter, Sandeno and Dick2001; Bronick & Lal Reference Bronick and Lal2005). Consequently, the potentialities of currently relatively minor husbandry tools, for example specialized sources of crop nutrients such as calcium cyanamide, should be assessed. Research of this nature is called for by Frank & Groffman (Reference Frank and Groffman2009) in their challenges asking for more information concerning the movement and uptake of nitrogen from the rhizosphere into roots. It is also highlighted by Paustian et al. (Reference Paustian, Lehmann, Ogle, Reay, Robertson and Smith2016), specifically in relation to improved fertilizer-use-efficiency.
Calcium cyanamide fertilizer was the first commercialized source of artificial nitrogen. While the quantities currently produced are far less than those made using the Haber-Bosch process, it has retained a market presence for over a century. During that time the uses of calcium cyanamide have mainly centred on specialized applications for high-value field and glasshouse vegetable and salad crops. Here it has been associated with the promotion of soil health and quality, and reducing the impact of soil-borne pathogens such as P. brassicae (Dixon et al. Reference Dixon, Naiki, Webster, Wilson and Williams1987) or species of Sclerotinia. Additionally, the presence of the dimer DCD in the commercially formulated fertilizer and its formation in soils treated with calcium cyanamide reduces nitrification and slows nitrate pollution. Properties of this fertilizer for slowly releasing nitrogen into the rhizosphere, linked with the ready availability of calcium, encourage the development of microbial diversity and suppressiveness towards soil-borne pathogens. The latter property, in particular, is encouraging interest in calcium cyanamide for application in oilseed rape crops, which are now increasingly damaged by clubroot disease (Dixon Reference Dixon2010; Diederichsen et al. Reference Diederichsen, Frauen and Ludwig-Muller2014). Consequently, there is wider recognition of calcium cyanamide as a potentially valuable component of environmentally sustainable IPM strategies for this destructive disease worldwide, as suggested by Tremblay et al. (Reference Tremblay, Belec, Coulombe and Godin2005) and Donald & Porter (Reference Donald and Porter2014). This strategy involves encouraging suppressive soils containing microorganisms that are antagonistic towards soil-borne pathogens (Dixon & Tilston Reference Dixon, Tilston, Dixon and Tilston2010). Developing soil suppressiveness towards P. brassicae is an established technique, following studies such as those of Arie et al. (Reference Arie, Kobayashi, Okada, Kono and Yamaguchi1998); Einhorn et al. (Reference Einhorn, Bochow, Huber and Krebs1991); Lahlali & Peng (Reference Lahlali and Peng2014) and Lahlali et al. (Reference Lahlali, McGregor, Song, Gossen, Narisawa and Peng2014). Increasingly, accurate means for targetting such fertilizers into the root-zone are becoming available following the development of automated robotic sensing of varying fertilizer requirements across crops through changes in foliar nitrogen status (Gianquinto et al. Reference Gianquinto, Sambo and Bona2003) combined with increased efficiency in granule distribution into the canopy (Antille et al. Reference Antille, Gallar, Miller and Godwin2015), with potential increases in efficacy and cost savings. As a result, the cost is likely to be reduced and efficacy increased.
Artificial nitrogenous fertilizers have made incalculable contributions to human welfare for over a century. This role in crop husbandry is likely to continue, but the manner by which this is achieved will be modified as needs for sustaining environmental security, biodiversity and human health increase. There are already requirements for protecting Nitrate Vulnerable Zones (NVZs) and the dangers of raised nitrate concentrations in crops (Pimpini et al. Reference Pimpini, Venter and Wünsch1970) have been long recognized. Consideration should be given to using nitrogen fertilizer formulations that are not accompanied by these problems (Sieling & Kage Reference Sieling and Kage2010) and which encourage beneficial microorganisms (Yao et al. Reference Yao, He, Wilson and Campbell2000). This improves soil health and quality, which is internationally recognized as means for increasing agricultural productivity and conserving and sustaining biological diversity. Increasingly multi-disciplinary research is providing knowledge, which will enable improved exploitation of the benefits offered by benign soil-inhabiting microbes in the repair and maintenance of soil health.
Agriculture is the sector of human activity most likely to be affected by climate change (Rosenzweig et al. Reference Rosenzweig, Elliott, Deryng, Ruane, Müller, Arneth, Boote, Folberth, Glotter, Khabarov, Neumann, Piontek, Pugh, Schmid, Stehfest, Yang and Jones2014). This assessment is based on a globally consistent protocol-based multi-model, which indicates strong negative effects of climate change, particularly where there are high levels of warming at low latitudes where developing countries are concentrated. The urgency of this situation is further emphasized by the large-scale meta-analysis by Challinor et al. (Reference Challinor, Watson, Lobell, Howden, Smith and Chetri2014) showing the relationship between rising temperatures and declining crop yields in the coming decades. The use of nitrogen fertilization will have particular relevance in mitigating some of these effects. In this process, compounds such as calcium cyanamide, which encourage natural soil microbial anatgonisms towards plant pathogenic organisms and have limited environmental impact, could offer considerable benefits for crop husbandry.
Thanks are given to Mr Paul Corfield (PP Products, United Kingdom) and Dr Hans-Juergen Klasse (AlzChem, Germany) for supplying information. The author is also grateful to the referees and editors for their constructive comments.
