CAB Reviews 2013 8, No. 023 Review Soil food web controls on nitrogen mineralization are influenced by agricultural practices in humid temperate climates

Joann K. Whalen*, Maria L. Kernecker, Ben W. Thomas, Vanita Sachdeva and Christopher Ngosong

Address: Department of Natural Resource Sciences, Macdonald Campus, McGill University, 21 111 Lakeshore Road, Ste-Anne-de- Bellevue, Quebec, H9X 3V9, Canada.

*Correspondence: Joann K. Whalen. Fax. +1 514 398 7990. Email: [email protected]

Received: 16 July 2012 Accepted: 10 March 2013 doi: 10.1079/PAVSNNR20138023

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews g CAB International 2013 (Online ISSN 1749-8848)

Abstract

Agricultural crop production depends upon judicious use of nitrogen (N) fertilizers to sustain yields. Globally, the N recovery rate by crops is about 60%, meaning that the rest of the N applied to agroecosystems is transformed to forms that are not available for crop uptake or are lost to the environment. Considering that part of the soil N supplied to crops comes from biological N2 fixation and mineralization of soil organic N, quantifying these contributions could reduce our reliance on exogenous N inputs. This review examined how the microbially mediated reactions of N mineralization and nitrification contribute to the soil N supply, and biotic controls on these reactions in the soil food web. Potential N mineralization by heterotrophic bacteria and fungi can exceed 10% of the total soil N per year, and ammonium released by mineralization is rapidly transformed to nitrate through the action of chemoautotrophic ammonia oxidizers (bacteria and archaea) followed by heterotrophic and chemoautotrophic nitrifiers (bacteria and fungi). Predation of these micro-organisms, primarily by soil microfauna, accounts for additional release of ammonium, estimated at 32–38% of the annual N mineralization. Soil meso- and macro-fauna also contribute to N mineralization and nitrification by accelerating the decomposition of organic substrates and modifying the soil habitat in ways that favour microbial activity. Tillage, application of organic amendments and improving soil drainage in humid temperate regions should favour N mineralization and nitrification processes in soil food web, whereas agrochemical use is expected to have a negligible effect. In summary, the soil food web contribution to N mineralization needs to be included in the soil N supply concept, which requires the development of field-based measurements and models of the soil N supply.

Keywords: Soil nitrogen cycle, Soil fauna, Soil nitrogen supply

Introduction fixation is from 30 to 50 kg N ha/ year for common bean (Phaseolus sp.) and may reach 170 kg N ha/ year for soy- Agricultural crop growth and yield depends on the avail- bean (Glycine max (L.) Merr.), while forage legumes such as ability of nitrogen (N) for protein synthesis, chlorophyll lucerne (Medicago sativa L.) fix an estimated 50–300 kg N formation, photosynthesis and other essential functions. ha/ year with symbiotic N2-fixing bacteria [1, 2]. These N2 Some agricultural crops, notably legumes, benefit from fixation rates represent 36–88% of the crop N require- associations with symbiotic and free-living N2-fixing bac- ments; the rest of the N required for crop production is + teria that supply a portion of the N required for primary absorbed from the soil solution as ammonium (NH4 ) and 7 production. Globally, N2 fixation provides an estimated nitrate (NO3 ), with free amino acids making a minor 50–70 Tg N/year to support the growth of pasture contribution to plant N nutrition [3, 4]. Since biological and fodder legumes, rice, sugarcane, non-legumes and N2 fixation accounts for only 15–20% of the N input savannahs [1]. In humid temperate climates, the N2 in agroecosystems [1, 5] and most crops grow on soils

http://www.cabi.org/cabreviews 2 CAB Reviews where the naturally-occurring concentrations of plant- reliance on N inputs and improving the N recovery rate? + 7 available NH4 and NO3 are insufficient to achieve This paper will explore these and other questions related maximum yields, other N inputs are needed. to how the soil food web controls N mineralization in Chemical fixation of N2 through the Haber–Bosch agricultural soils, with emphasis on findings from humid process is the starting point for synthesis of inorganic temperate agroecosystems. N fertilizers, the cornerstone of modern agriculture. The objectives of this review are: (1) to investigate how Globally, inorganic N fertilizer consumption increased N mineralization and nitrification processes contribute from 10.8 million tonnes N/year in the 1960s to an esti- to the soil N supply, (2) to determine how the soil food mated 97.9 million tonnes N/year in 2012 [6, 7]. Other web controls N mineralization and nitrification, (3) to N inputs to agroecosystems include manure (13% of determine how agricultural management practices affect global N input), wet and dry atmospheric deposition (11% the structure and functions of the soil food web related of global N input), sedimentation (2.4% of global N input) to N mineralization and nitrification, and (4) to give and crop residue (8.3% of global N input), based on recommendations about how to integrate soil food webs estimates from the year 2000 [8]. The fact that inorganic into our concept of the soil N supply. N fertilizers account for about 50% of the N input for global agricultural production is cause for concern. The chemical N2 fixation process generally relies on natural Microbial Basis of N Transformations gas (methane), a non-renewable energy source, to gen- Contributing to the Soil N Supply erate H2 for the chemical reaction and to heat the reac- tion vessel. Hence, agricultural systems that depend The soil N cycle is a dynamic, multi-trophic cascade heavily on inorganic N fertilizers require more energy to involving abiotic and biotic controls that govern the rates sustain in the long term. Global assessment of N flows in at which organic N compounds are transformed to cropland showed an average N recovery rate of 59% in inorganic N forms, and vice versa. In agroecosystems, crop biomass, indicating that more than 40% of N inputs biological N2 fixation, N mineralization and nitrification are transformed into forms that are not available for plant reactions are the most relevant for crop production uptake or lost from agroecosystems [8]. This imbalance in because these microbially mediated reactions produce the global N cycle means that reactive N is emitted to the inorganic N compounds that can be assimilated by plants. atmosphere or entering aquatic ecosystems, resulting in The next sections will focus mainly on how the soil food unintentional fertilization of non-agricultural ecosystems web affects N mineralization and nitrification, given the [5, 9, 10]. + 7 contribution of NH4 and NO3 from these reactions to One way to counteract these undesirable environ- the soil N supply (kg N/ha), defined as [15]: mental consequences of agricultural production is to increase the N recovery rate, and this can be done by Soil N supply = Mineral N+Crop N+Mineralizable Soil N following good management practices with respect to 1 fertilizer use (e.g., soil testing, diagnostic plant analysis, ð Þ choice of appropriate fertilizer compounds, selection of Mineral N (kg N/ha) is the NH4-N plus NO3-N con- proper nutrient ratios, attention to timing and placement centration of the soil in the potential rooting depth of the of fertilizers). These good management practices can crop, Crop N (kg N/ha) is the N concentration in the be fine-tuned for particular crops according to the 4R crop at the time that soil was sampled for Mineral N nutrient stewardship approach [11] or integrated nutrient measurement, and Mineralizable Soil N (kg N/ha) is the management planning [12]. Another way to improve N estimated amount of N that becomes available for crop recovery rate is to apply fewer N inputs to an agro- uptake from mineralization of soil organic matter during ecosystem and rely on the N supplied from mineralization the growing season, after the time that soil was sampled of soil organic N, resulting from soil biological activity. for Mineral N determination. Research dating from the 1980s suggests that more The soil N supply concept is illustrated in Figure 1. complex soil food webs increase N mineralization from In soil with no exogenous N inputs, the soil N supply + 7 soil organic matter [13, 14], which implies that agro- comes from the soluble NH4 and NO3 pool in the root ecosystems with such soil food webs will require less zone, which is derived primarily from N mineralization, inorganic N fertilizer to achieve optimal crop production. ammonia oxidation and nitrification reactions and sup- But how does the soil food web contribute to the soil N plemented by the biological N2 fixation of free-living, supply, which is defined as the amount of N in the soil associative and symbiotic bacteria. Since the inherent (in addition to that from N inputs) that is available soil N supply is generally insufficient to achieve optimal for uptake by the crop during the growing season, economic yields in humid temperate agroecosystems, taking account of N losses? Can agricultural soils under it becomes important to consider the contribution of N + 7 particular management support an active soil food web inputs to the soluble NH4 and NO3 pool, and to the community that mineralizes N from organic matter in mineralizable soil organic matter pool (Figure 1). In humid synchrony with crop N requirements, thereby reducing temperate regions, the inherent soil N supply comes

http://www.cabi.org/cabreviews Joann K Whalen, Maria L. Kernecker, Ben W. Thomas, Vanita Sachdeva and Christopher Ngosong 3

Figure 1 The nitrogen cycle in agroecosystems, illustrating major exogenous inputs (atmospheric N, inorganic N fertilizer, + manure N and crop residue N; the sediment N input is not shown). The soil N supply to crops includes NH4 originating from + 7 biological N2 fixation and from the NH4 and NO3 pools, which are replenished by N mineralization and nitrification reactions mostly from N mineralization during the growing season Nitrogen mineralization is intricately linked to the (spring and summer), since N mineralized during fall and decomposition of organic matter, since the heterotrophic winter is susceptible to loss in the environment [16]. The micro-organisms responsible for the reaction need car- + 7 NH4 and NO3 concentration in the root zone declines bon (C), N and other nutrients derived from organic with crop N uptake and when these reactive N forms matter to support their metabolic functions, growth and + are transformed through abiotic reactions (e.g., NH4 reproduction. As described by Schimel and Bennett [21], fixation on clays), biotic processes (e.g., immobilization in decomposition of organic matter is the depolymerization microbial biomass) or lost in gaseous forms and water of organic soil polymers by extracellular enzymes, fol- (Figure 1). lowed by their degradation to monomeric compounds such as amino acids, amines, amino sugars and urea Nitrogen Mineralization (Figure 2). Since less than 15% of the total N pool is potentially mineralizable, this suggests that depolymer- In the cool humid soils of eastern Canada, the soil organic ization is the rate-limiting step in the reaction. The reg- matter contains 4408–11 455 g organic C/m2 and between ulatory gate hypothesis [22] indicates that abiotic factors 359 and 1008 g total N/m2 [17]. Only a fraction of the such as those listed in Figure 2 control the rate limiting organic N pool is mineralized during the growing season, step in the reaction, which seems to be the case for C as most of the organic N is physically or chemically pro- mineralization [23] but is not yet confirmed for N tected from decomposition. In potato fields on sandy mineralization. soils, the potentially mineralizable N pool was 3.8–13% of After monomeric compounds are cleaved from com- + the total N pool [18], while the potentially mineralizable plex polymers, they may be degraded to NH4 through N pool was 7–10% of the total N pool on medium – to the action of abiotic enzymes (e.g., urease) present in heavy-textured soils under forage grass production with a soil solution or associated with soil organo-mineral history of manure application [19]. In those studies, the complexes [24]. Monomeric compounds are also absor- potentially mineralizable N pool was determined after bed by microbial cells and undergo ammonification to + aerobic soil incubation for 24 weeks at 25C, one yield NH4 as the end product of the reaction. Soil of the laboratory-based methods used to evaluate N microbes are proposed to assimilate N via two pathways: mineralization [20]. (1) the mineralization–immobilization–turnover (MIT)

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Figure 2 Soil N mineralization and nitrification reactions, showing depolymerization as the rate limiting step in the con- version of soil organic matter to monomeric N compounds, a small fraction of which is absorbed directly by plants, and the + remainder is transformed by microbes directly or through the MIT (mineralization-immobilization-turnover) route to NH4 + (adapted from [21]). Soil fauna control microbial communities through predation, which releases additional NH4 into the soil solution. Other biotic and abiotic factors controlling these reactions are listed route, indicated in Figure 2, and (2) the direct route. The estimated 30% of N mineralization under field conditions MIT route involves extracellular deamination of organic N [30]. Soil protists assimilate 10–40% of the microbial C + and ammonification of NH4 before it is assimilated by consumed and nematodes use an estimated 50–70% of soil bacteria, which is thought to occur when mineral N microbial C consumed [31, 32], which results in lysed availability is high [25]. The direct route occurs when microbial cells and cellular contents returning to the soil monomers (e.g., amino acids, amino sugars) are directly organic matter and monomeric N pools (Figure 2). When assimilated and deaminated inside bacterial cells, and N protists and nematodes prey on N-rich bacteria, they exceeding physiological requirements is actively excreted consume more N than their nutritional requirements and + + into the soil NH4 pool [25, 26]. It is hypothesized that release excess NH4 into the soil solution (Figure 2), both pathways operate concurrently, but within different which is available for plant uptake or other transforma- + microsites in heterogeneous soils [27, 28]. Surplus NH4 tions in the N cycle. Predation by larger soil fauna may + released from microbial biomass enters the NH4 pool, alter the growth pattern and enzyme production of soil where it is available for plant uptake or undergoes other micro-organisms, leading to higher protease and arginine transformations. deaminase activities in forest soil mesocosms with When organic N is transformed via the direct route, mesofauna [33, 34]. However, the stimulation or sup- the N immobilized in microbial cells can be released pression of N mineralization and other functions of the + as NH4 when those micro-organisms are consumed soil microbial community by predators appears to depend (predated) by protists and nematodes [29], as illustrated on the composition of available substrates and the mineral in Figure 2. Predation by soil fauna contributes an N concentration [34, 35]. Another way that soil fauna

http://www.cabi.org/cabreviews Joann K Whalen, Maria L. Kernecker, Ben W. Thomas, Vanita Sachdeva and Christopher Ngosong 5 affect N mineralization is by fragmenting, mixing and soil micro-organisms, but whether this is predation or a redistributing organic matter in the soil, which can bring consequence of their preference for palatable, partially the microbial community in contact with substrates or decomposed organic substrates with certain physical size create habitats (e.g., faecal pellets, burrow linings) that are (because of ease of ingestion) is not clear. Feeding rates favourable microsites for decomposition and N miner- are consistently high at lower trophic levels (e.g., micro- alization [36]. Soil food web interactions that moderate fauna) and relatively low at the higher trophic levels [39]. microbially mediated N transformations will be discussed For this reason, we consider microfauna to be the primary in more detail below. predators of soil micro-organisms involved in N cycling (Figure 3). The other way that soil fauna influence the activity of Nitrification heterotrophic and chemoautotrophic micro-organisms involved in N transformations is through the alteration In well-aerated mineral soils, including those in humid of organic substrates and the soil habitat (Figure 3). + temperate agroecosystems, the NH4 concentration Soil meso- and macro-fauna are well known for their is generally less than 10 mg NH4-N/kg [personal obser- manipulation of surface litter – they fragment fresh and + 7 vation] because NH4 is rapidly converted to NO3 partially decomposed residues, then mix some of those through nitrification [37]. Two groups of chemoauto- residues with soil by burying them [36, 38]. Later, they trophic micro-organisms are involved: (1) ammonia oxi- may return to eat the well-decomposed residue. Ingest- dizers, which catalyse the ammonia oxidation and ing fresh or partially decomposed residues, along with + hydroxylamine oxidation reactions (converts NH4 to mineral soil, is another way that residues come into 7 NH2OH and then NO2 ), and (2) nitrifiers that oxidize contact with decomposer micro-organisms. Faunal- 7 7 NO2 to NO3 . There is considerable diversity in the mediated inoculation of residue is expected to speed chemoautotrophs that derive energy from these reac- depolymerization and release of soluble substrates as the tions, with representative species from the autotrophic residue passes through the intestinal tract, or after faecal bacteria, archaea and heterotrophic bacteria among pellets are deposited on the soil surface or within the the ammonia oxidizers; nitrifiers include autotrophic soil profile [40]. Finally, soil meso- and macro-fauna can bacteria, heterotrophic bacteria and heterotrophic fungi physically modify the soil environment because their [38]. The diversity in these groups implies that ammonia faecal deposits are newly-formed macroaggregates, a oxidation and nitrification should occur over a wide range favourable habitat for soil micro-organisms, particularly of soil conditions, although these biological reactions aggregates with mean diameter from 250 to 425 mm will be affected by abiotic and biotic soil factors, as [41]. In addition, macrofauna burrows are macropores listed in Figure 2. The ammonia oxidation reaction is of (>10 mm diameter) that serve as conduits for water interest because it generates byproducts – nitroxyl rad- infiltration and gas exchange in the soil profile, which can icals (HNO), nitric oxide (NO(g)) and nitrous oxide indirectly affect the activity of micro-organisms involved (N2O(g)) – and the gaseous byproducts are susceptible to in soil N transformations [38]. 7 loss from soil. Nitrification produces NO3 , which can be assimilated by plants or immobilized in microbial biomass, but is not strongly bound to the soil matrix and therefore Predation as a Control on Soil N Mineralization is prone to loss via leaching or denitrification after rainfall and Nitrification and irrigation events. A classic microcosm experiment by Ingham et al. [42] demonstrated a 30% increase in soil mineral N con- Soil Food Web: Moderating the Microbially centration and 60% greater plant biomass (shoots and Mediated N Transformations roots of Bouteloua gracilis, a perennial C4 grass) when bacterial-feeding nematodes were introduced to micro- How does the soil food web moderate microbially cosms with plants and bacteria. However, the addition of mediated N transformations that are important for the fungal-feeding nematodes had negligible impact on the soil soil N supply? As illustrated in Figure 2, soil fauna interact mineral N concentration and plant biomass [42]. In a with heterotrophic micro-organisms to accelerate the N shortgrass prairie, Hunt et al. [43] estimated that bacteria + mineralization rate and increase the amount of NH4 were primarily responsible for N mineralization, releasing released in the soil solution, which can undergo further 4.5 g N/m2/year, while fungi contributed 0.3 g N/m2/year. transformation by chemoautotrophic ammonia oxidizers Predation by amoebae and bacterial-feeding nematodes and nitrifiers. Predation of soil micro-organisms by soil also contributed to N mineralization, with an additional microfauna (mainly protists and nematodes [31, 32]) can 2.9 g N/m2/year released by these predators [43]. alter the metabolic activity, population structure, com- Protists are the most effective bacterial predators because petitive and mutualistic interactions in the soil microbial they have short generation times (minimum of 2–4 h), community. Larger meso- and macro-fauna also consume large populations and high production rates (10–12 times

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Figure 3 Soil food web controls on the microbially mediated N mineralizaton and nitrification reactions, showing the importance of predation dominated by the microfauna (protists, bacterial – and fungal-feeding nematodes, underlined) as well as substrate quality and soil habitat modification by soil meso- and macrofauna, predominantly earthworms (under- the standing biomass per year) [44]. In a dryland wheat ivorous nematodes to predaceous nematodes, then agroecosystem, N mineralization from bacteria to nematophagous mites, and finally to predaceous mites) and fungi released 10.1 g N/m2/year and an additional in a shortgrass prairie [43], which implies that food webs 4.9 g N/m2/year came from predation, probably by pro- with predators at several trophic levels will stimulate + tists because they were more abundant (7-fold more NH4 release to the soil solution, since very little of it is biomass) than nematodes and microarthropods [45]. A retained in their biomass. portion of the N consumed by a microfaunal predator is The N mineralization from predation contributes to the retained within its biomass and may be recycled when the soil N supply, as demonstrated in controlled studies organism dies, or transferred to higher trophic levels where plant N uptake and biomass accumulation were within the soil food web. Only 2–3% of N was transferred enhanced in the presence of predators such as protists from lower to higher trophic levels (e.g., from bacter- [46], microbial-feeding nematodes [47], enchytraeids and

http://www.cabi.org/cabreviews Joann K Whalen, Maria L. Kernecker, Ben W. Thomas, Vanita Sachdeva and Christopher Ngosong 7 + microarthropods [48]. Yet in experimental microcosms alized NH4 may be taken up by the crop or it could with simulated forest soil and poplar (Populus trichocarpa), undergo nitrification. Still, most annual crops can access 7 soil microfauna did not seem to be important for N NO3 that moves to the rhizosphere by mass flow. mineralization because greater plant N uptake and bio- Nitrate assimilated is a highly regulated energy-dependent 7 mass accumulation occurred when soil micro-, meso- and process that involves active transport of NO3 through 7 macrofauna were present [49]. This suggests that pre- epidermal and cortical cells into the cytosol; next NO3 dation is often, but not always, controlling soil N miner- crosses the endodermis and moves through the xylem alization. to leaf cells where it is reduced to ammonia and then The previous examples demonstrate the net effect incorporated into glutamine for protein synthesis and 7 of predation on the soil N supply, but we also need to other metabolic functions [56]. However, NO3 losses consider the interspecific interactions between predators from leaching and denitrification during the growing sea- and their prey. Changes in bacterial morphology in re- son and in the post-harvest period are common in sponse to predation by protists can lead to larger or annually cropped agroecosystems in humid temperate smaller cell sizes, outgrowths of filamentous bacterial regions of Canada [57, 58], which implies that the soil N cells and microcolonies that the protists apparently supply from N fertilizer and from N mineralization with a + cannot digest effectively [50]. Selective predation on bacterial-dominated food web provides more NH4 and 7 older, larger bacterial cells can provide opportunities for NO3 than needed for plant uptake and often leads to N the growth of younger cells with higher metabolic activity losses. [30]. Predation by protists often stimulates nitrifying In contrast, a fungal-dominated food web has a slower 7 bacteria and leads to high NO3 concentrations in the N mineralization rate and retains more N in the soil- rhizosphere [51], which could be the result of greater plant system [59, 60], which led de Vries and Bardgett + availability of NH4 , selective removal of fast-growing [61] to propose a variety of management options to bacterial competitors, or sensory signals exchanged promote fungal-based soil food webs and plant-microbial between bacteria and plants when predators are present. linkages, thereby reducing N losses from agroecosys- Phillips et al. [52] proposed that the N2-fixing bacteria tems. Not only do larger fungal populations have sub- Sinorhizobium meliloti would respond to nematode pre- stantial capacity to immobilize added NH4NO3 fertilizer dation by producing sensory signals, warning signals and in their biomass [60], but fungal predators such as fun- exudation factors that could induce a response from a givorous nematodes and collembola have longer gen- host plant (e.g., secretion of nematode-repelling com- eration times, smaller populations and biomass than pounds by the plant, induction of nodulation genes) and bacterial predators [44]. This further lengthens the time thereby protect some of the bacterial population from that N is retained within the soil food web and hence the predator. This concept is consistent with the idea protected from loss. Restructuring the soil microbial of bacterial quorum sensing, in which the production, community to favour greater fungal abundance in detection and response to specific molecular signals agroecosystems can be achieved by manipulating abiotic (bacteria–bacteria, plant–bacteria and others) regulates factors such as the amount and chemical composition of gene expression [53]. The soil N supply may be partially C and N contained in detritus, inorganic N inputs, tillage controlled by plant–bacteria signalling since proteo- intensity and other agricultural practices [61]. However, bacterial signal molecules (acyl-homoserine lactones) it is not clear whether such interventions can be were linked to the production and activity of extra- accomplished without compromising crop yields. In cellular chitinase and protease enzymes responsible humid temperate regions, ideally the soil food web for organic N depolymerization in the rhizosphere structure would be dynamic and shift from bacterial- of oat seedlings [54]. Future research into bacterial dominated during the growing season (i.e., to promote N contributions to the soil N supply should consider the mineralization for crop production) to fungal-dominated multi-trophic interactions in the soil food web and plant in the post-harvest and overwinter period (i.e., to systems, from molecular to community levels. increase N retention). Selecting management practices The bacterial-dominated food web described above is that promote such soil food web dynamics requires a linked to a faster rate of N cycling than fungal-dominated deeper understanding of interactions between fungi and food webs [55]. A bacterial-dominated food web could bacteria, such as competition for simple and complex be advantageous when growing annual grain, oilseed or substrates such as root exudates and cellulose, mutua- vegetable crops in humid temperate climates since most listic interactions (e.g., cometabolism in lignocellulosic of those crops will require ample N and reach physio- degradation, bacteria that consume fungal exudates, logical maturity within 100–120 days under field con- endosymbiosis) and parasitism (e.g., mycophagy, decom- ditions. Depending on when the bacterial-mediated N position of fungal cell walls) [62]. Also, we do not know mineralization occurs during the growing season and how predators in the soil food web affect the activities of where in the soil profile, relative to the rhizosphere and recently discovered ammonia-oxidizing soil archaea in particularly young unsuberized root tips that actively the phyla Crenarchaeota and Thaumarchaeota [63, 64], + assimilate NH4 through root interception, the miner- so this remains an open research question.

http://www.cabi.org/cabreviews 8 CAB Reviews Substrate Quality and Habitat Modification as environment [38], which is often favourable for hetero- Controls on Soil N Mineralization and Nitrification trophs and chemoautotrophs involved in N mineralization and nitrification. For example, the casts deposited by Heterotrophic micro-organisms involved in N miner- earthworms on the soil surface or within the soil profile alization require ample substrates for growth and repro- support larger microbial populations owing to higher duction, primarily organic C as an energy source and for organic matter content and moisture than the bulk soil. metabolic processes. Soil organic matter, root exudates, Greater microbial biomass, higher N mineralization rates manure, crop litter and other organic substrates may be and higher nitrification rates are reported in casts used, as long as they are physically accessible and the [71, 72] and middens [73], relative to bulk soil. The lining micro-organism can produce the necessary exoenzymes of earthworm burrows is cemented with mucus, to cleave simple substrates from complex polymers. which serves as a substrate for microbial growth. Under Microbial metabolism also requires C and N in fixed laboratory conditions, nitrification rates were 20-fold proportions, based on the C : N ratio of the microbial cell higher in the burrow lining than in bulk soil [74]. Since (from 5 : 1 to 8 : 1 in bacterial cells; between 9 : 1 and 22 : 1 burrows function as macropores, the environment is well in fungal cells [38]). Consequently, micro-organisms may aerated, which should favour ammonia oxidation by not degrade a C-rich substrate if they cannot obtain the chemoautotrophic bacteria and archaea, followed sufficient N from the substrate or immobilize enough by nitrification by chemoautotrophic and heterotrophic + 7 NH4 and NO3 from the soil solution to support their micro-organisms. metabolic processes. In model soil food webs, increasing the C:N ratio of organic matter from 10 : 1 to 12.5 : 1 + reduced the N mineralization rates because more NH4 Agricultural Practices Impacting Soil Food was immobilized, whereas N mineralization rates Web Structure and Functions increased by 38% when the C:N ratio of bacterial biomass increased from 4 : 1 to 5 : 1 [65]. The previous sections described how predation and Fragmentation, consumption and mixing organic sub- modification of substrate quality and habitat by soil fauna strates with soil are ways that soil meso- and macro-fauna can accelerate microbially mediated N mineralization speed up decomposition and N mineralization processes. and nitrification. Much of the evidence to support this Increasing the surface area of litter and other organic notion is based on controlled laboratory experiments in materials allows it to be more readily colonized by het- homogenous (sieved) soils without much disturbance erotrophic bacteria and fungi [66]. In humid temperate (i.e., constant soil temperature and moisture) and often regions, earthworms are responsible for this process, without plants. Field soils have heterogeneous physical, with collembola and microarthropods contributing to a chemical and biological properties, even at relatively small lesser extent. Soil meso- and macro-fauna also facilitate spatial scales, while agroecosystems in humid temperate contact between soil micro-organisms and organic sub- regions are subject to changing temperatures and irre- strates. For example, earthworms consume soil, which gular rainfall events, and are planted with crops of eco- contains micro-organisms, along with fresh or partially nomic importance such as corn, soybean and other decomposed organic matter. After grinding in the gizzard, oilseeds, cereals, forages and potatoes. In addition, agri- the mixture is bathed in a solution of intestinal mucus cultural activities such as tillage, organic residue manage- containing water, electrolytes, glycoproteins, mucopoly- ment, agrochemical application and water management saccharides, lectins and haemocyanin [67]. Some of water may cause disturbance to the soil food web, or they may and nutrients are resorbed in the hindgut and procto- favour some organisms disproportionately. For better deum, but fresh casts excreted by the earthworm are predictions about the soil N supply, we require informa- + 7 generally wetter and enriched in NH4 and NO3 relative tion about how these agricultural practices influence to the bulk soil [68]. Soil leaving the earthworm gut has the soil food web structure and its functions related to more gram positive bacteria, gram negative bacteria and N mineralization and nitrification. eukaryotes than the bulk soil, as well as fewer fatty acids derived from plant material [69]. Faecal pellets from ori- batid mites had a lower lignin : N ratio than the original Tillage + litter and the presence of mites increased NH4 con- 7 centration by 4.9 times and NO3 concentration by Tillage is the mechanical manipulation of soil to prepare 35 times, after 34 d incubation with corn litter [70]. the seedbed, control weeds and incorporate agricultural This indicates that ingestion of organic substrates by chemicals and amendments in soil [75, 76]. Plough pans, soil meso- and macro-fauna favours N mineralization and rotary harrows and other tillage machinery are used to nitrification. reduce soil compaction and remove excessive surface Physical modification of the soil habitat by soil fauna can residues prior to planting the field. Thorough mixing of bring soil micro-organisms in contact with organic sub- surface residues and other materials in the plough layer strates or change the structure and porosity of the soil (generally 10–20 cm depth, depending on the machinery

http://www.cabi.org/cabreviews Joann K Whalen, Maria L. Kernecker, Ben W. Thomas, Vanita Sachdeva and Christopher Ngosong 9 used) can mitigate stratification of nutrients and soil [83]. No-till and strip-tillage alters the trophic structure organic matter, thereby homogenizing soil conditions in of soil nematodes, favouring bacterivorous and fungivor- this part of the crop root zone. Tillage practices may be ous nematodes and inhibiting herbivorous nematodes, intensive (e.g., mouldboard ploughing in the fall, following likely the result of the presence of predatory mites by one or more harrowing events in the spring) or [84, 85] and detritivorous isopods and amphipods that producers may choose to employ conservation tillage, aid in the decomposition of recalcitrant substrates for instance with a chisel plough or disk harrow, or even [85]. Tillage temporarily modifies the soil structure by no-tillage where the soil is undisturbed except for disrupting macroaggregates and causes localized com- small slots opened to plant seeds and apply fertilizer [76]. paction, so amoeba and other protists that inhabit Tillage replaces the functions of soil macrofauna by frag- the aggregate pore space will be impacted in the short- menting and mixing surface litter in the plough layer and term [86]. aerating the soil. A review of more than 100 studies of soil biota in Intensive tillage has a pronounced effect on macrofauna, intensively tilled and no-till agroecosystems [83] revealed particularly earthworms and beetles. For example, abra- that soil fauna with larger body size are more inhibited sion by plough pans and rotary harrows can kill earth- by tillage than those with a smaller body size. In addition worms [77], while soil compaction in wheel tracks of farm to the physical disturbance to large soil fauna caused by machinery can crush earthworms to death [78]. Turning tillage, two other reasons have been proposed to explain the soil exposes soil-dwelling earthworms to direct sun- this observation: (1) after organic substrates incorporated light and warmer, drier conditions at the soil surface, by tillage are metabolized by bacteria, food availability which can cause desiccation [76] and they also become declines, inducing a tropic cascade that results in dimin- vulnerable to predators, particularly birds. Carabid bee- ished food supply for their predators, as well as top-level tles are surface dwelling macroarthropods that live in detritivores, and (2) smaller organisms have a short life surface litter; when this litter is incorporated into deeper spans and recover quickly from tillage disturbance. soil horizons during tillage, beetles may be buried as well Intensive tillage generally favours bacterial decom- and those that survive the tillage operation will find their posers due to the mixing of fragmented surface litter in preferred habitat reduced or eliminated [79]. The inten- the soil profile, increasing the surface area for coloniza- sity and frequency of tillage events, as well as the organ- tion, with a corresponding increase in predatory protists ism’s response to tillage, determines whether tillage will that creates a positive feedback for decomposition and N have a temporary or persistent impact on the soil food mineralization [87]. The burst of soil respiration following web. Bostro¨m [80] reported a 73–77% reduction in tillage points to rapid growth of heterotrophic bacteria in earthworm populations dominated by the endogeic response to substrate availability and favourable soil earthworm Aporrectodea caliginosa following the rotary conditions. Ammonia oxidizers and nitrifiers also respond 7 cultivation and ploughing of meadow fescue and alfalfa positively to tillage, which generates a peak in the NO3 hayfields. One year later, the earthworm biomass (pre- concentration following tillage operations. Whereas til- dominantly individuals of A. caliginosa) was the same as in lage mechanically disrupts the fungal hyphal network, the the undisturbed, unploughed alfalfa hayfield. It appeared conditions in no-tillage agroecosystems (intact surface that crop residues incorporated by tillage provided ample litter, undisturbed soil profile) lead to soil organic C organic substrates to support reestablishment of this accumulation, larger soil microbial biomass and support endogeic earthworm species. However, intensive and fungal-mediated decomposition and N mineralization frequent tillage generally reduces populations of anecic [87, 88]. In the field, N mineralization and nitrification earthworms, likely because the surface litter that serves rates should be greater in intensively tilled than no-till as their primary food source is fragmented and mixed into agroecosystems owing to positive response of bacteria the topsoil by tillage implements [81]. and their protist predators to tillage [43]. The decline in Soil micro- and mesofauna can also be affected by til- soil meso- and macro-fauna populations resulting from lage, owing to modification or destruction of the soil intensive tillage probably have relatively little effect on the habitat, exposure to frost, dryness or heat, and changes in N mineralization rate, according to Andre´n et al [89]. the availability of organic substrates [82]. Soil mesofauna, Reports of greater potential N mineralization in soils including collembola, cryptostigmatid mites and meso- under long-term no-tillage compared with intensive tillage stigmatid mites, tend to be impacted negatively by tillage [90–92] probably reflect the accumulation of labile soil + because they cannot tolerate changes in the soil physical organic N in no-till soils that is transformed to NH4 and 7 environment and become trapped in the soil profile when NO3 when soils are disturbed (i.e., sieved to disrupt pores are disrupted [83]. However, enchytraeid popula- macro-aggregates) and incubated under favourable con- tions often increase following tillage, perhaps because ditions for microbial growth in the laboratory. In con- they are normally constrained by competition for food clusion, tillage is expected to alter the soil food web resources with larger detritivores such as earthworms, structure and increase the bacterial contribution to N and the decrease in earthworm numbers following tillage mineralization and nitrification in humid temperate gives the enchytraeids access to more organic substrates regions.

http://www.cabi.org/cabreviews 10 CAB Reviews Organic amendments to greater root growth and exudation during the growing season and more residues left in the field after harvest Depletion of soil organic C in intensively cultivated [38]. Non-mineralized organic C and N from organic agroecosystems can be counteracted by applying organic amendments is retained in soil, contributing to the for- amendments such as green manure, animal manure, mation of macroaggregates that are a preferred habitat farmyard compost and retaining a greater proportion of for certain micro-organisms and microfauna, improving crop residues in the field [93, 94]. Organic amendments soil structure and aeration, and increasing the soil contain organic C, N and other essential plant nutrients, organic matter content [103, 104]. In conclusion, organic so can be used to partially meet the nutritional require- amendments are predicted to increase the size and ments of agricultural crops if they can be decomposed activity of the soil food web, primarily by serving as an + 7 to yield NH4 and NO3 or solubilized to release non- input of organic N that can readily undergo N miner- covalently bound cations and anions (e.g., K+,Ca2+,Mg2+ alization and nitrification in humid temperate regions. and most micronutrients). Organic amendments become accessible to soil micro-organisms after they are incor- Agrochemicals porated in the soil by tillage or processed by soil mac- rofauna, so these organic substrates should promote Agrochemicals such as inorganic N fertilizers and pesti- growth of soil microbial populations and create a positive cides are popular inputs in agroecosystems of humid feedback in the soil food web. Organic amendments temperate regions owing to the demand for plant-avail- increase the abundance of soil micro-organisms [95–97], able N to achieve economic crop yields and the need to protists, nematodes, microarthropods and earthworms control weeds and other pests that compete with or [98–100]. Reports of greater microbial diversity following damage crops. When applied in sufficiently large doses, application of organic amendments could be related to some agrochemicals may prove toxic to organisms in laboratory methods (i.e., microbial populations grew large the soil food web, which can alter population dynamics, enough to be detected when they received ample organic community structure and diversity in the soil food web substrates) or introduced species coming from manure [9, 55, 87]. However, soil food web organisms are seldom and off-farm amendments [101]. the target of agrochemicals applied for crop nutrition Agricultural producers generally apply organic amend- and crop protection, so effects on the soil food web are ments with low C:N ratios to avoid immobilization of expected to be indirect and the result of feedbacks in the NH + and NO 7 from the soil solution as the material 4 3 soil-plant system [105]. Regardless, inorganic N fertilizers decomposes in the field. Animal manure and farmyard and pesticides applied to agroecosystems alter interac- compost have C:N ratios between 3 : 1 and 25 : 1 (lower tions between the aboveground and belowground values from liquid manure and slurry, higher values from soil food web, which can reduce [106] or increase [107] well-decomposed compost). In humid temperate agro- soil N mineralization rates, thereby impacting the soil N ecosystems, organic amendments with these character- supply. istics are decomposed by micro-organisms and other soil food web organisms during the growing season, releasing from 15 to 75% of the total organic N into soil solution Inorganic N Fertilizers + 7 as NH4 and NO3 [102]. Variation in N mineralization is the result of the C:N ratio of the organic amend- Although minerals can be mined to produce inorganic N ment (less N mineralization from materials with higher fertilizer (notably sodium nitrate or ‘Chile saltpetre’), C:N ratio), soil type (greater N mineralization from sandy most agricultural producers rely on inorganic N fertilizers and loamy soils than clayey soils) and the crop grown in derived from the Haber–Bosch process to fertilize the field (maize, oilseed rape and grass-based hayfields their crops. A variety of inorganic N fertilizers can be have greater N recovery than potatoes and cereal crops) purchased, including anhydrous ammonia, ammonium [103]. Decomposition and N mineralization from green sulphate, calcium ammonium nitrate and mixed nitrogen– manure probably follows the same trend as animal man- phosphorus fertilizers such as monoammonium phos- ure, since green manures are generally N-rich legumes phate and diammonium phosphate [38]. Inorganic N with C:N ratios below 15 : 1, but it depends on the fertilizers are water soluble, meaning that they are quickly + 7 lignocellulose content of the green manure at the time dissolved and release NH4 and NO3 into the soil of incorporation because lignocellulose acts as a barrier solution. Urea (CO(NH2)2) produced by the Haber– to decomposition [38]. Bosch process is an organic N fertilizer that must be + Mineralizable N contained in organic amendments is hydrolysed by urease before releasing NH4 into the soil + 7 transformed to NH4 and NO3 during the growing solution. season, as part of the soil N supply for plant uptake When applied to agroecosystems at agronomic or subject to other transformations in the N cycle. rates (generally less than 200 kg N/ha [15, 94]), inorganic Feedbacks between well-fertilized plants and soil food N fertilizers are not expected to have a direct effect + 7 web organisms are expected to be positive, owing on soil food web organisms because NH4 and NO3

http://www.cabi.org/cabreviews Joann K Whalen, Maria L. Kernecker, Ben W. Thomas, Vanita Sachdeva and Christopher Ngosong 11 solubilized from inorganic N fertilizers at these rates are chloropicrin, dazomet, metam sodium and metam potas- not toxic to soil organisms. Inorganic N is utilized as a sium and may be applied prior to planting crops, in substrate by ammonia oxidizers and nitrifiers in well- woodlots, nurseries, seed beds and turf [114]. aerated mineral soils when their preferred C substrates Soil fumigants generally act as a broad-spectrum con- are available (depending on whether their metabolism is trol for pests or pathogens such as insects, nematodes, heterotrophic or chemoautotrophic). The conversion of bacteria and fungi, thereby directly impacting these groups + 7 NH4 to NO3 through these microbially mediated of soil food web organisms. A study of N mineralization reactions appears to occur rapidly and dominate in agri- and nitrification rates in soils fumigated with a mixture cultural soils in the humid temperate regions, based on 1,3-dichloropropane and 1,3-dichloropropene showed evidence from natural abundance d15N stable isotopes both short- and long-term N mineralization rates were 7 and the fact that more than 50% of the NO3 leaching stimulated by fumigation, whereas nitrification was inhib- from these systems was the product of nitrification, not ited completely for at least 3 weeks in all soils, and lost directly from applied fertilizers [108]. the reduction in nitrification was maintained for up to By contributing to the soil N supply, inorganic N 17 weeks in one soil [115]. In contrast, most of commonly fertilizers stimulate crop growth and yield, which gen- used pesticides in Canada (herbicides, fungicides and erates a positive feedback for the soil food web (more insecticides) are non-target for soil food web organisms, root growth, more rhizodeposition, more crop residues but they should alleviate crop stress and thereby elicit a remaining in the field after harvest), similar to the effect positive feedback with the soil food web community described for organic amendments. However, long-term (healthier plants produce more roots, more rhizodeposits application of NH3-based fertilizers like anhydrous and leave more crop residues in the field after harvest); as ammonia and urea can lower soil pH owing to H+ gen- well, dead weed biomass constitutes an organic substrate eration during the nitrification process [109], which for the soil food web. In this regard, herbicide application could be deleterious to soil food web organisms that are may have a similar effect on the soil food web as the sensitive to acidic conditions (e.g., actinobacteria, earth- application of surface mulch, although the organic input worms) as well as biochemical processes in the N cycle from dead weed biomass is probably lower and patchy in [38]. In plots receiving ammonium nitrate fertilizer, N the field, compared with mulch. Modern pesticides have a mineralization was not affected by soil pH (ranged from half-life of days, weeks or months in the soil–plant system, 4.7 to 6.6), but nitrification was reduced by 75–85% at which implies that they are rapidly degraded as organic pH 4.7 compared with pH 6.6 [110]. Similarly, plots that substrates by soil micro-organisms. A few pesticides are were acidified to pH 4.5 by 10 years of anhydrous more persistent or susceptible to loss from soil, such as ammonia showed no difference in N mineralization but a chlorothalonil (fungicide) and the insecticides azinphos- 42% drop in the potential nitrification rate measured methyl, permethin, chlorpyrifos and diazinon, which were in the laboratory [111]. The decline in nitrification in found in Canadian aquatic ecosystems in concentrations soils with low pH is likely due to inhibition of ammonia that exceeded water quality and science-based benchmark oxidation, as chemoautotrophic bacteria and archaea limits [114]. seem to be sensitive to pH [112, 113]. In conclusion, Glyphosate is the most commonly applied herbicide in application of inorganic N fertilizers is expected to Canada [114] and has a C:N ratio of 3 : 1 [116]. Although stimulate nitrification directly and contribute indirectly glyphosate is not directly applied to soil, exposure in the to N mineralization and nitrification reactions in the soil rhizosphere can significantly stimulate N mineralization food web, except when fertilization results in a decline in without affecting microbial biomass [109, 117]. A 19-year soil pH that reduces the nitrification rate. field trial studying the effect of annual field application of five pesticides (benomyl, chlorfenvinphos, aldicarb, triadimefon and glyphosate) on soil processes found Pesticides that soil microbial biomass, N mineralization and nitrifi- cation rates were not affected by long-term exposure to Herbicides are the most widely used pesticides in Canada, single pesticides or combined pesticide applications [118]. representing 56% of the active ingredients purchased In conclusion, herbicides and other pesticides containing from 1998 to 2003 [114]. They are applied to control N may be degraded by soil micro-organisms and cause weeds that compete with field and vegetable crops for a small temporary increase in N mineralization and nitri- light, water and nutrients. Fungicides (11% of active fication, but are not expected to contribute directly to the ingredients purchased [114]) and insecticides (7% of active soil N supply. ingredients purchased, [114]) are generally applied to field and vegetable crops when pest populations reach eco- nomic thresholds according to the principles of integrated Water management pest management. A limited number of soil fumigants are registered for use as pre-plant soil fumigants in Canada, Soil moisture varies in humid temperate regions, with but include those containing the active ingredients flooding common after snowmelt and heavy spring rains;

http://www.cabi.org/cabreviews 12 CAB Reviews at the other extreme, soils may reach the wilting point germination of fungal spores and their distribution in the during dry spells in the summer. Field crop production in soil profile [123], which could also favour predator-prey humid temperate regions generally relies on rainfall as the relationships. main water source, with irrigation reserved for specialty Soil micro-organisms tolerate extreme wetting and vegetable and small fruit crops. Flooding in spring can drying events due to their ability to osmoregulate [124], delay planting, especially on heavy clay soils, so many but soil drying and rewetting can also create osmotic producers install artificial tile drainage to remove excess stress leading to microbial death and cell lysis. Conse- water from the subsurface layer, thereby facilitating water quently, soil drying and rewetting causes a flush of C, N infiltration and drainage from surface soils as well. There and phosphorus (P) in the soil solution, probably from cell are approximately two million hectares of croplands with lysis and an increase in soil respiration due to greater artificial tile drainage in Quebec and Ontario, Canada microbial activity and metabolism of organic substrates [119]. Controlled drainage and free-outlet drainage when soils are rewetted [125]. The integrity of fungal-rich are the two most common drainage systems in part of communities is maintained during drying-rewetting cycles, eastern Canada. Controlled drainage maintains the water which resulted in less dissolved organic N and inorganic N table level at a desired level, which gives more control losses from fungal-rich unimproved grassland soils com- over soil moisture. In contrast, free-outlet drainage con- pared with a bacterial-rich intensively managed grassland tinuously removes excess water in the field by carrying it soils [126]. Schimel et al. [125] suggested that adaptation to a series of resistance-free conduits via gravity. While may increase the microbial resistance and resilience to free-outlet drainage gives slightly drier soil conditions, drought, but experimental results are not consistent in however, both systems improve the overall water-holding this regard [122]. Furthermore, the presence of growing capacity of soil but exaggerate the wetting-drying cycle plants, which supply readily-mineralizable organic sub- within a field. strates in their rhizodeposits, can compensate for the Fluctuating wet–dry cycles cause selective pressure on depletion of organic substrate following multiple or pro- soil food web organisms. The oligochaeta (enchytraeids longed drying–rewetting cycles [122]. and earthworms) are among the most sensitive to dry Biochemical reactions catalysed by micro-organisms conditions because they require sufficient water to move depend on soil redox conditions (related to the con- through soil and avoid desiccation [38]. Under excessively centration of oxygen and other electron acceptors) that dry conditions, they may die, enter diapause or aestivate, are influenced by soil moisture. The heterotrophic which reduces their metabolism to a basal level. Soil and chemoautotrophic micro-organisms responsible for macrofauna and microarthropods belonging to the N mineralization and nitrification are facultative aerobes phylum Arthropoda are more tolerant of dry conditions, with maximum reaction rates around 60–70% water-filled since most possess an exoskeleton and have behavioural pore space [127]. Due to the strong dependence of soil adaptations to avoid desiccation (e.g., hiding in soil cre- food web organisms on soil moisture for survival, avail- vices, retreating to deeper soil layers, anhydrobiosis) [38]. ability of organic substrates and biochemical reactions Gergo´cs and Hufnagel [120] reported that oribatid mites such as N mineralization and nitrification, water man- can survive in dry soils, but are affected by drought agement is expected to exert an important control on the because of a reduction in fungi that serve as food; soil N supply. therefore the effect of drought on some arthropods may be due to food limitation rather than a lack of water. Prolonged flooding can be deleterious for soil meso- and Integrated crop management systems macrofauna, as they may eventually drown from the lack of oxygen. The previous sections have examined how selected Soil microfauna (amoebas and other protists, nema- agricultural practices could individually affect the size, todes) live and swim through water films surrounding soil composition and activity of the soil food web in relation particles [30], so are highly active in moist and flooded to N mineralization and nitrification. However, agri- soils and become inactive when water films evaporate in cultural producers select a suite of agricultural practices very dry soils. Protists did not grow in soils with 11.4% based on their values and production goals, in the context moisture content, but grew rapidly and preyed on bac- of local site factors such as climate and weather, agri- terial populations when moisture content increased to cultural policies, land tenure, technologies, markets, soil 18.6% [121]. Following drought, fungal- and bacterial- conditions, crop demands and ecosystem vulnerability feeding nematodes and their prey (fungi, bacteria) [11]. It is informative to compare some contrasting crop recovered more rapidly in C-rich grassland than arable management systems to determine how these may affect soil under wheat production [122], which highlights pre- the soil food web and ultimately the soil N supply. dator–prey relationships that are relevant for N miner- Bloem et al. [106] described a long-term study at alization. When soils are saturated, the movement of the Lovinkhoeve Experimental Farm (Marknesse, the gravitational water towards tile drainage may facilitate Netherlands) where soil food web and N dynamics the movement of soil microfauna and also stimulates were compared in integrated and conventional crop

http://www.cabi.org/cabreviews Joann K Whalen, Maria L. Kernecker, Ben W. Thomas, Vanita Sachdeva and Christopher Ngosong 13 management systems. Integrated crop management fungi was detected between organic and conventional systems received nearly twice as much organic matter production systems [129]. Greater microbial biomass each year as farmyard manure, green manure and crop (particularly bacterial biomass), more bacterivorous, residues, whereas conventional crop management herbivorous and omnivorous nematodes, enchytraeids, systems received crop residues only. During the winter earthworms, spiders, fly larvae (Diptera and Brachycera) wheat production year of the crop rotation, the N and surface-dwelling arthropods in the organic production mineralization rate was on average 30% greater in the systems [128, 129] suggests that a bacterial-dominated integrated crop management system, which received 40% food web was responsible for N and P mineralization. lower inorganic N fertilizer inputs, reduced soil tillage This is supported by greater enzyme activity linked to N (10 cm depth in the integrated crop management system and P mineralization in the organic than conventional versus 20 cm depth in the conventional crop management production systems in this study [128]. system), lower pesticide use and no soil fumigation compared with the conventional crop management sys- tem. Greater N mineralization was attributed to greater Conclusions organic matter content in the integrated crop manage- ment system, which also received with 30 tonnes/ha of The concept of the soil N supply expands previous mushroom compost (C:N ratio=14) following winter notions of soil fertility because it acknowledges the wheat harvest in August. According to Bloem et al. [106], potential of the soil food web to furnish part of the crop the presence of easily decomposable organic matter from N requirements through N mineralization and nitrification organic amendments increased bacterial growth rates, and processes. Better estimates of the soil N supply from the supported more amoebae (64% higher) and nematode soil food web should allow us to reduce N fertilizer inputs (22% higher) biomass, which presumably preyed upon the and to adjust the timing of N inputs so that exogenous bacteria and increased N mineralization in the integrated N sources are applied when crops really need them. For crop management system, especially during the growing instance, a cold wet spring may hinder soil food web + 7 season (April–August). No soil fumigants were applied to organisms from supplying enough NH4 and NO3 for the integrated crop management system, and this led to early crop growth, necessitating a larger input of starter N larger populations of bacterivorous fauna [106]. Their fertilizer under these conditions. Extra N fertilizer inputs study confirms that predator–prey relationships in the soil may be needed to achieve target yields when managing food web control N mineralization and the soil N supply, agroecosystems with a fungal-dominated soil food web especially in agroecosystems where organic amendments that retains N and keeps plant-available N concentrations contribute to the annual N input. However, N miner- low. Since N mineralization and nitrification can continue alization was not enough to achieve the potential yield at after harvest in humid temperate climates, producers + this site, as grain yield was 23% lower and N removal in can consider planting cover crops to deplete the NH4 7 harvested grain and straw was also less in the integrated and NO3 produced during this period or avoid fall tillage crop management system (111 kg N/ha) than the con- and manage surface residues to support more N retention ventional crop management system (165 kg N/ha) [106]. in fungal-based soil food webs, thereby minimizing over- Lower crop yields are not unusual in farming systems winter N losses to the environment. Some of these ideas that rely on N mineralization from organic amendments were already proposed by de Vries and Bardgett [61]. to furnish part of the soil N supply, but in some cases the At present, most research on the soil N supply focuses low yields seem to be the result of inadequate N input on developing quick laboratory methods to measure rather than an inability of the soil food web organisms to the fraction of total N or organic N in soil that is + 7 efficiently convert organic N to NH4 and NO3 .Ma¨der potentially mineralizable. Aerobic incubations to deter- et al. [128] reported 20% lower crop yield in organic mine the potentially mineralizable N (No) are lengthy (biodynamic and bioorganic) than conventional produc- (20–40 weeks) but considered to be the best predictor of tion systems in Switzerland over a 21-year period, and a the soil N supply, with chemical methods (e.g., hot KCl- follow-up study after 27 years found 23% lower wheat extractable N, UV absorbance of NaHCO3 extract at 205 grain yield in the organic than conventional production or 260 nm, Illinois soil test for N) showing very poor to 2 systems [129]. However, crop yields were likely con- very good relationships with No (R = 0.11–0.83) and strained by the fact that NPK inputs were 34–51% lower crop N uptake under field conditions (R2 = 0.09–0.87) [20]. in the organic than conventional production systems. This In-field measurements of soil N supply such as the pre- suggests that mineralization (N and P) and solubilization plant and pre-sidedress nitrate tests, and anion/cation (P and K) reactions liberated a supply of plant-available exchange membranes appear to be more robust indica- NPK that was efficiently transferred from soil to plants. tors of crop N uptake (R2=0.34–0.91) [20], which argues Although symbiotic mycorrhizal fungi were proposed for the use of field-based tests or development of soil to facilitate nutrient transfer and improve crop nutrition tests that mimic field conditions, because this is the only [128], no difference in hyphal biomass of saprophytic way to truly account for soil food web structure and its and mycorrhizal fungi or the biomarker for mycorrhizal functions related to the soil N supply.

http://www.cabi.org/cabreviews 14 CAB Reviews The fundamental difficulty with chemical methods of supported by a Discovery Grant to JKW from the Natural measuring the soil N supply is that those methods do not Sciences and Engineering Research Council of Canada account for soil biological processes and physical prop- (NSERC). erties governing N mineralization and nitrification. All organisms will consume substrates as fast as possible [130], but their activities are restrained by physical bar- References riers and other constraints (e.g., temperature, moisture, 1. Herridge DF, Peoples MB, Boddey RM. Global inputs of redox conditions). Aerobic incubations may be better biological nitrogen fixation in agricultural systems. Plant for determining potentially mineralizable N because the and Soil 2008;311:1–18. experiments are relatively long in duration and use sieved 2. Carlsson G, Huss-Danell K. Nitrogen fixation in perennial soil ( < 2 mm mesh) that probably contains soil micro- forage legumes in the field. Plant and Soil 2003;253:353–72. organisms, their primary predators (protists, nematodes) 3. Jones DL, Shannon D, Junvee-Fortune T, Farrar JF. Plant and some of the mesofauna, but not earthworms and capture of free amino acids is maximized under high soil other macrofauna. Yet, potentially mineralizable N is not amino acid concentrations. Soil Biology and Biochemistry a direct measure of soil N supply – it overestimates the 2005;37:179–81. + 7 NH4 and NO3 pools because sieving removes physical 4. Sauheitl L, Glaser B, Weigelt A. Uptake of intact amino barriers to potentially mineralizable substrates that are acids by plants depends on soil amino acid concentrations. not accessible to the soil food web in the field [90–92] and Environmental and Experimental Botany 2009;66:145–52. the incubations are run under constant temperature 5. Galloway JN, Cowling EB. Reactive nitrogen and the world: and moisture conditions (35C, 55–65% water-filled pore two hundred years of change. Ambio 2002;31:64–71. space) [20]. 6. Maene LM. International fertilizer supply and demand. In: How do we reconcile these challenges in determining Proceedings of the Australian Fertilizer Industry Conference, the soil N supply with the fact that we wish to measure 6–10 August, 2007, Hamilton Island, Queensland. the contribution to N mineralization and nitrification of 7. FAO. Current World Fertilizer Trends and Outlook to 2012. soil food web organisms under field conditions, to be able Food and Agriculture Organization of the United Nations, to make practical recommendations about fertilizer use in Rome, Italy; 2008. Available from: URL: ftp://ftp.fao.org/agl/ agroecosystems without compromising producers’ yield agll/docs/cwfto12.pdf [accessed 9 July 2012] objectives? Addiscott [130] wrote ‘if mineralization is an 8. Liu J, You L, Amini M, Obersteiner M, Herrero M, emergent process, it will be characterized by bottom-up Zehnder AJB, et al. A high-resolution assessment on global nitrogen flows in cropland. Proceedings of the National behaviour’ and this is consistent with our view that Academy of Sciences of the United States of America the microbially-mediated N transformations are the key 2010;107:8035–40. to understanding the soil N supply, with microfaunal 9. Vitousek PM, Howarth RW, Likens GE, Matson PA, predators showing strong and consistent control on the Schindler D, Schlesinger WH, et al. Human alterations of the N mineralization and nitrification processes. Soil meso- global nitrogen cycle: cause and consequences. Issues in and macro-fauna also contribute to the soil N supply by Ecology 1997;1:1–17. moderating substrate quality and soil habitat, but spor- 10. Canfield DE, Glazer AN, Falkowski PG. The evolution and adically because of their sensitivity to environmental future of Earth’s nitrogen cycle. Science 2010;330:192–6. conditions and relatively small, patchy populations (com- 11. International Plant Nutrition Institute. 4R Plant Nutrition: pared with micro-organisms and microfauna). Ideally the A Manual for Improving the Management of Plant Nutrition. soil food web structure and functions would be measured International Plant Nutrition Institute, Norcross, Georgia, and modelled in the field, but this does not necessarily USA; 2012. call for large research teams to collect and enumerate a 12. Vanlauwe B, Bationo A, Chianu J, Giller KE, Merckx R, multitude of soil organisms. Functional genomics targeting Mokwunye U, et al. Integrated soil fertility management: genes involved in soil N transformations (e.g., amo, hao operational definition and consequences for implementation and dissemination. Outlook on Agriculture 2010;39:17–24. and nrx genes in the ammonia oxidation and nitrification pathways [10]) and quorum sensing of chemical signals 13. Anderson RV, Coleman DC, Cole DV, Elliott ET. Effect of the involved in the depolymerization of organic N (e.g., acyl- nematodes Acrobeloides sp. and Mesodiplogaster lheritieri on substrate utilization and nitrogen and phosphorus homoserine lactones from proteobacteria [54]) can give mineralization in soil. Ecology 1981;62:549–55. us insight into microbial activities and responses in the soil 14. Verhoef HA, De Goede RGM. Effects of collembola grazing environment. These approaches may hold promise for on nitrogen dynamics in a coniferous forest. In: Fitter AH, linking the soil food web to the soil N supply in the future. Atkinson D, Read DJ, Usher MB, editors. Ecological Interactions in Soil. Blackwell, Oxford, UK; 1985. p. 367–77. 15. Department for Environment, Food and Rural Affairs. 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