In-soil organisms as drivers of nutrient cycling

5. In-soil organisms and ecosystem services in agricultural landscapes

5.3. In-soil organisms as drivers of nutrient cycling

Soil fauna

Soil fauna is the assemblage of a very diverse group of invertebrates, including e.g. earthworms, arthropods, gastropods, nematodes. Many representatives of soil fauna are important facilitators of organic matter decomposition and nutrient transformation. They can feed on litter material and excrete it partially decomposed as faecal pellets, thus increasing the surface area for microbial activity (Hasegawa and Takeda, 1995). They also act as dispersal agents of fungal spores and bacteria.

Moreover, they exert a more direct effect on microbial communities by performing a selective grazing on archaea, bacteria and fungal hyphae (Lummer et al., 2012; Garcia-Palacios et al., 2013), promoting microbial (mainly fungal) succession in decomposing plant material, accelerating decomposition and enhancing nutrient mineralisation (Cragg and Bardgett, 2001; Cole et al., 2005; Ke et al., 2005;

Crowther et al., 2012).

Even though microorganisms are directly involved in the biochemical decomposition of organic matter and nutrient transformations, their activity is closely related to the presence and activity of soil invertebrates that act as catalysts of microbial activity and modulators of community composition of microorganisms (Lavelle and Spain, 2005). The role of soil fauna in organic matter decomposition and nutrient turnover can be direct, via feeding on litter material (fragmentation), or indirect, by creating favourable conditions for microbial communities. Many species composing the soil macrofauna (lumbricids, isopods, millipedes, ants, insect larvae) and mesofauna (collembolans, mites, enchytraeids) are actively involved in organic matter breakdown via their feeding activity, contributing to its efﬁcient and fast decomposition and associated nutrient release (e.g. Ketterings et al., 1997; Schrader and Zhang, 1997; Briones et al., 1998; Filser, 2002; Dechaine et al., 2005; Van Eekeren et al., 2008).

‘Litter transformers’ (e.g. isopods, millipedes and some earthworm species) participate in the early phase of this process, promoting litter fragmentation and inﬂuencing microbial dynamics by altering substrate quality when excreting the vegetal material as faeces. They develop external mutualistic associations with microﬂora by contributing to an increase in substrate surface area accessible to microbial attack and to an increase in substrate pore volume and aeration, thus enhancing the overall microbial resource exploitation (Hassall et al., 1987; Kayang et al., 1996; Maraun and Scheu, 1996;

Cotrufo et al., 1998). This may, ultimately, inﬂuence nutrient mobilisation rates in the system (Anderson et al., 1983; Teuben and Roelofsma, 1990; Verhoef and Brussaard, 1990).

However, results from microcosm studies reported in the literature on the effects of ‘litter transformers’ on microbial communities are diverse. Enhanced microbial activity induced by the presence of isopods or diplopods was observed for oak litter (Hanlon and Anderson, 1980; Anderson et al., 1983), black pine (Teuben and Roelofsma, 1990) and on ¹⁴C-labelled pondweed (Grifﬁths et al., 1989). In contrast, a decrease in microbial activity caused by macrofauna was reported for oak litter under high feeding intensity (Anderson et al., 1983), for poplar (Van Wensem and Adema, 1991; Van Wensem et al., 1991, 1992) and for a mixture of deciduous leaves (Vink and Van Straalen, 1999).

When litters in different decomposition stages were analysed, contrasting effects were found in experiments with poplar (Van Wensem et al., 1997), black pine (Teuben, 1991) and beech (Maraun

and Scheu, 1996). These results indicate that the type and magnitude of effects depend, among other factors, on the type and status of the substrate, namely its chemical composition and degree of processing by soil fauna.

Effects on nutrient mineralisation may follow similar contrasting trends, and the observed diverging results have been also related to the nutrient status of the litter. To a certain extent, animal activity seems to act as a buffering factor, inducing an element of mineralisation when basal nutrient contents are low and vice-versa (Teuben and Roelofsma, 1990; Teuben, 1991). Model simulations revealed that effects of isopods on nutrient pools in decomposing litter were dependent on the litter C:N ratio (Van Wensem et al., 1997), with available carbon and nitrogen levels increasing in the presence of woodlice in litter with medium to high C:N ratios. The role of litter transformers on decomposition is not only affected by the quality of litter or soil organic matter but also by microbial communities and nutrient release. In a microcosm experiment with isopods, millipedes and earthworms, evaluated either as single species or in different combinations, Heemsbergen et al. (2004) demonstrated that litter decomposition, microbial respiration and nitrogen mineralisation were more inﬂuenced by community functional dissimilarity (different species with different traits and having different roles in the process) than by species richness per se.

Although ‘ecosystem engineers’ are involved in litter consumption and nutrient cycling, their role in organic matter turnover is also exerted via their burrowing and casting activities, providing habitat for microbes and facilitating the availability of organic substrates, regulating their decomposition activities (e.g. Jegou et al., 2001; Smith and Bradford, 2003; Cole et al., 2006; Frouz et al., 2006; Postma-Blaauw et al., 2006). Brussaard et al. (2007a) postulate that the role of soil macrofauna on water and nutrient use efﬁciencies in crop areas might be better related to their inﬂuence on soil structure. The biogenic structures they produce (soil aggregates and pores) modulate the water and nutrient ﬂuxes, with macroaggregates contributing to the stabilisation of soil organic matter and to the storage of nutrients and their consequent slow release during their decomposition (Jimenez et al., 2003;

Brussaard et al., 2007b; Mariani et al., 2007). However, their inﬂuence on N mineralisation can be seen beyond the area of the burrows, as found out for Lumbricus terrestris by Amador et al. (2006), who observed an increase in soil nitrate in the surrounding of these structures in a mesocosm experiment.

The role of earthworms in nitrogen mineralisation seems to depend on the ecological group they belong to and the nutrient source. In a microcosm experiment analysing the inﬂuence of different combinations of earthworm species representing different life strategies, Postma-Blaauw et al. (2006) reported enhanced mineralisation of crop residues in the presence of epigeic and anecic species (Lumbricus rubellus and Lumbricus terrestris, respectively), whereas the mineralisation of SOM increased in the presence of the endogeic species Aporrectodea caliginosa in combination with the epigeic species Lumbricus rubellus. Both interactions resulted in a reduction in mineral N in soil, possibly due to its immobilisation in microbial biomass. When the endogeic and anecic worms were present, an increase in microbial biomass was also observed with a decrease in total soil carbon.

These results demonstrate that the effect of earthworms on nutrient mineralisation depends on the traits of the different species present and can be modiﬁed by their interactions. Most land snail species are herbivorous and feed mainly on decaying or half-decayed plant material; some are predators (Burch and Pearce, 1990) and possess a very different feeding strategy compared to, e.g. earthworms.

There is no known herbivorous snail species in Europe whose food spectrum is limited to particular plant species and a few snail and slug species are known as pest organisms in ruderal systems, often due to their preference for crop plants that show higher palatability than their wild forms (Kerney et al., 1983; Gosteli, 1996). As for other organisms, some terrestrial snails and slugs can be, thus, considered both non-target organisms and pest species, depending on particular circumstances.

Considering only ingestion, the average contribution of terrestrial gastropod species to litter input in temperate ecosystems seems to be lower than for other soil invertebrates (see e.g. Mason, 1970;

Jennings and Barkham, 1976; Petersen and Luxton, 1982), although data on environments other than woodlands are scarce. Comparing anatomical and physiological features, Wieser (1978) reported gastropods to be ‘both efﬁcient digesters and assimilators’, whereas isopods can be considered

‘efﬁcient digesters but usually inefﬁcient assimilators’, which suggests that gastropods turn over a lower amount of organic material for the same gain of nutrients compared to isopods. Newell (1967) discusses the possible role of terrestrial gastropods in soil formation and states that terrestrial gastropods may have an important function by producing partially digested plant material and modifying their environment during crawling and with their faeces. Faeces and mucus may provide a suitable habitat for the proliferation of microorganisms as a starting point for decomposition processes, which Dallinger et al. (2001) consider to be probably their most important function in nutrient cycling

in temperate ecosystems. Since terrestrial gastropods (mainly snails but also slugs) probably make a signiﬁcant contribution to the ﬁxation of calcium in the upper soil layer, they may have a strong impact on nutrient cycling in terrestrial ecosystems by diverting ﬂuxes and changing availabilities of macronutrients in terrestrial ecosystems (Dallinger et al., 2001).

Many soil arthropods ingest large amounts of dead organic matter, fungal hyphae and bacteria.

Although their role in direct plant-litter decomposition is probably minor, they signiﬁcantly affect organic matter decay by a range of indirect effects. For example, several studies have shown that, at a moderate density of Collembola, litter enzyme activity, litter respiration and rates of nutrient release increase when compared with litter decomposing in the absence of these animals (Verhoef and Brussaard, 1990). The inﬂuence of springtails on nitrogen and phosphorus mineralisation depends on the dominant species involved and their traits, on the climate and type of ecosystem (Cragg and Bardgett, 2001; Filser, 2002).

Interactions between microarthropods and nematodes have been reported to affect soil carbon (C) and nitrogen (N) cycles (Yeates, 2003; Osler and Sommerkorn, 2007). In addition, abundance of total, bacterivorous, and fungivorous nematodes were found to be positively correlated with net N mineralisation rates. Neher et al. (2012) attempted to quantify the relative importance of speciﬁc faunal groups in the decomposition of organic matter and for the N availability in soils. Variation in soil N availability and decomposition rates were analysed accounting for the contributions of two faunal communities: nematodes and arthropods. Nematode communities explained between 7% and 12% of the variation in NO₃^–and NH₄⁺ availability, indicators of N mineralisation, in disturbed and undisturbed forests. Microarthropod communities explained almost 15% of the variation in decomposition rates in forests. Therefore, alterations in soil food web structure can result in signiﬁcant changes in decomposition processes (Setala, 2002).

Considering that soil fauna includes a number of identiﬁed ‘ecosystem engineers’, the ecological entity holding different traits in terms of nutrient mobilisation and cycling in agricultural soils is the functional group. However, it is questioned whether deﬁning different functional groups (e.g. anecics worms = vertical burrowers, endogeic worms = burrowing in soil matrix and epigeic worms= surface dwellers) as the ecological entities to be protected would be sufﬁcient to address these key drivers. As illustrated above in the section on the role of species diversity for the long-term performance of functional groups in strongly disturbed agricultural soils, the solely deﬁnition of SPU at the level of functional groups might lead under unfavourable conditions to a loss of function performance. Species loss within a functional group will lead to the erosion of trait diversity and to a reduced resilience and stability under changing environmental conditions. In order to support the long-term performance of the functional role of soil fauna in nutrient cycling of agricultural soils, it is therefore recommended to deﬁne the SPU as the abundance/biomass of species belonging to different functional groups.

Soil microorganisms

Soil microorganisms play a dominating role in the degradation of organic matter in soil, which results in mineralisation of C and the essential macronutrients N, P and S (Hussain et al., 2009;

Hopkins et al., 2010). The mineral forms can then be further transformed by speciﬁc groups of microbes (Prosser, 2007; Hopkins et al., 2010). Since in crop-production soils the plant material is largely harvested and removed, the direct dependence on remineralisation of primary production in ﬁeld is principally over-run. Resident soil microbial communities, however, still perform critical functions related to mineralisation and transformation of nutrients supplied as organic and inorganic fertilisers (e.g. Ninh et al., 2015).

The nitrogen cycle is particularly relevant to how in-soil organisms increase fertility and is one of the most studied processes. Nitriﬁcation and denitriﬁcation represent key processes determining the availability and forms of nitrogen (N) in soils. The ability to denitrify is widespread among various microbial taxa, including such phylogenetically diverse groups as bacteria, archaea and eukaryotes (Hallin et al., 2009; Szukics et al., 2010). Conversely, nitriﬁcation, including ammonium oxidation and nitrite oxidation, was long believed to be accomplished by a small, speciﬁc group of bacteria, until the existence of an archaeal ammonium oxidiser was identiﬁed about a decade ago (Hu et al., 2014). Fixation of atmospheric nitrogen by diazotrophic bacteria is a signiﬁcant N source in rice and legume cultures, and is thus critical for sustainable production in these systems. In rice paddies, it can be performed both by heterotrophs and photosynthetic cyanobacteria (Choudhury and Kennedy, 2004; Wartiainen et al., 2008) and research is ongoing, aiming to increase the use of cyanobacterial inoculants in rice production (Choudhury and Kennedy, 2004; Das et al., 2015). In legume crops, nitrogen ﬁxation is performed by several genera of root-nodule forming bacteria (Graham, 2008). Rhizobium-legume symbioses massively contribute to biological nitrogen ﬁxation entering soil ecosystems (Hussain et al., 2009) with over 100

agriculturally important legumes. Altogether, Rhizobia form symbiotic relationships with an estimated 15,000 legume species. The symbioses between Rhizobium or Bradyrhizobium and legumes are a cheaper and usually more effective agronomic practice for ensuring an adequate supply of N for legume-based crop and pasture production than the application of fertiliser-N. It is estimated that N-ﬁxing bacterial symbionts of the legumes can contribute up to 20% of all plant N. Actinorhizal interactions (Frankia-non-legume symbioses) are major contributors to nitrogen inputs in forests, wetlands,ﬁelds and disturbed sites of temperate and tropical regions.

Microorganisms also play a central role in the phosphorus cycle. Most agricultural soils contain large reserves of phosphorus. However, a large portion of soluble inorganic phosphate applied to soil as chemical fertiliser is rapidly immobilised soon after application and becomes unavailable to plants. A second major component of soil P is organic matter. Organic forms of P may constitute 30–50% of the total phosphorus in most soils, although it may range from as low as 5% to as high as 95%. To make this form of P available for plant nutrition, it must be hydrolysed to inorganic P. Mineralisation of most organic phosphorous compounds is carried out by means of phosphatase enzymes, such as acid phosphatases. Soil bacteria expressing a signiﬁcant level of acid phosphatases include strains from the genus Rhizobium, Enterobacter, Serratia, Citrobacter, Proteus and Klebsiella, as well as Pseudomonas and Bacillus (Rodrıguez and Fraga, 1999).

The provision and the regulation of primary production is one of the most important services delivered by soils. Plant growth and productivity is heavily inﬂuenced by the interactions between plant roots and the surrounding soil, including the microbial populations within the soil. Thus, soil microorganisms have a strong impact on plant productivity. The main mechanisms for plant growth promotion driven by microorganisms include suppression of disease (biocontrol), enhancement of nutrient availability (biofertilisation), and production of plant hormones (phytostimulation) (Pereg and McMillan, 2015). The service of pest regulation is indirectly related to the primary production, since such a control limits the loss of plants and plant products.

Plant uptake of water and mineral nutrients from the soil is greatly aided by mutualistic associations with mycorrhizal fungi, which grow into and extend out of the plant roots. Nutritional ﬂuxes are bidirectional (Berruti et al., 2014). Nitrogen acquisition strategies are different in arbuscular mycorrhizae and ectomycorrhizal fungi (Marschner and Dell, 1994; Rebel et al., 2013) but both play a key role in providing plants with phosphorus, which is mainly available in soil as insoluble organic or inorganic forms that make it unavailable to plants (Jones et al., 1998; Smith et al., 2011; Berruti et al., 2014).

Arbuscular mycorrhizal fungi have been shown to enhance plant productivity by improving P uptake by plants (Van der Heijden et al., 2006) up to 90%. This is particularly important for legumes, for example, which have a high P-requirement. Also, a functional complementarity has been demonstrated between families of arbuscular mycorrhizae. For instance, Glomeraceae provides protection against fungal pathogens while Gigasporaceae enhances P uptake (Van der Heijden et al., 2008).

It is known that morphological arbuscular mycorrhizae traits are rather well preserved within the same genus (i.e. hyphal length, fungal biomass, number and volume of spores, internal vs external mycorrhizal root colonisation). However, the manifestation of those traits can be quite variable even within one species, being highly dependent from the host plant (and plant community) and the symbiosis established. Among the potentially important ectomycorrhizal fungal response traits inﬂuencing their abundance in various communities are preference for N source, exploration morphotype and the deposition of melanin in cell walls (Koide et al., 2014). Fungi that form ectomycorrhizae are not a monophyletic group in contrast to arbuscular mycorrhizae which all belong to the monophyletic group, the Glomales. The ectomycorrhizae can belong to all of the phyla of true fungi (Zygomycota, Ascomycota and Basidiomycota) (Horton and Bruns, 2001). Ectomycorrhizae communities are species rich, however, there is still a lot of uncertainty on the composition of ectomycorrhizae community in terms of number and abundance of species mainly because ectomycorrhizae are not easily manipulated and cultivated in laboratory. One of the main elements of mycorrhizal symbiosis is foraging for nutrients and carbon. The foraging strategy may include: proliferation of hyphae, carbon and nutrient allocation within a mycelium and spatial distribution of the mycelium (internal mycelium for carbon and external mycelium for nutrients) (Olsson et al., 2002). It is well reported in the literature that foraging-related functional traits of hyphae are typically conserved at the genus level (Agerer, 2006; Aguilar-Trigueros et al., 2014), although it is also reported that signiﬁcant within-species functional variability exists in ectomycorrhizal fungi (Koide et al., 2007).

Due to the complexity of soil fungal communities and the interaction plant-fungi also considering environmental variables, arbuscular mycorrhizae and ectomycorrhizae taxa have not been categorised by using speciﬁc criteria but a mix of taxonomic, morphological and physiological characteristics.

So, although these arguments could indicate that ‘population’ (= species) would be the ecological entity to protect, the variation of trait expression within each arbuscular mycorrhizae species, being highly context-dependent and to the ubiquity of these fungi species in terms of geographical distribution (Davison et al., 2012) and ability to colonise many plant species, makes it difﬁcult to base the risk assessment at population (species) level and rather focus on the functional group arbuscular mycorrhizae. The same conclusion can also be drawn for ectomycorrhizae because, although much has been learned about behaviour, physiological ecology and traits have been measured on individual species, particularly of Suillus, Rhizopogon, Paxillus, Laccaria, Pisolithus and Cenococcum, in laboratory microcosms, meaningful extrapolations to species also depend on trait variability among individuals and populations, as well as on the adequacy of the species concept for fungi. In addition, it is not very clear how factors like host diversity, soil types, organic inputs, disturbance, and succession can affect the structure composition. Moreover, vegetative structures of these fungi (i.e. mycorrhizae and mycelium in the soil) occur largely below ground and are difﬁcult to track and identify (Horton and Bruns, 2001).

Free-living microbes also increase nutrient availability for plants through breakdown of organic matter and releasing mineral nutrients to soil solution. For example, most of the N in soil is contained in complex insoluble polymers, such as proteins, nucleic acids and chitin, which are broken down and mineralised by soil microorganisms, eventually releasing mineral forms of N that are available to plants.

In turn, free living N-ﬁxing bacteria are able to ﬁx signiﬁcant amounts of N, thus contributing to the N budget in many ecosystems. Free-living microorganisms can also contribute to the availability of nutrients to plants by weathering the bedrock via exudation of organic acids and solubilisation of precipitated P. In addition, they can improve plant productivity by suppressing plant diseases, for example through the production of antifungal metabolites by Pseudomonas spp.

Soil microorganisms seem to be characterised by a redundancy of functions. However, functional redundancy is considered greater for functions that are performed by a large number of microorganism groups, such as litter decay, than for processes performed only by few speciﬁc

W dokumencie Scientific Opinion addressing the state of the science on risk assessment of plant protection products for in-soil organisms (Stron 30-35)