In-soil organisms as drivers of food web support

Table 8: Key drivers for the ecosystem service soil structure formation. Main taxa, examples of species and exposure routes.

Key drivers Maintaxa Main exposure

routes Example species

Macropores creators Lumbricidae Oral soil Oral litter Contact soil

Anecic worms: Lumbricus terrestris, Aporrectodea longa

Soil mixers Lumbricidae Oral soil

Contact soil

Endogeic worms Aporrectodea caliginosa

Litter/organic matter fragmenters

Oniscidae Oral litter Isopods: Porcellio scaber

Lumbricidae Oral soil

Oral litter

Anecic worms: Lumbricus terrestris, Aporrectodea longa

Collembola Oral litter/org.

matter Contact soil

Folsomia quadrioculata, Pseudosinella alba, Entomobrya multifasciata, Lepidocyrtus cyaneus

Oribatida Oral litter/org.

matter Contact soil

Oribatid mites: Oppiella nova, Tectocepheus velatus, Punctoribates punctum, Scheloribates laevigatus Aggregates stabilisers Fungi and bacteria Contact soil/contact

soil pore water Glomalin producers Arbuscular mycorrhizal fungi

Figure 6: Soil food web (Reprinted from Hunt and Wall, 2002. Copyright John Wiley and Sons from Hunt et al., 1997)

Soil fauna

Although the overall importance of the in-soil invertebrate fauna to terrestrial food chains is rather poorly recognised, there are several species and food-chain links that have been relatively well studied.

Most of them show unequivocally that at least certain in-soil invertebrate species are of crucial importance for supporting terrestrial food chains. Among the best recognised links between the soil environment and terrestrial fauna are those mammals and birds for which earthworms constitute an important food resource. The prime and long-known example is the Eurasian badger (Meles meles) with up to ca. 90% of food biomass consumed in the spring made up of earthworms (Goszczynski et al., 2000). The authors noted also an important difference between pristine forest habitats and farmlands. In forests, earthworms constituted on average 62% of the badger diet, while in farmlands and pastures earthworms and plant material were equally important (34% each). These differences are probably not without an effect on badgers: Kruuk and Parish (1985) found that badger body weight is positively correlated with earthworm consumption and suggested that long-term differences in earthworm availability affect badger population size. During their studies, the average badger biomass decreased gradually between 1978 and 1981, by 14% in males and 17% in females, and the trend was strongly correlated with the proportion of earthworms in the diet (see Figure 7). The authors hypothesised that the observed decrease in earthworm population size and availability to badgers resulted from changes in pasture management. Unfortunately, they did not study whether it was related to the use of any plant protection products. Nevertheless, these data clearly show the importance of earthworms for maintaining healthy populations of badgers.

Earthworm availability was also the main factor besides altitude determining the spatial distribution of Eurasian Woodcock (Scolopax rusticola) at the landscape scale in Cantabrian Mountains in Spain (Brana et al., 2013). Indeed, according to Hoodless and Hirons (2007), earthworms can provide 50–80% of food biomass for this species.

While earthworms represent an important food resource for birds and mammals, many smaller in-soil invertebrates support a number of ground dwelling and aboveground invertebrate predators. For example, Pardosa spiders, which predate on both above-ground (e.g. Diptera) and small soil invertebrates, seem to prefer aphids when they are abundant but springtails prevail at low aphid densities (Kuusk and Ekbom, 2010) (see Figure 8). The authors conclude that the abundance of springtails may help in maintaining spider populations and, in consequence, enhance spider predation on pests.

10

9

8

7

0 30 40

Earthworms (% volume in diet) Males

Females

Live weight (kg)

50 60 70

Figure 7: Relation between relative volume of earthworms in badger diet and the live weight of badgers during March-June: males: r= 0.89, P < 0.05; females: r = 0.99, P < 0.001.

Redrawn after Kruuk and Parish (1985), copyright John Wiley and Sons

Springtails are also the most numerous and important prey of epigeal linyphid spiders. Even if the spiders consume also substantial quantities of other prey, with aphids as the main component, Romero and Harwood (2010) noted that a diet consisting of aphids alone is not sufficient for spider development. Similar to Kuusk and Ekbom (2010), the authors stress the importance of spiders in controlling pest populations, especially aphids. At the same time, they found that spiders were severely prey limited and hypothesised that this is due to the impact of adverse climate conditions and agricultural practices on prey. If the latter is the case, the study by Romero and Harwood (2010) provides an important link between protection goals for in-soil invertebrates and non-target, above-ground arthropods (NTA). In the recently published ‘Scientific Opinion addressing the state of the science on risk assessment of plant protection products for non-target arthropods’ (EFSA PPR Panel, 2015a), the crucial importance of landscape structure for the maintenance of NTA biodiversity has been stressed. The work by Romero and Harwood (2010) indicates that landscape structure may be of crucial importance in maintaining the important ecosystem function that small and less mobile soil invertebrates have in supporting higher trophic levels in a food chain.

A recent extensive study across four European countries, Sweden, the UK, the Czech Republic and Greece, showed that increasing land-use intensity negatively affects species richness of earthworms, springtails and oribatid mites and reduces mean body mass of soil fauna (Tsiafouli et al., 2015). A comparison of invertebrate prey abundance for birds between organic and conventional arable farms showed that earthworm abundance was 2–4 times higher on the former than on the latter (Kragten et al., 2011). Having in mind the trophic relationships described briefly above, this can also mean negative changes at higher trophic levels, including populations of important invertebrate and vertebrate carnivores.

Many birds, mammals, reptiles and insects are known to include gastropods in their diet, but there is a lack of studies about the ecological significance of malacophagy (Barker, 2004). As reviewed by Nyffeler and Symondson (2001), it has been shown for around 20 genera of spiders that they include gastropods in their diet. For harvestmen, gastropods are a particularly significant component in their diet, and some genera, mainly Trogulus and Anelasmocephalus, specialise in these prey. Their diet includes larger snails (e.g. family Helicidae) but also smaller sized species (e.g. families Vallonidae, Cochlicopidae, Pupillidae, Enidae, Endontonidae, see Nyffeler and Symondson (2001)). Carabid beetles of the tribe Cychrini, of which in Europe only the genus Cychrus occurs (Freude et al., 2005), principally feed on snails and slugs (Larochelle, 1972), and some species of the genus Carabini have specialised in eating snails and slugs (Freude et al., 2005).

Snail shells might be a vital calcium source for organisms at higher trophic levels. It has been shown for birds on poor soils in Dutch forests that a decline of snail densities resulted in eggshell defects in the great tit Parus major caused by calcium deficiency (Graveland and van der Wal, 1996). Graveland and Van Gijzen (1994) showed that forest passerines need to ingest calcium-rich items, e.g. snail shells, additionally to their normal food to satisfy their calcium requirements. It cannot be excluded that birds occurring in the agricultural landscape also require snails as a source of lime, but this topic requires further study.

Figure 8: Percentage of Pardosa spiders collected in spring-sown cereals that tested positive for aphid consumption, springtail consumption or consumption of both prey by polymerase chain reaction (PCR)-based gut-content analysis. Reprinted from Kuusk and Ekbom (2010), Copyright (2010), with permission from Elsevier

Nematodes are important food sources for several species of other nematodes or soil microarthropods (Huhta et al., 1998), and opportunistic scavenging of dead invertebrates is common.

Isotomid, entomobryid, tomocerid, and hypogastrurid collembolans have been found to correlate negatively with wood-decomposition rate, suggesting that direct feeding on fungi by these organisms may contribute to this negative relationship. Collembola form a significant proportion of the diets of ground-dwelling spiders, ground beetles (Carabidae), rove beetles (Staphylinidae), mesostigmatid mites, ants, diplurans, and other predacious arthropods (McBrayer and Reichle, 1971; Hopkin, 1997).

Data on their importance as food supply for vertebrates are not available but, due to the small size of nematodes, they are probably negligible as direct food for larger animals.

The positions and roles of soil animals in the terrestrial food webs are extremely diverse. The ecological entity to be protected should be attributed therefore to functional groups in terms of position in the food web, but the functional groups are yet to be defined. From the point of view of present knowledge on food-web relationships, as described above, the following groups may be identified as crucial prey for different groups of animals: annelids, nematodes, gastropods, and arthropods. It should be also noted that the food-web relationships may be complex and multi-level, so that specific functional/taxonomic groups serve as food to other in-soil invertebrates which, in turn, are preyed upon by other animals, representing domains other than soil.

Soil microorganisms

Biotic interactions within soil food webs can be both bottom-up and top-down. Bottom-up interactions can be based on, for example, fresh root material for plant feeders, dead roots, root exudates and litter in the case of primary decomposers or prey in the case of secondary decomposers and predators. Top-down effects are mainly driven by predation (Turbe et al., 2010). Top-down regulation at higher trophic levels may appear marginal, considering that microbial biomass comprises the majority of the total biomass in soil. However, bottom-up interactions can be mainly ascribed to the prokaryotes and fungi (Mulder et al., 2005).

Prokaryotes, fungi and protozoa are considered key players in the soil food web, being at the bottom of the detritus food web. Thus, they are mainly eaten by all the other in-soil organisms including nematodes and protozoans. For example, the diet of earthworms mainly consists of organic material in various stages of decay. Dead plant tissue comprises the bulk of the organic matter consumed, but living microorganisms, nematodes and other microfauna, mesofauna and their dead remains are also ingested. It has been reported that earthworms are usually food generalists with a preference for dark pigmented fungi (Dematiacea), which often comprise up to 60% of fungal isolates from soil and are generally of high food quality. In addition to fungi, protozoa and algae may constitute a significant part of the diet of earthworms.

Most oribatid mite species appear to feed preferentially on certain genera of dark pigmented fungi, such as Alternaria and Ulocladium, but the food spectrum varies among oribatid mite species. Oribatid mites have also shown feeding preference for ectomycorrhizal fungi (Schneider et al., 2005). It has been reported, however, that some species can also be bacteria feeders, detritivorous species and some of them feed on carrion (Behan-Pelletier, 1999).

Nematodes can be classified according to their feeding behaviour in either bacterial, fungal or protozoan feeders. Like nematodes, protozoans can also be classified according to their feeding behaviour in bacterial or fungal feeders. Collembola have also been considered as generalist in their feeding behaviour feeding both on fungi and bacteria.

As presented above, soil microorganisms make up a taxonomically diverse yet single functional group in terms of food-web support. Even if some organisms show preferential feeding on certain groups of microorganisms, none is fully selective and generalists prevail. Hence, for SPGs, soil microorganisms should be regarded as one functional group, indispensable to support viable populations of a range of in-soil organisms.

Table 9: Key drivers for the ecosystem service food web support. Main taxa, examples of species and exposure routes.

Key drivers Examplesof

taxa

Main exposure

routes Example species

Soil non-arthropod invertebrates

Lumbricidae Oral soil Oral litter Contact soil

Anecic worms: Lumbricus terrestris, Aporrectodea longa

Endogeic worms: Aporrectodea caliginosa

6. Speci fic Protection Goal Options for in-soil organisms in agricultural