Soil animals

Soil harbours a huge number of animal species (30% of arthropods live in soil), whether over their entire life or at least during larval stages.^[1] Soil offers protection against environmental hazards, such as excess temperature and moisture fluctuations, in particular in arid and cold environments,^[2] as well as against predation.^[3] Soil provisions food over the year, especially since omnivory seems the rule rather than the execption,^[4] and allows reproduction and egg deposition in a safe environment, even for those animals not currently living belowground.^[5] Many soil invertebrates, and also some soil vertebrates, are tightly adapted to a subterranean concealed environment, being smaller, blind, depigmented, legfree or with reduced legs, and reproducing asexually,^[6] with negative consequences on their colonization rate when the environment is changing at landscape scale.^[7] It has been argued that soil could have been a crucible for the evolution of invertebrate terrestrial faunas, as an intermediary step in the transition from aquatic to aerial life.^[8]

Rotifera microscopic view

SEM image of Milnesium tardigradum in active state - journal.pone.0045682.g001-2

Soil fauna have been classified, according to increasing body size, in soil microfauna (20 μm to 200 μm), mesofauna (200 μm to 2 mm), macrofauna (2 mm to 2 cm) and megafauna (more than 2 cm).^[9] The size of soil animals determines their place along soil trophic networks (soil foodwebs), bigger species eating smaller species (predator-prey interactions) or modifying their environment (nested ecological niches).^[10] Among bigger species, soil engineers (e.g. earthworms, ants, termites, moles, gophers) play a prominent role in soil formation^[11][12][13] and vegetation development,^[14][15][16] giving them the rank of ecosystem engineers.

From a functional point of view soil animals are tightly interconnected with soil microorganisms (bacteria, archaea, fungi, algae).^[17] Soil microorganisms provide food to saprophagous and microbivorous species,^[18] and play a significant role in the digestion of recalcitrant compounds by saprophagous animals.^[19] In turn, soil animals, even the tiniest ones, create environments, e.g. digestive tracts,^[20] feces,^[21] cavities,^[22] favourable to soil microorganisms, allow their dispersal for those unable to move by their own means (e.g. non-motile bacteria),^[23] and regulate their populations.^[24]

The identification of soil animals, needing to be extracted (e.g. microarthropods, potworms, nematodes),^[25] expelled (earthworms)^[26], trapped (e.g. carabids)^[27] or searched by hand (e.g. termites, ants, millipedes, woodlice)^[28] before being observed under a dissecting, light microscope or electron microscope,^[29] has slowed down the development of soil zoology compared to the aboveground. To a few exceptions (e.g. vertebrates) the identification of soil animals was only done by specialists, using various published or unpublished keys and their own collections. From a few decades on molecular tools such as DNA barcoding helped field ecologists to achieve complete lists of species or OTUs.^[30] Such automated tools have been implemented in the study of nematodes,^[31] protozoa,^[32] and are still in development for other soil invertebrates such as earthworms and collembolans.^[33] They will be most useful for giving us reliable estimates of soil biodiversity, taking into account the huge amount of cryptic species which cannot be identified by morphological criteria.^[34]

Soil microfauna

Soil microfauna comprise unicellular (protozoa), and multicellular (nematodes, rotifers, tardigrades) organisms. By their small size (20 μm to 200 μm) they are able to move within mesopores (30–75 μm) and macropores (>75 μm) where they find microorganisms (for microbivorous species) or other microfauna (for predatory species) as food.^[35] To the exception of resting stages (e.g. eggs, cysts, dauer larvae) microfauna are more often in tight contact with water films surrounding soil aggregates and roots (rhizoplane).^[36] Microfauna are involved in strong interactions with soil microorganisms, together consuming and stimulating them by rejuvenating microbial colonies.^[37] Through the excretion of nutrients in a plant-available form (e.g. ammonium) they contribute to plant nutrition.^[38]

Although difficult to verify experimentally,^[39] Clarholm's microbial loop hypothesis^[40] explained how the growth of roots, when exploring a new environemnt, exerts a priming effect on quiescent soil bacteria which in turn are predated by naked amoeba, liberating nitrogen in a mineral form, further absorbed by root hairs, stimulating in turn the plant through a positive feedback process.^[41]

Chemical signalling through the water film in which mesofauna are living (e. g. chemotaxis) is strongly involved in intra-species (pheromone)^[42][43][44] and between-species (allomone)^[45][46] communication. Mesofauna are also involved in chemical signalling with plants, in particular in parasitic forms (e. g. root-feeder nematodes). Interesting parallels between nematode-plant chemical interactions and plant-fungal symbioses (mycorrhizae) have been suggested.^[47]

Because of their physiological and locomotory dependence to pore water microfauna are very sensitive to moisture fluctuations.^[48] Variations in population size of active forms (e.g. protozoan trophozoites) are correlated with variations in soil moisture along precipitation cycles.^[49][50] However, resistant life-cycle cryptobiotic stages (e.g. protozoan resting cysts, nematode dauer larva, rotifer anhydrobiotes, tardigrade tuns), allow them to stay and wait for better conditions, restoring fully active metabolism with a few hours.^[51][52][53] It can thus be postulated that, contrary to most other soil invertebrates, soil microfauna will not suffer to a critical extent from climate warming,^[54] while they are highly sensitive to other man-induced global changes such as acid rains.^[55]

Asexual reproduction (e.g. parthenogenesis, fission) is commonplace in protozoa (amoebae and flagellates),^[56] nematodes,^[57] rotifers,^[58] tardigrades, allowing them to rapidly exploit new or temporary environments or new hosts for parasites.

Soil mesofauna

Soil mesofauna are invertebrates between 0.1mm and 2mm in size,^[59] which live in the soil or in a leaf litter layer on the soil surface. Members of this group include nematodes, mites, springtails (collembola), proturans, pauropods, rotifers, earthworms, tardigrades, small spiders, pseudoscorpions, opiliones (harvestmen), enchytraeidae such as potworms, insect larvae, small isopods and myriapods.^[60] They play an important part in the carbon cycle and are likely to be adversely affected by climate change.^[61]

Diet and effects on soil

Soil mesofauna feed on a wide range of materials including other soil animals, microorganisms, animal material, live or decaying plant material, fungi, algae, lichen, spores, and pollen.^[62] Species that feed on decaying plant material open drainage and aeration channels in the soil by removing roots. The fecal material of soil mesofauna remains in channels that can be broken down by smaller animals.

Soil mesofauna do not have the ability to reshape the soil and, therefore, are forced to use the existing pore space in soil, cavities, or channels for locomotion. Soil Macrofauna, earthworms, termites, ants, and some insect larvae, can make the pore spaces and hence can change the soil porosity,^[63] one aspect of soil morphology. Mesofauna contribute to habitable pore spaces and account for a small portion of total pore spaces. Clay soils have much smaller particles which reduce pore space. Organic material can fill small pores. Grazing of bacteria by bacterivorous nematodes and flagellates, soil mesofauna living in the pores, may considerably increase Nitrogen mineralization because the bacteria are broken down and the nitrogen is released.^[64]

In agricultural soils, most of the biological activity occurs in the top 20 centimetres (7.9 in), the soil biomantle or plow layer, while in non-cultivated soils, the most biological activity occurs in top 5 centimetres (2.0 in) of soil. The top layer is the organic horizon or O horizon, the area of accumulation of animal residues and recognizable plant material. Animal residues are higher in nitrogen than plant residues with respect to the total carbon in the residue.^[65] Some Nitrogen fixation is caused by bacteria which consume the amino acids and sugar that are exuded by the plant roots.^[66] However, approximately 30% of nitrogen re-mineralization is contributed by soil fauna in agriculture and natural ecosystems.^[67] Macro- and mesofauna break down plant residues^[68][69] to release Nitrogen as part of nutrient cycling.^[70]

Reproduction

Many species of mesofauna reproduce in a variety of ways. Non-arthropod species such as nematodes and potworms can reproduce both sexually and asexually, the nematode through parthenogenesis which only creates females, and the potworm through whole-body regeneration. Soil rotifers another non-arthropod mesofauna, are only female and reproduce using unfertilized eggs. Arthropod species of soil mesofauna such as thrips, springtails, and pauropods reproduce solely by parthenogenesis. Diplurians and mites reproduce sexually, but some species of mites can reproduce by parthenogenesis.  Some species of soil mesofauna are susceptible to soil and vegetation changes because they rely on soil fertility and plant biomass for food and comfortable living conditions. The changes can affect some species' ability to reproduce, but since there are many variations in the species of soil mesofauna, the changes won’t affect all. For mesofauna such as springtails temperature and soil moisture influence the reproduction and growth rates of the individuals.

Soil macrofauna

Soil megafauna