In the sections above, we described the grazing of secondary sapro- trophs on primary saprotrophs, and on each other. In addition to those, there are other trophic interactions between the interstitial saprotrophs.
These trophic interactions include predation on secondary saprotrophs.
In this section, we group trophic interactions that are mostly between microinvertebrate predators. Several trophic interactions have been studied in particular, whereas many others are poorly described. The roles of predatory rotifers (Monogomontes), the tardigrades and ony- chophorans are poorly quantified and neglected (see Chapter 1). One needs to remember that one species does not necessarily belong to any one trophic level, but can also be found at other levels. For example, some of the ligninolytic fungal species complement their nitrogen-poor diet by capturing nematodes.
Nematotrophy
In this section, we consider primarily feeding on nematodes. The mecha- nism of capturing a nematode prey is the most studied; however, the same mechanisms operate on rotifers, tardigrades and similar sized organisms that can be captured or penetrated. It is unclear what the extent of nematotrophy, or feeding on microinvertebrates in general, is in the soil. The phenomenon is common but has been quantified insuffi- ciently. A variety of microarthropods are known to feed on nematodes (or microinvertebrates) or at least to supplement their diet with nema- todes (Walter, 1987) (Fig. 4.12). These include pseudo-scorpions and sev- eral families of mites and Collembola. Many soil Collembola probably supplement their diet with nematodes (Hopkins, 1997). Among the Acarina, these include the groups listed below as predatory. However, the nematodes are often the preferred prey, especially for Mesostigmata, Prostigmata (Bdellidae and Cunaxidae) and some Endostigamata (Alycus andAlicorhagia). Certain predacious testate amoebae, such as Nebella, are known to hold nematodes with pseudopodia, immobilize the prey and engulf the whole organism. Sometimes, only the tail is held and the rest of the nematode breaks free (Yeates and Foissner, 1995). In all the above cases, access to nematodes in soil pores is not restricted by the size of the predator as much as by the diameter of the amoeba pseudopodia, the chelicerae of mites or other appendages. Several interactions involving hyphal fungi (Basidiomycetes and mitosporic species), Chytridiomycetes, Zygomycetes and the Oomycetes (chromista and pseudo-fungi) are con- sidered below (for further details and references, see Barron, 1977).
One method of attacking and digesting nematodes involves monociliated dispersal cells which swim towards prey. The dispersal cells do not hold many reserve nutrients and have a limited time of activity to find a new prey. The cells probably track a solute from the prey’s path by chemotaxis. Penetration into the prey can be through an orifice or through the cuticle. Once attached to the prey cuticle, the cilium is lost and the cell encysts. From the cyst, cytoplasmic extensions grow into the
host and form a mesh. The prey is invaded by the hyphae which secrete digestive enzymes, absorb the solutes and empty the cuticle. When nutrients run out or the hyphae become crowded, spores form which grow an exit tube and swim off. In dry conditions or through tight exit tubes, cells can be amoeboid. This mechanism is common in Chytrids (fungi) such as Catenasia. The chytrids also attacks similar sized organ- isms such as rotifers, tardigrades, invertebrate eggs or macrodetritus consisting of animal corpses or parts thereof.
A modification of this mechanism occurs in the Oomycetes (chromista) Myzocitium, where the dispersal ciliated cells encyst in the soil and become sticky. Attachment on to the cuticle of a passing prey is the stimulus to extend hyphae into the prey. In Haptoglossa, the cyst dis- charges a coiled tube into the passing prey. The coil is 5–8 µm long and 0.5 µm wide, and discharged in about 0.1 s. No infection occurs if the coil is discharged into a cuticle which is too thick to traverse. In Zygomycetes, such as Meristacrum, at the end of the growth phase in the prey, some mycelia extend out of the cuticle and form adhesive conidia spores, which are then picked up by passing prey. Some of the spores remain inside the old cuticle. The Basidiomycetes Nematoctonus also form adhesive conidia spores which then attach to the cuticle of a new prey. The protoplasm migrates out of the hyphae inside the prey and accumulates in conidia bearing branches outside the prey. Several mitosporic species form adhesive dispersal spores, such as Cephalosporium, Mesia and Verticillium. Ingestion of infective spores can also stimulate growth. In the case of Harporiumspecies, the shape of the spore prevents passage through the nematode pharynx into the middle intestine. Sporulation occurs in the oesophageal muscle, and invasive hyphae grow through the organism. One difference between nematotro- phy by soil hyphal fungi (such as the Basidiomycetes genera mentioned here) and others such as Chytrids and Oomycetes is that the latter two tend to grow into the prey, with very few vegetative hyphae in the soil.
In contrast, Basidiomycetes grow extensive saprotrophic hyphae in the soil and only supplement their nutrition with nematodes, or other microinvertebrates. This is particularly important in some lignin-decom- posing fungi (such as the oyster mushroom, Pleurotus), which are other- wise nitrogen limited. The Pleurotus and Hohenbuchelia genera (family Pleorotaceae, order Agaricales, Basidiomycetes) are nematotrophic white rot fungi (Thorn et al., 2000). They secrete a non-adhesive nema- totoxic substance (trans-decenedioic acid) to immobilize nematodes, which are then invaded with hyphae through the orifices. The Hohenbuchelia also produce adhesive knobs, as for the anamorph Nematoctonus.
Hyphal fungi in the soil and litter rely on adhesive mycelium or rings for capturing nematodes and similar sized prey (Fig. 4.14). Barron (1977) distinguishes between six methods as follows.
1. Adhesive hyphae of the Zygomycetes, such as Cystopageand Stylopage, secrete a sticky substance. Trapped invertebrates will fight it to exhaus- tion. Branching mycelia grow into the prey. The protoplasm moves out of the hyphae in the prey and grows outside the prey. These vegetative hyphae in the soil near the prey form conidia.
2. Short adhesive branches or rings occur in only a few mitosporic species. For example, Dactylella tylopage captures amoebae on its sticky surfaces, although other species in the genus capture nematodes, which become stuck at several points. Only a few seconds of contact are suffi- cient, and mycelial growth begins rapidly. Nematodes can withdraw quickly enough to avoid being trapped, often succeeding. Sometime they try to proceed only to be caught again.
3. Adhesive nets are formed by ubiquitous and abundant fungi, such as Arthrobotrys. These form more extensive adhesive hyphae branches and rings. Some species secrete toxins which help to immobilize or kill the prey while mycelia grow into it. As in other groups, the protoplasm retracts from the hyphae in the prey and grows outside the cuticle which is left almost empty. Conidia form outside the cuticle from these later emerging branches.
4. Adhesive knobs are formed by several Basidiomycetes, such as Nematoctonus and Hyphoderma, and mitosporic fungi such as Dactylaria.
These consist of single adhesive cells at the end of short branches, which can be broken off by a struggling prey. Each adhesive cell, once attached to a nematode or cuticle, will grow invasive hyphae. This mechanism
B A
C
B
Fig. 4.14. Examples of protist and invertebrate traps used by filamentous fungi. (A) Zygomycete hyphae coated with a sticky substance, showing a glued nematode. (B) Sticky knob with a coat of sticky substance. (C) Loop of collar cells which constrict around a passing organism.
combines prey invasion with dispersal. The adhesive substance of Nematoctonusis very strong and the knob will not break off. A struggling nematode can escape at the cost of losing some epidermal cells and cuti- cle (causing a wound).
5. Many mitosporic species that form adhesive knobs also form rings that consist of three cells. These break off, so that the nematode carries a collar of three cells which grow mycelia through its cuticle to digest the nematode.
6. Constricting rings also consist of three cells, with a fourth supporting cell and a fifth which branches from the main mycelium. These also occur in the genera Arthrobotrys andDactylaria. The collar is about 20 µm in diam- eter and constricts inward within 0.1 s by rapid uptake of water. The collar cells constrict around the nematode, then grow into the caught prey.
Predatory microinvertebrates
Numerous genera of Acarina are implicated in predation, or facultative predation (Table 4.12). These would include many of the species of piercing-sucking mites and the nematophagous mites mentioned previ- ously (Walter and Proctor, 1999). For example, the Cunaxid mite Coleoscirus simplex (piercing–sucking) can move 20 cm/min in the labora- tory at 25C to attack a prey. The dominant predatory mites are the Mesostigmata (suborders Dermanyssina and Parasitina) and several fam- ilies of Prostigmata. The Mesostigmata and the Rhagidiidae (Prostigmata) species are fast and constantly searching for prey, so that time spent foraging is important in understanding their behaviour.
Some of the Prostigmata families include the Bdellidae, Cunaxidae (Bdelloidea); the slow moving Labidostommatidae; seven of the eight Anystina families; both Erythracoidea; the adults of the Trombidiioidea (red velvet mites); one Chyletinae subfamily; and nine families of Raphignathoidea, particularly in drier soils. Among the Mesostigmata, the Laelopidae include particularly aggressive predators (not all are edaphic species) that are used in greenhouses for pest control, such as Hypoaspis,Geolaelaps andStratilaelaps.
Among the Collembola, Frisea species are known to prey on tardi- grades, rotifers and invertebrate eggs. The Antarctica species Cephalotoma gradicepspreys on other Collembola, as well as Isotoma mac- namarai(Denis, 1949; Hopkins, 1997).
The main predators of microarthropods and of other predatory microinvertebrates are larger litter invertebrates which are part of the meso- and macrofauna (Coleman and Crossley, 1996). The predominant ones are Opiliones, hunting spiders and those with webs in the litter, pseudo-scorpions and ants. Some beetles are specialists on particular prey.
For example, setal and antennal traps of carabid beetles or Stennus comma
(Staphylinid) are effective predators on Collembola. Predation of the cara- bid beetle Notiophilus biguttatus on the Collembola Orchesella cincta showed that there was positive density-dependent mortality of the Collembola (de Ruiter et al., 1988). This suggested a Holling (1959) type III sigmoid func- tional response. It also suggests that the beetle can, in theory, control the abundance of the prey species. The beetle also exhibits some prey prefer- ence and optimal foraging behaviour (Ernsting and van der Werf, 1988).
Earthworms
Earthworms have a diurnal rhythm and tend to be more nocturnal, probably to avoid ultraviolet light, solar radiation and desiccation. They are active when there is sufficient moisture and become inactive as the soil dries, by dehydrating and entering dormancy. The earthworms are generally placed into three functional groups based on the observations of Bouché (1977) on Lumbricina. Epigeic species tend to tunnel through the surface litter and organic horizons near the surface. They have a preference for partially decomposed litter and ingest rich organic matter and surface litter. Some species can also be found in animal dung (some species of Lumbricus and Aporrectodea), composts or under tree bark. Anecic species reside in deeper permanent burrows and emerge at night to drag selected leaf litter into their tunnel. The litter is eaten in the tunnel and in some species the excreted material, the earthworm cast, is deposited on the soil surface. Endogeicspecies tend to remain in the mineral soil horizon, where there is less organic matter. They can feed on rootlets and ingest whole soil to digest the organic component, including the living organisms. Truly endogeic species avoid composts and soils rich in organic matter. Therefore, some earthworms can be found in tunnels or burrows several metres below the surface, though most occupy the top 30–60 cm of the profile. Many species do not fit neatly into these categories and are best described as intermediates.
Others may be predators, such as the Chaetogaster (Naididae) which are reported to hunt and prey on microinvertebrates (Avel, 1949, p. 387).
The integument of earthworms is permeable to the soil solution through the coelomic pores, and bacteria or protist cells potentially can enter this space. Richard and Arme (1982) demonstrated that the soil solution could enter the coelom, but it was insufficient to be a source of food.
Mark recapture has been possible using a variety of labels, such as dyes, fluorescent stains and radioactive tracer, and it contributes to under- standing the behaviour and function of individuals.
The main earthworm predators vary with the ecosystem and region- ally. When they are out of the soil, particularly when the soil is wet, they are preyed on by a variety of birds (during the day), and surface preda- tory arthropods, such as ants, centipedes and Carabid beetles.