Fungivory

Species that feed on filamentous fungi and yeasts are referred to as fun-givorous or mycophagous. Feeding on fungi is distinguishable from other protists in that the fungal cell wall is difficult to penetrate and digest. Mycophagous species are specialized for penetrating or ingesting hyphae. In this section, we will distinguish between two types of fun-givory. The first involves removing a length of hyphae, or hyphal bundle from mycorrhizae and fruiting bodies (ingesters). Ingesters remove hyphal lengths by ingesting the cell wall and chewing it. It is more common among microarthropods, such as a variety of mites and Collembola. Lengths of hyphae can be recognized along their digestive tract. The second involves piercing a hole in hyphae to ingest the cytoplasm (piercers). Piercers puncture a hole through the cell wall, which is otherwise intact. This avoids having to feed on the chitin wall which is difficult to digest. Instead, the cytoplasm is ingested and a length of hyphal wall empty of cytoplasm remains. This mechanism is more common in nematodes, amoebae and several colpodid ciliates. It is worth noting here that although many organisms can ingest fungal spores or whole yeast cells, these are not necessarily digested. Observations on recovered spores, cysts and yeast cells, from faecal pellets or excreted from amoebae and ciliates often report viability of a fraction of the material after egestion (e.g. Behan and Hill, 1978; Anderson, 1988).

However, in some cases, there is evidence for feeding on yeasts or spores. One study showed a reduction of spores placed on filter membranes set out in the field, which correlated with microarthropod faecal pellet accumulation on the membranes (Gochenaur, 1987). This resulted in an 80% decline of spores of one species in the autumn, reflecting some selective grazing. A second study showed that microarthropod grazing, primarily by Collembola on perithecia of pathogenic fungi, eliminated the infection the next year (Kessler, 1990). Two pathogens of black walnut (Juglans nigra), Mycosphaerella juglandis (causing leaf spots) and Gnomonia leptostyla (causing anthracnose) form perithecia in fallen leaves, which could be eaten by the microarthropod fauna. In areas with less surface litter, where soil microarthropods were not abundant, the perithecia survived to re-infect trees in the next year. Selective preferences for different yeast were reported for six mite species in beech forests (Maraun et al. (2000). With protozoa, Ekelund (1998) modified the MPN approach to enumerate those that would grow on yeasts and spores. That approach was not suitable to enumerate mycophagous amoebae.

Hyphae ingesters

A variety of organisms are known to graze on lengths of hyphae, or on bundles of hyphae. Collembola and mites are the better studied hyphae ingesters in the soil. Some can be found several metres deep along roots, grazing on mycorrhizae or dead roots. Other fungivores include some armoured nematodes (Fig. 4.12), enchytraeids, meso-fauna invertebrates and small mammals (particularly on aerial fruiting bodies). There is some evidence that juveniles and smaller species of microarthropods are more dependent on bacteria and protozoa in the soil solution, whereas larger individuals can ingest hyphae (Bakonyi, 1989).

Collembola. Most Collembola in the soil are considered to be at least partially fungivorous, especially Hypogastrura, Tomocerus and Sminthurinus. Grazing interactions between Collembola and hyphae can affect both the vertical distribution of fungal species and the rate of decomposition. The Collembola Onychiurus latus feeds preferentially on hyphae of Marasmius androsaceus, rather than Mycena galopus, at a Picea plantation in England (Newell, 1984a). The two Basidiomycota which represent 99% of the sporocarps are restricted spatially by this grazing. The preferred prey M. androsaceus occurs in the H (or Ao) horizon, and the other in the A1 horizon. When the abundance of the Collembola was increased experimentally at the site, the abundance of the preferred prey was reduced (Newell, 1984b). The less preferred M. galopus is a slower decomposer and, thus, there was accumulation of forest floor litter at the experimental site. Moore et al. (1985) showed that the Collembola species Folsomia candida, Onychiurus encarpatus, O. folsomi and Proisotoma minuta would feed on hyphae of the arbuscular mycorrhizal fungus Gigaspora rosea, none ate G. mosseae, and only F candida ate G. fasciculatum. In a hyphae choice experiment, F. candida was offered a variety of arbuscular mycorrhizal (Zygomycetes and Glomales) and saprotrophic species (Klironomos et al., 1999). The Collembola were followed over two generations, and the numbers of eggs laid and hatched were counted. The results showed that saprotrophic species offered were preferred to the mycorrhizal species of fungi. Furthermore, when fed on single species or less preferred hyphae, the reproductive success of the F1 generation was reduced because the number of eggs laid was greatly reduced. One possibility for the bias could be hyphae diameter, so that finer mycelia are grazed preferentially by microarthropods (Klironomos and Kendrick, 1996). Another possibility is the secretion of glomalin by the Glomales, which may have a defensive role against grazers. In a separate study, Onychiurus subtenuis (Collembola) and Opiella nova (Oribatei) were found to prefer the larger diameter hyphae of the saprotrophic fungal species offered, when the fungi were cultured on agar (Kaneko et al., 1995). This was not true when the fungi were grown on their natural substrate of pine needles. However, both species showed some food preferences even in field trials.

The overall effect of fungivory by hyphae ingesters was investigated in a microcosm grazing study, where the abundance of grazers was altered (McLean et al., 1996). Despite the significant, and sometimes limiting effect of fungivory on hyphal growth, it is not clear whether grazing is intense enough to reduce species richness of fungi. This study concluded that even at twice natural abundances, their microcosm study did not change the number of fungal species, species frequency or species dominance, in pine needle fungi grown on agar. This example is contrary to the previous examples above (Gauchenaur, 1987; Kessler,

1990) where, in field studies, the Collembola grazer was shown to reduce species abundance. There are limits to interpretation of microcosm studies when not repeated in situ.

The interactions of fungi with their grazers is more complicated than one would imagine initially. For example, some Collembola are attracted to hyphae species by odour. However, a predacious species of mite is also attracted by the odour of hyphae, in order to find its Collembola prey (Hall and Hedlund, 1999). The effect of grazing on the hyphae can also modify the growth physiology of the fungus locally. After several days of being grazed by the Collembola Onychiurus armata, the Zygomycetes Mortierella isabellina switched to a faster aerial mode of growth, correlated with increased protease secretion (Hedlund et al.,

1991). It is unclear whether the protease was being secreted to favour growth or if it was defensive.

Hyphae piercers

Nematodes with narrow tubular stylet and mycophagous amoebae are the more abundant organisms in this category. Some colpodid ciliates are also known to specialize in piercing hyphae. The impact of fungivo-rous nematodes on hyphal growth was studied in a series of microcosm studies recently (Ruess et al., 2000). The role of spore and hyphae-pierc-ing amoebae was reviewed earlier (Old and Chakraborty, 1986). Some species of Myxobacteria, otherwise better known for their lysis of bacterial colonies, are also reported to feed on hyphae and conidia by digesting a perforation into the cell wall (Homma, 1984). Many of the Acarina with fine stylet-like chelicerae (piercing-sucking group) pierce hyphae to ingest the protoplasm (Walter and Proctor, 1999). Some mites feed primarily on fungi (such as Ameroseiidae) while others are facultative fun-givores and predacious (such as the Mesostigamata Proctolaeleps, Protogamasellus and Uropodina). The Tydeidae are primarily fungivores, which are also important predators on nematodes.

Nematodes. In a series of feeding experiments between fungivorous nematodes and fungal hyphae, it became clear that different nematodes preferred to graze on different hyphae (Ruess and Dighton, 1996; Ruess et al., 2000). Species of Aphelenchoides, Aphelencus and Ditylenchus were tested on a variety of hyphae on nutrient agar plates. Some fungal feeders would not feed on the hyphae offered; others grew well with preferences for certain hyphae. These types of studies usually stress the importance of mixed diets for long-term cultivation of fungivores. Preferential feeding on mycorrhizae would suggest that these fungivores should be more abundant in the rhizosphere of mycorrhizal roots than in non-rhizosphere soil. Overall, the nematodes tested grew better on mycorrhizal fungi than saprotrophic hyphae. Some saprotrophic fungi are known to have nematicidal substances (Cayrol, 1989). Interestingly, several plant feeders were observed to feed on the ectomycorrhizae, and one bacterivore could grow on the agar film (apparently axenically). It is from similar observations that nematode feeding groups based on stoma morphology alone provide a false sense of rigidity or specialization in food choice. Although many species are specialists and rely on one feeding mechanism, many other species are more flexible and supplement their diet with a variety of food sources, especially when preferred food items are less abundant.

Amoebae. A variety of amoebae genera are recognized to be fungivores at least some of the time (facultative), such as Acanthamoeba, Arachnula, Gephyramoeba, Mayorella, Ripidomyxa, Saccamoeba, Thecamoeba, Theratromyxa and Vampyrella, although some are obligate fungivores such as Thecamoeba granifera minor and Cashia mycophaga (Old and Chakraborty, 1986; Foissner, 1992). Most attach to the surface of a length of fungal mycelium or spore and dissolve a perforation through the chitin cell wall (Fig. 4.13). A pseudopodium is sent into the cell through the pore, usually 2-6 |im wide, although some as small as 0.2 |im are possible by species with filopodia. The perforation is probably caused by fusion of lysosomes with the cell membrane, digestion of the cell wall and penetration of the amoeba's pseudopodia into the cytoplasm of the mycelium. Ingestion of the cytoplasm is by phagocytosis and pinocytosis, and digestion is in food vacuoles. In some species, observations suggest that at first the amoeba attempts to ingest the spore or mycelium and, if it proves too large, it releases enzymes to digest part of the wall before invading the prey with pseudopodia. Old

Fig. 4.13. Filose amoeba penetrating into fungus cells. The cell wall is digested to create a narrow opening and ingestion of the cytoplasm with invasive filopodia.

Fig. 4.13. Filose amoeba penetrating into fungus cells. The cell wall is digested to create a narrow opening and ingestion of the cytoplasm with invasive filopodia.

and Chakraborty (1986) reviewed several papers that observed ingestion of cysts and spores. However, not all studies confirmed continued growth on this diet, or checked the egested cysts and spores for viability. It is safer to assume that at least a portion of the cysts and spores are excreted viable at a distance (Wolff, 1909; Heal, 1963; Chakraborty and Old, 1982). None the less, many species, such as Mayorella, clearly are able to ingest and digest spores or cysts. There is some evidence that melanin pigmentation of fungal cell walls provides some resistance to lytic enzymes, but this is not a generalization, because the same fungi can be eaten by mycophagous amoebae (Old and Chakraborty, 1986).

Other amoebae that are not normally recognized as mycophagous, such as Hartmanella and Schizopyranus, also produce cellulase and chiti-nase (Tracey, 1955), to digest fungal cell walls and plant cell walls (in the microdetritus). Since other organisms also possess chitin, such as microinvertebrates, then it is not surprising that these are also preyed on by some mycophagous amoebae. For example, the well-known mycophagous genus Arachnulla (Cercozoa: Filosea: Vampyrellidae) and the giant amoeba Leptomyxa also attack and perforate nematodes and diatoms (Old and Darbyshire, 1978; Anderson and Patrick, 1980; Homma and Kegasawa, 1984). This mechanism of perforation feeding is also known to occur in amoebae feeding on filamentous algae (Lloyd, 1927). Many mycophagous species also feed on prokaryotes, although it may not be the preferred food item.

The impact of mycophagous amoebae was reviewed by Old and Chakraborty (1986). Most observations are based on laboratory incubations or pot experiments; much less is known of their impact in situ, where migration and predation also occur, and where conditions for growth are not always suitable. For example, amoeba grazing on ecto-mycorrhizae reduced the extent of fungal colonization of pine roots in pots (Chakraborty et al., 1985). Although the experiments provided an idea of the impact it could have on seedlings and mycorrhizae, it could not establish whether the same would apply in situ. In fields that were infected with a plant pathogenic fungus, the mycophagous amoebae could reduce but not eliminate the abundance of spores in the soil (Chakraborty, 1985; Chakraborty and Warcup, 1985). Therefore, in agricultural soils that would support amoebae, i.e. with adequate organic matter to support microorganisms, there is the potential to reduce infectivity greatly in successive years.

Some families of Prostigmata and Endostigmata (both Acarina) have stylet-like chelicerae that puncture hyphae and other prey, such as microinvertebrates and protists (Table 4.12), if they can be immobilized (Walter, 1988; Kethley, 1990; Curry, 1994). The drained solution and cytoplasm are externally partially digested and sucked in by the oral structures.

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