Effects On Invertebrate Behaviour

A wide range of volatile organic compounds (VOCs), including alcohols, terpe-nes, aldehydes, ketones, sesquiterpenes and aromatics, are produced by Basiomycota fruit bodies (Faldt et al., 1999; Rosecke et al., 2000), mycelium (Hynes et al., 2007) and decomposing organic resources (Cole et al., 1989), and often increase in quantity and quality if physically damaged (Stadler and Sterner, 1998; Faldt et al., 1999) or during inter-specific mycelial interactions (Hynes et al., 2007; Chapter 7). Likewise, dissolved organic compounds (DOCs) are also produced (e.g. Su, 2005). Invertebrate responses to VOCs and DOCs include attraction, repulsion, arrestant and antifeeding behaviour (Table 2).

Effects on termites are particularly well documented (see references in Swift and Boddy, 1984; Su, 2005). Mycelium of brown-rot fungi (Chapter 2), wood

Os Os

Table 2 Examples of effects of basidiomycota on animal behaviour

Fungus/compound

Invertebrate

Nature of effect

References

Agaricus bisporus mycelium

Megaselia halterata

Attraction of gravid

Tibbles et al. (2005), Smith

(Phoridae)

females to mycelium

et al. (2006a)

Agaricus bisporus mycelium

Lycoriella ingenua

Tibbles et al. (2005), Smith

(Sciaridae)

et al. (2006b)

Perennial fruit bodies

Ciid beetles

Long- and short-range

Jonsell and Nordlander

attraction and inter

(1995), Guevara et al.

specific discrimination

(2000a, 2000b), Jonsson

et al. (2003)

Mating incompatible

Bradysia sp. (Sciaridae)

Apparent attraction to

Boddy et al. (1983)

mycelia of Stereum spp.

mycelial interaction zone

and Phlebia spp.

Conocybe lactea mycelium

Nematodes

Activity arrested and

Hutchison et al. (1995)

antifeedant

Brown-rot fungi, e.g.

Reticulitermes, Heterotermes,

Attraction

Swift and Boddy (1984), Su

Ganoderma applanatum,

Coptotermes, Kalotermes

(2005)

Gloeophyllum trabeum,

spp., Rhinotermitidae

Serpula lacrymans

Sesquiterpenes

Antifeedant activity or are

Kahlos et al. (1994), Stadler

ultimately toxic to

and Sterner (1998)

invertebrates

Cadinenes, muurolenes

Many

Used insect

El-Sayed (2005), Hynes

and amorphenes

communication systems

et al. (2007)

decomposed by them and extractives from such wood are often attractive to termites, and VOCs can stimulate termites to eat more sound wood and build more galleries. White-rot fungi and white-rotted wood are often unattractive and even toxic to termites, though P. ostreatus was attractive. White-rot fungal mycelia are, however, attractive to other arthropods. For example, fungus gnats (Bradysia; Sciaridae) are highly attracted to and oviposit in interaction zones of mating incompatible mycelia of Stereum spp. and Phlebia spp. (Boddy et al., 1983; Figure 2a). Collembola are also attracted to and preferentially graze in interaction zones between mycelia growing from woody resources into soil (Figure 2b). These regions are presumably more palatable and leak nutrients, and VOCs are upregulated (Hynes et al., 2007). Sciarids and phorids (Diptera) are attracted to the mycelium and compost of cultivated mushrooms (Agaricus species; Grove and Blight, 1983; Tibbles et al., 2005). There were, however, large differences in the sizes of phorid populations emerging from different Agaricus species and strains of the same species, which may have resulted from differences in numbers of females choosing to oviposit, as a result of lack of attractants or production of inhibitory chemicals by some strains but not others (Smith et al., 2006a, 2006b).

Not only are direct utilizers of fungi attracted by mycelium and colonized organic resources, but so also are parasitoids of direct users. Thus, Ibalia leucospoides, a parasitoid of the wood wasp Sirex noctilio that lives in association with the wood decaying Amylostereum areolatum, was attracted by volatiles emitted by the fungus (Martinez et al., 2006). The fungal VOCs also appear to elicit increased parasitoid activity, and it has been speculated that they may provide information on the relative densities of host wood wasps (Martinez et al., 2006).

Some fruit bodies produce VOC attractants, the attraction of Diptera to the spore mass of P. impudicus being a classic example. Ciid beetles live and breed in the fruit bodies of lignicolous Basidiomycota, and exhibit specific host-use groups (Orledge and Reynolds, 2005). They use VOCs for location of fruit bodies and discrimination of suitable species. For example, C. boleti and O. glabriculus were attracted to T. versicolor, whereas C. nitidus was attracted to Ganoderma sp., and Cis bilamellatus was attracted to both (Guevara et al., 2000b). VOCs are apparently used over long and short distances (Jonsell and Nordlander, 1995; Guevara et al., 2000a, 2000b; Jonsson et al., 2003), though whether the same chemical cues are involved in both instances is not known.

VOCs are also sometimes involved in the regulation of breeding (Guevara et al., 2000a). Both O. glabricus and C. boleti feed and breed in T. versicolor fruit bodies, but O. glabricus colonizes young basidiocarps in early spring while C. boleti is most abundant in autumn. O. glabricus was actually attracted to both old and young fruit bodies but C. boleti was only attracted to older fruit bodies. The implication is that changes in VOC emission as fruit bodies age cause a partitioning of resource use by these two ciid beetle species. Differences in attraction in the field may not be as clear-cut as in these laboratory experiments since other abiotic variables may modify effects. For example, the relative attractiveness of two non-Basidiomycota species for oviposition by Lycoriella inegnua (Sciaridae) completely changed with CO2 enrichment of the leaf litter in which they grow (Frouz et al., 2002).

Figure 2 Preferential grazing by invertebrates in interaction zones. (a-e) Interactions between mycelia growing from 2 x 2 x 2 cm wood inocula across compressed non-sterile soil. (a) Considerable grazing by Folsomia candida (Collembola) of Resinicium bicolor (left) in the region of interaction with Hypholoma fasciculare. (b) Localized F. candida grazing (arrowed) of H. fasciculare near interaction front. (c) Grazing by F. candida of both H. fasciculare (left) and R. bicolor in the interaction zone. (d) F. candida grazing of Phanerochaete velutina and R. bicolor. Note that grazing of P. velutina is largely in regions (arrowed) where cords of R. bicolor had overgrown P. velutina. The R. bicolor cords in these regions were completely removed by grazing. (e) Fungus gnat grazing (arrowed) largely in the interaction zone between non-mating compatible homokaryons of Stereum gausapatum in agar culture. Note grazed regions (arrowed) in interaction zone. (f) Grazing (arrowed) by F. candida in the interaction zone of P. velutina (left) and R. bicolor, centred largely on the latter, in agar culture. Scale bar 1 cm. (a)-(d) and (f) courtesy of T.D. Rotheray. (See Colour Section)

Figure 2 Preferential grazing by invertebrates in interaction zones. (a-e) Interactions between mycelia growing from 2 x 2 x 2 cm wood inocula across compressed non-sterile soil. (a) Considerable grazing by Folsomia candida (Collembola) of Resinicium bicolor (left) in the region of interaction with Hypholoma fasciculare. (b) Localized F. candida grazing (arrowed) of H. fasciculare near interaction front. (c) Grazing by F. candida of both H. fasciculare (left) and R. bicolor in the interaction zone. (d) F. candida grazing of Phanerochaete velutina and R. bicolor. Note that grazing of P. velutina is largely in regions (arrowed) where cords of R. bicolor had overgrown P. velutina. The R. bicolor cords in these regions were completely removed by grazing. (e) Fungus gnat grazing (arrowed) largely in the interaction zone between non-mating compatible homokaryons of Stereum gausapatum in agar culture. Note grazed regions (arrowed) in interaction zone. (f) Grazing (arrowed) by F. candida in the interaction zone of P. velutina (left) and R. bicolor, centred largely on the latter, in agar culture. Scale bar 1 cm. (a)-(d) and (f) courtesy of T.D. Rotheray. (See Colour Section)

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