Elsevier

Fungal Ecology

Volume 4, Issue 1, February 2011, Pages 42-55
Fungal Ecology

Grazing by collembola affects the outcome of interspecific mycelial interactions of cord-forming basidiomycetes

https://doi.org/10.1016/j.funeco.2010.09.001Get rights and content

Abstract

While there is a plethora of studies on the effects of invertebrate grazing on mycelia, including several studies on saprotrophic cord-forming basidiomycetes, there is little information on the effects of grazing on mycelial interactions. The study compares the progress and outcomes of interspecific mycelial interactions between Hypholoma fasciculare, Phallus impudicus, Phanaerochaete velutina and Resinicium bicolor when grazed by the collembola Folsomia candida or Protaphorura armata in agar culture and trays (24 × 24 cm) of non-sterile soil. In ungrazed systems results were broadly consistent with previous studies, though there were few instances of deadlock, and a clear transitive (A > B > C) hierarchy could not be discerned. Instead, there was an intransitive hierarchy (i.e., A > B, B > C but C > A). Additionally, in agar culture, there were considerable differences in combative ability of four different strains of H. fasciculare.

Collembola grazing had major effects on mycelial interactions. F. candida grazing altered both the outcome and progression of half of the fungal interactions studied, while the less active P. armata had almost no discernable effects on fungal interactions. Grazing by F. candida affected mycelial extension rate in five of the interaction combinations, some increasing, others decreasing. In grazed systems of P. velutina interacting with H. fasciculare, extension rate of the former was much more rapid over the opponent than over soil. Not only did grazing affect mycelial interactions, but interactions affected grazer activity; H. fasciculare was grazed in areas where it was interacting with P. velutina mycelium, but less so elsewhere.

By altering the outcome of mycelial interactions and mycelial extension rate, collembola grazing may alter the distribution of cord-forming fungi on the forest floor, and may also play a role in maintaining the diversity of fungal species. The differences in combative ability of different strains of a species imply an even more complex scenario in the natural world.

Introduction

As many species of saprotrophic cord-forming fungi occupy similar spatial niches at the soil–litter interface, interactions are inevitable (Boddy 2000). Interspecific fungal interactions are highly aggressive and generally occur following gross mycelial contact (Boddy 2000). Interactions result in either deadlock or some form of replacement (i.e. partial, complete, or mutual); these outcomes are variable and can be substantially affected by both biotic and abiotic variables (Chapela et al., 1988, Woods et al., 2005). Intraspecific genetic variability may also be important in determining fungal interaction progression and eventual outcome, although most studies investigating interactions of higher fungi have tended to concentrate on a single strain of each species. A few studies with Trichoderma species (Ascomycota) interacting with wood-decay fungi have involved multiple strains (see Philp et al., 1995, Wheatley et al., 1997) but most of these have focussed on strains of medical or biocontrol value (Walker et al., 1995, Vainio et al., 2001). Despite possible implications for both species abundance and diversity, the role played by fungal genetic variability in fungal fitness remains unknown.

As well as encountering other fungi, non-unit-resource-restricted fungi (sensu Cooke & Rayner 1984) growing out from resources are also more accessible to grazers. Various soil invertebrate taxa, including Nematoda, Collembola and Oligochaeta, are known to graze on fungal mycelia and can substantially alter fungal morphology and physiology (Ruess et al., 2000, Harold et al., 2005, Tordoff et al., 2006, Boddy and Jones, 2008). Such effects are likely to alter fungal fitness and, therefore, their combativeness in interactions with other soil microorganisms, including fungi.

The visible changes in morphology and physiology during fungal interactions are associated with biochemical changes, such as increased enzymatic activity and production of diffusible (DOC) and volatile (VOC) organic compounds (Griffith et al., 1994, Baldrian, 2004, Hynes et al., 2007, Evans et al., 2008). This enhanced activity may also lead to lysis of hyphal compartments and nutrient leakage into the surrounding environment (Wells & Boddy 2002). Numerous plant species use chemicals emitted as a result of insect–herbivore action to attract parasitoids to the vicinity (Dicke, 1994, Tentelier and Fauvergue, 2007), and a comparable process may occur with fungi. Mycophagous grazers may use chemical cues arising from interaction activity to locate high quality resource patches while fungi may actively recruit grazers to provide a competitive advantage over an opponent. Orientation to fungal odours by invertebrates has been well documented (Swift and Boddy, 1984, Hedlund et al., 1995, Guevara et al., 2000) and anecdotal evidence exists of attraction of fungus gnats to fungal interaction zones (Boddy et al. 1983).

This study aims to: (i) elucidate the effects of invertebrate grazing on the morphology and competitive abilities of saprotrophic cord-forming basidiomycetes when interacting interspecifically; (ii) determine whether physiological and chemical changes in the mycelium, such as pigment production, may affect invertebrate behaviour (e.g. with preferential invertebrate grazing at interaction zone); (iii) determine whether different fungal strains of the same species affect fungal combativeness and invertebrate grazing. One set of experiments was performed in agar culture, and another set in trays of soil. Though soil trays are more realistic, agar culture allows many more combinations to be performed.

Section snippets

Collembola culturing

Folsomia candida and P. armata were cultured in 0.6 l plastic tubs with pierced lids for aeration. Each tub contained 9:1 plaster of Paris (Minerva Dental Ltd., Cardiff, UK): activated charcoal (Sigma, UK). Collembola were provided with dried baker’s yeast (Saccharomyces cerevisiae, Spice of Life Ltd., Cardiff, UK) weekly. Tub moisture was maintained with deionised water (DI).

Experimental F. candida were selected using a stacked sieving system with sieves of known pore size, the larger sieves

Outcome of interactions in agar culture

H. fasciculare: It was combative, several strains replacing R. bicolor, and being replaced only occasionally by P. velutina and R. bicolor 1. H. fasciculare 4 was, however, sometimes replaced by R. bicolor and P. velutina though not P. impudicus. There were marked differences between different strains of the same species. H. fasciculare 3, for example, replaced R. bicolor 1 whereas H. fasciculare 4 did not (Table 1). H. fasciculare 1 was the most combative of the four isolates, and H.

Discussion

The outcomes of ungrazed interations in agar and soil were similar to those reported in previous studies of the same species (Dowson et al. 1988). Importantly, outcomes on agar varied depending on strain (only single strains were studied on soil), H. fasciculare 1 being more combative than the other three strains. Such intraspecific variation in combativeness has also recently been reported in the non-cord-forming basidiomycete, Hericium coralloides (Crockatt et al. 2008). Thus, care must be

Conclusions

Saprotrophic fungi play a critical role in ecosystem function making recalcitrant nutrients available for continued plant primary productivity. These nutrients tend to be retained in mycelia, but are probably released during mycelial interactions (J.M. Wells & L. Boddy unpub.). Further, invertebrate grazing of the microbial communities (including fungi) can increase the rate of carbon mineralisation (Bardgett et al., 1993, Cole et al., 2000). The present study indicated that collembola may also

Acknowledgements

We thank the Natural Environment Research Council for provision of a studentship (TDR), and the Cardiff University Mycology Research Group for useful comments on the manuscript.

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