Collembolan grazing affects the growth strategy of the cord-forming fungus Hypholoma fasciculare

Abstract

Mycelia of cord-forming fungi show remarkable patterns of reallocation of biomass and nutrients indicating an important role of these, often extensive, organisms in the spatial translocation of energy and nutrients in forest soils. Despite the rich tradition of interaction studies between soil microarthropods and fungi, the spatial implications of these interactions, due to the potential growth responses of the fungi and to the translocation of energy and nutrients within the mycelial network, have been largely ignored. In this paper we analyse fungal growth responses in two-dimensional model systems composed of compressed soil, the cord-forming fungus Hypholoma fasciculare and three fungivorous Collembolan species. We hypothesised that (i) the highly co-ordinated nature of cord-forming fungi would lead to growth responses following collembolan grazing, and that, (ii) such changes are dependent on grazing intensity, and (iii) changes are dependent on the species grazing. Mycelial extent and hyphal cover decreased with increasing grazing density; at highest grazing density also the fractal dimension of the mycelial border decreased, indicating a less branched foraging front due to the regression of fine hyphae and the development of mycelial cords. Effects differed greatly between collembolan species although they exerted comparable grazing pressure (the smaller species were added in larger numbers according to their allometric size-metabolic rate relationships): while grazing by Folsomia candida resulted in less mycelial extension and hyphal cover, these variables were not affected when Proisotoma minuta and Hypogastrura cf. tullbergi grazed. The effects of a species mix suggested an additive effect of the component species. This shows that fungal mycelia may suffer from damage caused by few but large collembolans, affecting extension as well as coverage of the mycelium, but that fungi may compensate for the biomass loss caused by more but slightly smaller collembolans. In about 20% of the model systems H. fasciculare switched from a growth pattern with a broad contiguous foraging front and uniform growth in all directions to a pattern with fast growing sectors while other sectors stopped growth completely. The switch occurred in grazed systems exclusively; thus we interpret this observation as a fugitive response and as a strategy for quickly escaping from places where grazing pressure is experienced. q

Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots

“…Unfortunately, we know little about fungal defence strategies against fungivores which are probably as complex as bacteria-predator relationships (Kampichler et al 2004;Scheu and Folger 2004;Scheu and Simmerling 2004;Harold et al 2005;Bretherton et al 2006;Tordoff et al 2006Tordoff et al , 2008Wood et al 2006).…”

Saprotrophic cord systems: dispersal mechanisms in space and time

“…1), microclimate (Donnelly and Boddy 1997a;Owen 1997;Wells et al 2001), nutrient status of the mycelial system to which they are connected and of the resource from which they are growing (Bolton and Boddy 1993;Donnelly and Boddy 1997b;Boddy et al 1999;Zakaria and Boddy 2002), nutrient status and structure of the environment through which they are growing (Donnelly and Boddy 1998;Boddy et al 1999;Zakaria and Boddy 2002), interaction with other mycelia (Donnelly and Boddy 2001), invertebrate grazing (Kampichler et al 2004;Harold et al 2005;Bretherton et al 2006;Tordoff et al 2006;Wood et al 2006), and time, size, and age of the system Boddy et al 1999). Outgrowth patterns range between mycelia characterized by diffuse, slowly extending search fronts, with a high mass fractal dimension (D M close to 2 in two dimensions), and open systems characterized by well-defi ned, rapidly extending cords throughout the system, with a lower D M (between 1 and about 1.8).…”

“…This concept is clearly seen in the improved global transport effi ciency of the uniform MST, even though the MST would be expected to be very vulnerable to disconnection during attack. Robustness to damage, e.g., by physical breakage or grazing by invertebrates (Kampichler et al 2004;Bretherton et al 2006;Tordoff et al 2006;Wood et al 2006;Jones 2007, 2008), is of major significance to long-lived mycelial systems. Having a large number of alternate pathways is important in this context, and the differential strengthening of links not only imparts high transport capacity but also robustness to damage, which can be seen by examining the effects of breaking links in models of the fungal networks compared with corresponding uniform networks.…”

Fractal Geometry and Microorganisms in the Environment

“…Much research has focused on the grazing of soil invertebrates on fungal mycelia, but the spatial implications due to fungal growth responses have received little attention. Microarthropod grazing results in dramatic changes in mycelial morphology (Figure 8.10), including changes in fractal structure [73]. When the collembolan Folsomia candia grazed on Hypholoma fasciculare, at different grazing intensities (20,40 or 60 collembola added to mycelia with a radius of 1.5 cm), there was no significant difference in D BM , but D BS differed significantly: from 30 days D BS was significantly higher in controls and decreased monotonously with increased grazing intensity.…”