the significance of grazing on fungi in nutrient cycling

The significance of grazing on fungi in nutrient cycling

Terence P. McGonigle

Abstract: Excretion of N by fungal grazers is not the dominant process by which N is released in nutrient cycling: it accounts for one eighth or less of total net N mineralization. Fungivores comprise between 21 and 76% of the fauna biomass. Other fauna, as well as fungi and bacteria, all participate in the mineralization process. Microcosm studies have shown fungal grazing can promote release of N, but immobilization by concomitant microbe production can occur in tandem with that release. Studies using field applications of biocides have had inconsistent outcomes. Fungivores contribute to nutrient cycling by the combined action of comminution, mixing, and dispersal of inoculum, which promote microbial activity. Passage through the Collembola gut has been estimated to have the capacity to bring about a 42-fold increase in nitrate concentration from food to faeces, which on an ecosystem scale could conceivably translate into a doubling of levels of nitrate. Recent laboratory work has shown that fungivores may prefer the thinner mycorrhizal hyphae that occur some distance away from the more coarse mycorrhizal hyphae in the rhizoplane. Where this occurs, grazing can be expected to have only a small impact on the effectiveness of mycorrhizal fungi for the promotion of plant nutrient absorption in the field.

Key words: fungivores, fauna, soil, litter, mineralization, mycorrhizal effectiveness.

R&sumC : L'excrCtion de N par les brouteurs fongiques n'est pas le processus principal conduisant au reldchement de l'azote dans le cyclage des nutriments : il rend compte de moins d'un huitibme ou moins de I'azote total minCralisC. Les fongivores constituent de 21 21 76% de la biomasse faunique. D'autres membres de la faune aussi bien que des champignons et des bacttries participent tgalement au processus de mintralisation. Les Ctudes de microcosmes montrent que les brouteurs fongiques peuvent provoquer le reldchement de N, mais on peut observer une immobilisation microbienne concomitante, en tandem avec ce reldchement. Les Ctudes au champ avec biocides conduisent a des rtsultats inconsistants. Les fongivores contribuent au cyclage des nutriments par I'activitC combinCe du dCcoupage, du mClange et de la dispersion de l'inoculum, lesquels favorisent l'activitt microbienne. On estime que le passage dans l'intestin des collemboles peut conduire B une augmentation de 42 fois de la teneur en nitrates, de l'aliment aux dijections, ce qui a 1'Cchelle de I'Ccosystbme pourrait bien se traduire par un doublement des teneurs en nitrate. Des Ctudes rCcentes en laboratoire ont montrt que les fongivores peuvent prtftrer les hyphes mycorhiziens les plus minces sur le rhizoplan. LB o~ cette situation existe, on peut s'attendre i ce que le broutage n'ait qu'un effet mineur sur 1'efficacitC des champignons mycorhiziens pour la promotion de l'absorption des nutriments au champ.

Mots clds : fongivores, faune, sol, litibre, minCralisation, efficacitt mycorhizienne. [Traduit par la rCdaction]

Introduction The pool of inorganic nutrients in the soil solution is added

The majority of studies on nutrient cycling in relation to faunal activity have focused on nitrogen (N). The microorganisms in decomposition systems undertake the catabol- ism of substrates with concomitant release of nutrients such as N and phosphorus (P), which are present in organic com- binations in living tissues. At the same time much of the carbon (C) within decomposing substrates is evolved as carbon dioxide (CO?) by respiration. Nutrients, such as potassium, that are in inorganic form in the tissues are quickly released from substrates without need of microbes (Seastedt 1984).

to by microbial mineralization, but it is also used by microbes, which immobilize nutrients during biosynthesis. For example, after 5 days 89% of I5N added to soil as l5NH4I5NO3 had become organically bound (Shields et al. 1973).

This review will assess the role of grazing in decomposition systems in terms of the flow of nutrients through the grazing pathway. This includes the transfer of nutrients from fungal biomass to fungivore biomass and the excretion of nutrients by the fungivores. It is important to make the dis- tinction between standing crop of mass Der unit area or - A

volume and the change in that standing crop with time. Graz- Received August 17, 1994. ing can also influence nutrient cycling by (i) comminution T.P. McGonigle. Department of Land Resource Science, and mixing of the substrate, (ii) dispersal of microbial inocu- University of Guelph, Guelph, ON N1G 2W1, Canada. lum, and (iii) the impact of grazing on fungal vigour (Ander-

Can. J . Bot. 73(Suppl. 1): S1370-S1376 (1995). Printed in Canada 1 ImprimC au Canada

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son and Ineson 1984; Moore et al. 1988). Comminution, mixing, and dispersal of inoculum facilitate further microbial activity. Grazers typically show preferences among fungi in food choice tests. Suppression of a fungus by grazing can allow proliferation of other fungi, or promote bacterial growth. Alternatively, low intensities of grazing can increase the respiration rate or growth of the part of the mycelium that remains behind. Both suppression or stimulation of fungi by grazing can in turn cause either mineralization or immobilization of nutrients, depending on the type of fungus and on the availabilities of those nutrients relative to that of C.

Aggressively pathogenic fungi will not be treated separately here. Many parasitic symbiotic fungi in soil behave saprotrophically part of the time, and in the present discus- sion of the effect of grazing on nutrient cycling, they will be considered along with saprophytes.

To be mycorrhizal is the normal condition for the majority of plants in the field (Allen 1991). Mycorrhizal fungi absorb nutrients from the soil solution and pass them to plant roots in exchange for simple sugars (Harley and Smith 1983). Arbuscular mycorrhizal (AM) fungi are dependent on sapro- trophs to mineralize the nutrients they require. AM fungi are susceptible to grazing by the soil fauna, and in much the same way as for saprotrophic fungi, they can be expected to form part of the flow of nutrients through the grazing pathway. The responses of mycorrhizal fungi to grazing, in terms of stimulation or suppression of fungal biomass and turnover, have not been studied.

There exists for mycorrhizal systems an additional con- sideration that relates to the role of grazing in nutrient cycling. The ability of mycorrhizal fungi to acquire nutrients over and above those that nonmycorrhizal roots can access is dependent on the spatial arrangement of the extraradical hyphae of the mycorrhizal fungi. The extraradical hyphae extend beyond the nutrient depletion zones around roots and transfer otherwise spatially unavailable nutrients to the plant (Harley and Smith 1983). Points of contact between intra- and extra-radical hyphal systems occur at a frequency of 1.0 mm-' colonized root length (Fitter 1991). Grazing of hyphae close to the points of connection between internal and external hyphae would be expected to severely impede nutrient transfer to the plant (Fitter and Sanders 1992). In the last section of this review, investigations into the effects of grazing on the effectiveness of mycorrhizal associations will be summarized. Recent studies that have investigated the form and distribution of extraradical mycorrhizal hyphae and the grazing of microarthropods on different size categories of hyphae will be evaluated.

The flow of nutrients in the grazing pathway

Biomass and nutrient content The soil fauna account for 15% of the soil biomass C in forest systems (Reichle 1977). Equivalent values ranged seasonally from 0.4 to 22.5% of biomass C in winter rye (Secale cereale L.) litter (Beare et al. 1992). The remainder of the biomass is composed of the fungi and bacteria. To assess the role of grazing of soil fungivores in ecosystems we need to know what part of the faunal biomass is fungivorous and what part of the microbe biomass is fungal. It is also

Fig. 1. Proportions of fauna biomass in the fungivore, bacterivore, and other (carnivore, herbivore, and saprovore) trophic categories, in soils of pine forest and shortgrass prairie, and in winter rye litter bags buried in conventional tillage (CT) and placed on the surface of no-till (NT) agricultural systems (after Persson et al. 1980; Hunt et al. 1987; Beare et al. 1992).

Pine Forest Prairie

Winter Rye CT 6 July Winter Rye NT 6 July Winter Rye NT 28 Sep*

important to consider the turnover of these groups. Oribatid mites typically live for 1 or 2 years (Norton 1985). Calcula- tions based on published listings reveal that fungivores comprise between 21 and 76% of the fauna biomass in both natural and managed ecosystems (Fig. I).

With direct observation of fungi it is often difficult to tell apart empty fungal walls from viable sections with cytoplasm. Staining based on activity does not necessarily pick out the viable cytoplasm because various activity stains give different results with the same material (Hamel et al. 1990). Fluorescein diacetate (FDA) typically stains between 1 and 10% of total hyphal length from field samples (Persson et al. 1980; Ingham et al. 1986a) but stains more of the hyphae in pot studies (Hamel et al. 1990), suggesting dead hyphae accumulate in field systems. Of the 2500 kg dry mass fungi - ha-' in an oak (Quercus) woodland, 400 kg. ha-I or 16% was living (Frankland 1982). Using total hyphal lengths Paustian et al. (1990) found the ratio of biomass of fungi to bacteria (FIB) was between 1.8 and 2.6 among four cropping systems. Hunt et al. (1987) assumed that 10% of the total fungal length was viable and part of the biomass, and calculated an FIB ratio of 0.1 for Bouteloua gracilis (Humb., Bonpl. & Kunth) Lag. ex Steudel shortgrass prairie. Using a conversion factor to accommodate both viable and empty hyphae, Ingham et al. (1989) calculated FIB ratios of 0.8, 0.1, and 8 for shortgrass prairie, Agropyron smithii Rydb. mountain meadow, and lodgepole pine (Pinus contorta Loud.) forest, respectively. Measurement of C02 evolution after glucose addition in the presence or absence of streptomycin gave an FIB ratio of 14 for a soil-fungivore dominated hem- lock (Tsuga canadensis (L.) Carr.) stand compared with 2.7 for a soil-bacterivore dominated red pine (Pinus resinosa Ait.) system (Blair et al. 1994). Using respiration measurements Bewley and Parkinson (1985) estimated that for an aspen (Populus) woodland 80% of the litter microbial biomass was fungi. Rates of turnover have been estimated as 7.7 yearpi for fungi and 0.9 year-' for bacteria (McGill et al. 1981).

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Transfer of nutrients from fungus to fungivore and their release

Fungivores consume a mass of food equivalent to 5 % (Kowal and Crossley 1971) or 7 % (McBrayer and Reichle 1971) of their own dry body mass. day-I. For an aspen woodland soil dominated by oribatid mites the mass of fungi passing through the sum of all oribatid guts was 6 g . mP2 . year-' compared with a fungal standing crop estimated separately as 220 and 280 g . mP2 (Mitchell and Parkinson 1976).

The proportion of N in the fungal biomass for which there is a net movement into the fungivore biomass can be estimated as follows: 0.07 g N . mP2 in fungivores as a proportion of 3.2 g N . mP2 in saprotrophic fungi plus 1.3 g N . m-2 in mycorrhizal fungi (Persson 1983) gives 1.6% for a scots pine (Pinus sylvestris L.) system; 0.043 g N . m-2 in fungivores as a proportion of 0.63 g N . m-2 in saprophytic fungi plus 0.07 g N . mP2 in mycorrhizal fungi (Hunt et al. 1987) gives 6.1 % for shortgrass prairie.

Soil fauna contribute to the pool of nutrients in soil by excretion (Anderson et al. 198 1). The shedding of body parts and death yield substrates for decomposition. The carbon to nitrogen (CIN) ratios of bacteria and fungi are of the order of 5 and 15, respectively (McGill et al. 1973). For nematodes the CIN ratio is between 7.5 and 12 (Anderson et al. 1981) and for Collembola and oribatid mites the CIN ratios are 3.8 and 4.8, respectively (Teuben and Verhoef 1992). Anderson et al. (1981) argue that because the CIN ratios of the fungi and bacteria are similar to those of their grazers and because those grazers have a demand for respiratory C, then as the microflora is consumed, so N is mineralized. The efficiency of biomass production relative to respiration will affect this process.

Studies on mineralization Microcosm experiments Mineralization of N was studied in microcosms using the chitinolytic fungus Fusarium oxysporum Schlect. together with the fungivorous nematode Aphelenchus avenae Bastian (Trofymow and Coleman 1982; Ingham et al. 19856). Fusarium was able to mineralize 20 pg N . g-I dry soil as ammonium (NH,) N from added chitin in 100 days; with Aphelenchus present this increased by an additional 6 pg N . g-I (Trofymow and Coleman 1982). Growth of Bou- teloua gracilis shoots was promoted by Fusarium by a factor of three, while at the same time soil NH4-N concentration was increased from 33 to 49 pg N . g-' by the fungus (Ingham et al. 19856). Addition of Aphelenchus did not change shoot growth or soil N levels, although the nematodes proliferated well in the microcosms. Thus, Aphelenchus has only a small impact on the contribution of Fusarium to nutrient cycling. It seems that Fusarium alone mineralizes a considerable amount of N from chitin. These studies do not necessarily mean that other fungi would behave similarly or that Aphelenchus would be equally ineffective at liberating N when grazing other fungi.

NH4-N was mineralized at the same time as a Collembola- induced reduction in fungal standing crop (Ineson et al. 1982). Folsomia caizdida Willem. populations rose from 20 to 300 animals per microcosm over 8 weeks, at which level they remained for a further 2 weeks. During the period of lower Collembola densities, fungal standing crop was

Table 1. Total elemental concentrations (pmol . g-') of P, N, and C, as well as extractable concentrations of inorganic P (Pi), nitrate, and ammonium, in a food consisting of a mixture of various fungi and algae from tree bark and tree branch surfaces and in the resulting faeces produced by the Collembolan Tomocerus minor (after Teuben and Verhoef 1992).

1.0 M KC1 Total extractable

Element Food Faeces Ion Food Faeces

increased from 2 to 32 mg . g-' litter by the Collembola. Stimulation of NH4-N mineralization by the Collembola occurred during the 6- to 12-week phase, during which time fungal standing crop fell to 8 mg . g-I with Collembola present, yet remained at 20 mg . g-I in their absence. By the end of the experiment the amount of NH4-N released had doubled in response to Collembola from a rate of 6 to 13 pg N leached. week-'. In similar experiments (Ander- son et al. 1983) the Collembola Tomocerus minor Lubbock and Orchesella villosa Geoffroy were both able to increase NH4-N release from forest litter from 3 to 10 pg N . g-' over a 6-week period.

Although Collembola are capable of promoting N release from fungus - leaf litter microcosms, as with other mineralization processes the nutrients liberated can be quickly immobilized by more microbial growth, if other factors are not limiting. Such immobilization was shown for grazing of Onychiurus subtenuis Folsom on isolate sterile dark 298 (Visser et al. 1981). Similarly, grazing of Onychiurus procampatus Gisin at densities in excess of field levels on Phoma exigua Desm. reduced both fungal biomass and respiration, yet release of NH4-N, NO3-N, and H2P04- did not occur (Bardgett et al. 1993).

Several studies (reviewed by McGonigle 1996) have demonstrated changes in the respiration rates of the fungi and changes in fungal community structure in response to grazing. Grazing has been shown to promote higher respiration of the fungal biomass that is not eaten, presumably by removal of inhibitory or senescent portions of the mycelium. Alternatively, other fungi or bacteria can take advantage of any reduction in vigour of a grazed fungus and invade. For the most part the significance of changes in fungal community structure with regards to nutrient cycling in the field is unknown.

Passage through the gut of Collembola reduced total P and total N in a food of mixed fungal and algal tissue in greater proportion than the loss of total C (Table I). Teuben and Verhoef (1992) found that nitrifying bacteria had been active either in the gut or within hours of the deposition of faeces, because of the manyfold increase in NO3- and loss of NH4+ (Table 1). Based on these measurements (Table 1) and on an annual consumption rate of 6 % of litter fall, the potential stimulation of NO3- in litter was calculated as 0.06 x (75.811.8) = 2.5, i.e., a 2.5-fold increase in NO3- concentration in litter as a whole a result of the passage of 6 % of

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Fig. 2. Estimates of rates of mineralization of inorganic nitrogen by fungi and fungivores in relation to that by other fauna and by bacteria. Release of N from fungivores and other fauna is by excretion (after Persson 1983; Hunt et al. 1987).

1 Net mineralization 1 g N.in-',year-'

PRAIRIE '

\/ Bacteria

the litter through Collembola guts (Teuben and Verhoef 1992).

Studies in ecosystems As a proportion of total mineralization of N, the contribution of the fauna has been estimated as 38% (Hunt et al. 1987), 16-27% depending on cropping system (Paustian et al. 1990), and 10 -49% depending on assumptions made about assimilation efficiency (Persson 1983). However, as described earlier only a portion of the soil fauna is fungivorous (Fig. 1). When the fungivores are considered separately, the quantity of N mineralized is seen to be lower than for the soil fauna as a whole (Fig. 2). For the scots pine forest 13% or about one eighth of total mineralization of inorganic N is due to excretion by fungivores. This was the highest of three estimates based on different efficiencies of assimilation of N by the soil animals (Persson 1983). The corresponding value for the fungivores in shortgrass prairie is only 1.4% of total N mineralized (Fig. 2).

Ingham et al. (1986b) reduced the density of total fungi by applying fungicide to shortgrass prairie; densities of fungivorous nematodes were decreased by application of carbofuran and dimethoate, but microarthropods were unaffected. Soil NH4-N and NO3-N pool sizes were not changed in response to the reductions in fungal density and reductions in nematode biomass (Ingham et al. 1986b). In contrast, Ingham et al. (1989) were able to reduce soil microarthropod densities using a mixture of carbofuran and dimethoate at the same shortgrass prairie site, as well as in a mountain meadow and at a lodgepole pine site. At the forest site the reduction in numbers of microarthropods was associated with a reduction in FDA-staining hyphae from 400 to 250 m . g-I, and an increase in soil NH4-N from 11 to 16 pg N . g-l. However. at the meadow and ~rair ie sites the reductions in numbers of microarthropods were associated with small increases in the densities of hyphae; at the same time the combined soil NH4-N and NO3-N levels increased from 16 to 23 pg N . g-l, and from 10 to 33 pg N . g-I at the meadow and prairie sites, respectively. These results were

interpreted (Ingham et al. 1989) as follows: fungal production is normally stimulated by grazing of microarthropods in the forest system, with the fungi behaving as net immob- ilizers of N. Thus, killing the microarthropods reduced fungal standing crop and released N. In the meadow and prairie sites microarthropods instead act to lightly suppress fungal populations, with the fungi acting as net mineralizers of N. Thus, elimination of microarthropods allowed a small increase in fungal production, and in turn N was released (Ingham et al. 1989).

Microarthropod grazing caused the loss of 1.1 g N . m-2 from winter rye litter bags on the surface of no-till (NT) plots (Beare et al. 1992). Naphthaline decreased microarthropod densities from a maximum in controls of 175 animals . ggl ash-free dry mass (AFDM) to levels that remained below 25 g-I AFDM throughout the growing season. The reduction in microarthropod density was associated with an increase in total hyphae from 1235 to 2040 m - g-I. There was a greater retention of N in the naphthaline-treated litter: 100% of original N remained in naphthaline-treated bags in August compared with only 75 % in control bags (Beare et al. 1992). Microarthropod numbers were reduced from a maximum of 750 g-' AFDM to a maximum of 450 g-I AFDM in naphthaline-treated bags buried in soils given conventional tillage (CT) management, but the density of total hyphae was stable at about 4500 m . ggl. For the CT plots the percen- tage of N remaining in the litter bags was not affected by biocide treatment.

From the above outline it is evident that studies that have used applications of biocides to field systems have had inconsistent outcomes. The direct effects of the biocides are some- times but not always realized, for example the action of carbofuran and dimethoate to reduce microarthropod numbers in shortgrass prairie was effective in the study of Ingham et al. (1989), but not in that of Ingham et al. (1986b). In addition, where the primary targets of the biocides have been decreased as intended, inconsistencies arise in the responses of the processes or groups that are expected to be secondarily affected. For example, the reduction of microarthropods in NT plots seemingly increased fungal production to 165% of the control level, whereas reduced numbers of microarthropods in CT plots had no effect on the fungi (Beare et al. 1992). Further, N was found to be mineralized following both increases or decreases in fungal biomass, depending on the ecosystem (Ingham et al. 1989). This variety of responses serves to underline the complexity of fauna - microbe - nutrient interactions in field systems. Such studies generate hypotheses that subsequently need to be evaluated. It appears that the fungal community may function either to immobilize or mineralize N and it seems that microarthropods may act to maintain the fungal biomass at a higher or lower level than that at which it would be in their absence.

Grazing and the effectiveness of mycorrhizal nutrient uptake

Reviews of the effects of grazing of AM fungi was presented by Fitter and Sanders (1992) and Ingham (1992). Based on spore abundance and on the allocation of photosynthate to mycorrhizal structures, Fitter and Sanders (1992) argued that

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AM fungi comprise much of the biomass of fungi in soil. Other approaches also support this view. For a selection of herbaceous species the total length of AM fungal hyphae per cm root length ranged from 1.2 to 14.2 m hyphae . cm- (Smith and Gianinazzi-Pearson 1988). Assuming a root length density in soil of 5 cm . ~ m - ~ and a soil bulk density of 1.15 g . ~ m - ~ , these values correspond to a range from 5 to 62 m . g-I. If these length densities are representative, then AM fungal hyphae must indeed form a significant part of the hyphae in field systems. Ingham et al. (1986~) found the density of total hyphae in the top 5 cm of shortgrass prairie increased linearly from 30 to 110 m g-I between April and August. Quantitative studies of the impact of grazing on the mutualistic effectiveness of AM fungi have manipulated densities of grazers in pot cultures of the fungi. In all of these studies growth of mycorrhizal plants in the absence of fauna exceeded that of nonmycorrhizal controls.

Salawu and Estey (1979) reduced the shoot and root growth of mycorrhizal soybean by 60% relative to controls by the addition of 32 x lo3 Aphelenchus avenae nematodes to each of several 15-cm pots of topsoil. Assuming a pot volume of 2000 mL and a bulk density of 1 .O, this converts to 16 nematodes . g-I dry soil, which is close to published field densities (Ingham et al. 1985~) . Hussey and Roncadori (1981) found that 40 x lo3 Aphelenchus avenae added. pot-' suppressed growth of cotton (Gossypium hirsutum L.) mycorrhizal with an isolate of Gigaspora; however, for plants colonized with a Glomus isolate, growth was retarded by 10 x lo3, but unaffected by 40 x lo3 or 80 x lo3 nematodes . pot- I.

A range of initial Onychiurus sp. densities up to 100 L-I were stimulatory to P absorption and growth of (Allium porrum L.) in pots, whereas 200 L-I was inhibitory (Finlay 1985). The inhibitory effect of final Collernbola densities above 100 L-' were also seen in a variety of experiments with Onychiurus and Folsomia added to pots of red clover (Trifolium pratense L.) colonized by a selection of AM fungi; when Collembola were present the growth of colonized plants was not significantly different from that of noninocu- lated plants (Finlay 1985). These data are broadly consistent with other studies (Warnock et al. 1982; Harris and Boerner 1990). Folsomia candida achieved a final density of approximately 700 L-' in pots of mycorrhizal leeks, and in response the growth of plants was half of that seen in the absence of Collembola, with P inflows being reduced by the activity of the animals from 68 to 17 fmol . cm-I . s-I (Warnock et al. 1982). A density of 15 E;: candida . L-I promoted the growth of Geranium robertianum L. grown in potting mix relative to pots without Collembola or relative to pots with up to 70 Collernbola , L-I (Harris and Boerner 1990). A clear exception to these studies was that of Kaiser and Lussenhop (1991) who found no changes in the growth of mycorrhizal soybean, relative to controls without Collem- bola, when F candida was present at densities of 8.2 animals . g-I in a 1 : 1: 1 soil-peat-perlite potting mix. Assuming a bulk density as low as 0.5 for this potting mix, 8.2 animals . g-I would correspond to densities in excess of 4000 L-I.

Finlay (1985) reduced the density of Collembola by 80% to 1000 animals . m-2 by applying the insecticide chlorfenvinphos to a fumigated field plot that had been recolonized

Fig. 3. Production of faeces as an index of feeding activity by microarthropods in regions with arbuscular mycorrhizal hyphae > 10 and < 5 pm in diameter. The microarthropods tested were the Collembola Tullbergia clavata Mills, Folsomia penicula Bagnall, and Folsomia candida, and the oribatid mites Nothrus anauniensis Can. & Franz., Ceratozetes gracilis Michael, and Lasiobelba rigida Ewing. Asterisks indicate significant differences between pairs of means (after Klironomos 1994).

Tullbergia

F. penicula *

Nothrus I* Ceratozetes

Lasiobelba

Mean faecal count

by Collembola, inoculated with AM fungi, and sown with red clover. Shoot growth and P absorption were stimulated by insecticide application (Finlay 1985). Reduction of Collembola from 5700 to 2000 m-2 by applying chlorfenvinphos to a meadow more than doubled the growth of Holcus lanatus L. and increased P inflows from 4 to 14 fmol P . cm-I . s-I (McGonigle and Fitter 1988). The interpreta- tion made in each of these studies was that plant P absorption and growth were improved by reduction of grazing by Collembola on the extraradical AM mycelium. These experiments can be criticized (Rabatin and Stinner 1991) on the grounds that the chlorfenvinphos could have had effects on nontarget organisms.

Recent advances have been made (Friese and Allen 1991 ; Jakobsen et al. 1992) in understanding the structure and distribution of the extraradical mycelium of AM fungi. Jakob- sen et al. (1992) monitored the density of hyphae produced in sterile soil by AM fungi at increasing distances away from a 25-pm mesh, behind which roots had been inoculated. Hyphal densities in soil gradually decreased, depending on AM fungal isolate, from between 6 and 27 m . g-I at the mesh to trace levels at a distance of 10 cm (Jakobsen et al. 1992). Friese and Allen (1991) qualitatively described different phases of AM fungal external mycelium: spore and root infection networks that colonize roots from spores and senescent root fragments, runner hyphae that spread from active areas of colonization to infect other parts of the same root or other roots, and absorptive hyphal networks that grow out from roots in a branched manner reminiscent of root growth. Friese and Allen (1991) provided excellent photographs of spore and root infection networks, but they gave only a schematic drawing of the absorptive hyphal networks. Hyphal diameters within absorptive hyphal networks were reported to decrease linearly from 10 to 2 pm through net- work branching orders of 1 -5 (Friese and Allen 1991). Klironomos (1994) physically separated external hyphae of AM fungi into diameter classes > 10 and > 5 pm. Four out of six microarthropod species gave significantly higher

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faecal counts on the regions with the smaller diameter hyphae (Fig. 3). Where soil fauna feed preferentially on finer rather than coarser AM fungal hyphae, effects of grazing on symbiotic effectiveness of the mycorrhizal association would be expected to be minimized.

Conclusions

The soil fauna as a whole has been estimated as contributing 16-49% of total net mineralization of N in soils through excretion. The contribution of fungivores is approximately one eighth of total net mineralization or less. This is because only a fraction of the soil fauna, 21 -76% of faunal biomass, is fungivorous.

Fungivores have indirect effects on mineralization processes by promoting comminution, mixing, and inoculum dispersal, which stimulate microbe activity. Fungivore grazing can stimulate fungal production, which in turn may give a net immobilization or mineralization of nutrients depending on the fungi involved. Grazing may promote the replacement of some fungi with others, but the extent to which this plays a role in nutrient cycling in field systems is difficult to ascer- tain. Experimental biocide applications to field systems have been inconsistent in their outcomes and serve primarily to generate hypotheses.

The stimulation of nitrification in laboratory feed of fungal and algal tissue by its passage through Collembola guts could increase nitrate concentration on an ecosystem

I level by a factor of 2.5 if the same occurs with the diet of Collembola in forest litter. Confirmation of this is necessary for foods more typical of such environments.

The effectiveness of mycorrhizal fungi should suffer only minor interference from fungivore grazing if recent informa- tion on their preference for finer hyphae is representative. Pot studies on grazing of AM fungi by Collembola have shown that densities below 100 L-I soil are stimulatory to plant growth, while higher densities generally depress the P absorption by mycorrhizal plants. Important questions to be answered are to what extent growth depressions caused by high Collembola densities in pot studies are due to a paucity of nonmycorrhizal fungi for the Collembola to feed on, and the lack of predatory animals in such systems. Unless the preference of microarthropods for finer hyphae seen under controlled conditions does not reflect the situation in the field, one must conclude that pot studies on grazing of AM fungi have to some extent given a misleading view of the role of grazing in nature.

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the significance of grazing on fungi in nutrient cycling

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