Grazing by collembola affects the outcome of interspecific

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

Timothy D. ROTHERAY, Matthew CHANCELLOR, T. Hefin JONES, Lynne BODDY*

Cardiff School of Biosciences, Cardiff University, Cardiff, CF10 3AX, United Kingdom

a r t i c l e i n f o

Article history:

Received 16 June 2009

Revision received 28 July 2010

Accepted 15 September 2010

Available online -

Corresponding editor: Gareth Griffith

Keywords:

Accelerated mycelial extension

Interspecific variation

Mycelial morphology

a b s t r a c t

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 bicolorwhen 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). Addi-

tionally, 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.

ª 2010 Elsevier Ltd and The British Mycological Society. All rights reserved.

Introduction

As many species of saprotrophic cord-forming fungi occupysimilar spatial niches at the soilelitter interface, interactionsare inevitable (Boddy 2000). Interspecific fungal interactionsare highly aggressive and generally occur following gross

mycelial contact (Boddy 2000). Interactions result in eitherdeadlockor someformof replacement (i.e. partial, complete,ormutual); these outcomes are variable and can be substantiallyaffectedbybothbiotic andabiotic variables (Chapela et al. 1988;Woods et al. 2005). Intraspecific genetic variability may also be

* Corresponding author.E-mail address: [email protected] (L. Boddy).

ava i lab le at www.sc ienced i rec t . com

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Please cite this article in press as: Rotheray TD, et al., Grazing by collembola affects the outcome of interspecific mycelialinteractions of cord-forming basidiomycetes, Fungal Ecology (2010), doi:10.1016/j.funeco.2010.09.001

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important in determining fungal interaction progression andeventual outcome, although most studies investigating inter-actions of higher fungi have tended to concentrate on a singlestrain of each species. A few studies with Trichoderma species(Ascomycota) interacting with wood-decay fungi haveinvolved multiple strains (see Philp et al. 1995; Wheatley et al.1997) but most of these have focussed on strains of medicalor biocontrol value (Walker et al. 1995; Vainio et al. 2001).Despite possible implications for both species abundance anddiversity, the role played by fungal genetic variability in fungalfitness remains unknown.

As well as encountering other fungi, non-unit-resource-restricted fungi (sensu Cooke & Rayner 1984) growing out fromresources are also more accessible to grazers. Various soilinvertebrate taxa, including Nematoda, Collembola and Oli-gochaeta, are known to graze on fungal mycelia and cansubstantially alter fungal morphology and physiology (Ruesset al. 2000; Harold et al. 2005; Tordoff et al. 2006; Boddy &Jones 2008). Such effects are likely to alter fungal fitness and,therefore, their combativeness in interactions with other soilmicroorganisms, including fungi.

The visible changes in morphology and physiology duringfungal interactions are associated with biochemical changes,such as increased enzymatic activity and production of diffus-ible (DOC) and volatile (VOC) organic compounds (Griffith et al.1994; Baldrian 2004; Hynes et al. 2007; Evans et al. 2008). Thisenhanced activity may also lead to lysis of hyphal compart-ments and nutrient leakage into the surrounding environment(Wells & Boddy 2002). Numerous plant species use chemicalsemitted as a result of insecteherbivore action to attract para-sitoids to the vicinity (Dicke 1994; Tentelier & Fauvergue 2007),and a comparable process may occur with fungi. Mycophagousgrazersmay use chemical cues arising from interaction activityto locate highquality resource patcheswhile fungimay activelyrecruit grazers to provide a competitive advantage over anopponent. Orientation to fungal odours by invertebrates hasbeenwell documented (Swift & Boddy 1984; Hedlund et al. 1995;Guevara etal.2000)andanecdotalevidenceexistsofattractionoffungus gnats to fungal interaction zones (Boddy et al. 1983).

This study aims to: (i) elucidate the effects of invertebrategrazing on the morphology and competitive abilities of sap-rotrophic cord-forming basidiomycetes when interactinginterspecifically; (ii) determine whether physiological andchemical changes in the mycelium, such as pigment produc-tion, may affect invertebrate behaviour (e.g. with preferentialinvertebrate grazing at interaction zone); (iii) determinewhether different fungal strains of the same species affectfungal combativeness and invertebrate grazing. One set ofexperiments was performed in agar culture, and another setin trays of soil. Though soil trays are more realistic, agarculture allows many more combinations to be performed.

Materials and methods

Collembola culturing

Folsomia candida and P. armatawere cultured in 0.6 l plastic tubswith pierced lids for aeration. Each tub contained 9:1 plaster ofParis (Minerva Dental Ltd., Cardiff, UK): activated charcoal

(Sigma, UK). Collembolawere providedwith dried baker’s yeast(Saccharomyces cerevisiae, Spice of Life Ltd., Cardiff, UK) weekly.Tub moisture wasmaintained with deionised water (DI).

Experimental F. candida were selected using a stackedsieving system with sieves of known pore size, the largersieves being uppermost (Nickel-Electro Ltd., Weston-super-Mare, UK). Collembola were added to the top sieve andallowed to self-sort by moving through the sieves for 5 min.Those of body diameter 250e400 mm were placed in freshculture pots and left without food for 24 hr to evacuate any gutcontents. These were then removed to experimental platesusing an electric “pooter”.

Fungal isolates

H. fasciculare (four fruit bodies isolates, from disparate loca-tions; agar medium experiment only; Supplementary Table 1),Phallus impudicus (isolated from a cord), P. velutina (isolatedfromwood) and Resinicium bicolor (two wood isolates (1, 2) agarexperiment only) were cultured on 2 % malt extract agarmedium (MEA, 20 g l"1 malt, Munton and Fison, UK; Lab Magar no. 2) and maintained in the dark at 20 #C. H. fasciculare,P. impudicus and P. velutina were from the Cardiff UniversityCulture Collection and the R. bicolor isolate from SteveWoodward, Aberdeen University. The first three species areextremely common in temperate deciduous woodland;R. bicolor is common in coniferous woodland though infre-quent in deciduous woodland. These species were selected forstudy because they cover a broad spectrum of foragingpatterns (Boddy 1999), and their interaction outcomes (Boddy2000) and effect of collembola grazing when growing alone(Boddy & Jones 2008) have been well characterised.

Interactions in agar culture

Fungiwerepairedopposite to eachother inall of the36possiblecombinations. Inoculation was timed to ensure that when thetwo mycelia met each individual had colonised an equivalentareaofagarmedium.Three, 5 mminoculumplugswerespacedequidistantly along a chord 2 cm from the edge of 2 % MEAplates (9 cmdia). Plateswere incubated at 20 #C in the dark andmaintained in cardboard boxeswithin black polythene bags toreducewater loss.Twentycollembolawereaddedat twopointsat theedgeof thePetridish, 10oneachmycelium, toeachoffivereplicates per combination when the interacting fungi inaminimumof50 %of the replicateshadmadecontact for 2 dormore. Twenty collembola are a realistic field density (Petersen& Luxton 1982) and have effects on fungal morphology andactivity when growing alone (Boddy & Jones 2008).

Agar plate interactions were photographed with a NikonªCoolpix! 5700 digital cameramounted on aKaiser RA1 camerastand (Kaiser,Germany) set at aheight of 36.7 cm. Photographystarted on thedayof collembola addition (t0) and thenevery 2 duntil 14 d (ty), followed by every 4 d until 26 d (tx).

Determination of outcome of interactions in agar culture

Outcome of interaction was classed as: (1) deadlock, whereneither fungus gained territory of the other; (2) partialreplacement, where one fungus extended at least 5 cm into

2 T. D. Rotheray et al.


the territory of the opponent but did not reach the oppositeside of the plate; (3) mutual replacement, as (2) but bothopponents extended into the territory of the other; or (4)replacement, where the mycelium of one fungus wascompletely killed by the other and the former’s territorycompletely colonised.

In agar, outcomes were determined by visual inspectionand confirmed by reisolation from the underside of the agaronto 2 % MEA. Relative combative ability of different H. fas-ciculare strains was compared by employing a scoring system,following Crockatt et al. (2008). Each replicate was scored as: 2,total replacement of opponent; 1, partial replacement ofopponent; 0, deadlock; "1, partial replacement by opponent;"2, total replacement by opponent. A cumulative score wasattributed to each strain providing a combative index. A strainshowing total replacement in all five replicates scored 10,while a species totally replaced in all replicates scored "10.

Soil tray preparation

Soil (pH 4.5) collected from the top 5e10 cm mixed deciduouswoodland in (SO517069) was air-dried for 7 d, and sievedthrough 4 mm then 2 mm mesh to remove large organicmaterial and stones. The soil was then frozen for 24 hr toprevent population explosions of resident soil fauna (butminimising effects on microbial community) before rewettingwith DI to attain a soil matric potential of ca. "0.012 MPa. Thewet soil (200 g/tray) was evenly compacted to 4 mmdepth into24! 24! 2 cmnon-vented lidded bioassay trays (NunceGibco,Paisley, UK), whichwere thenweighed to$0.01 g and stored instacks of 20, double-wrapped in black PVC bags to preventdesiccation (20 #C$ 1 #C, dark). Trays were used within 7 d ofbeingmade, and rewetted to original weight with DI every 7 d.During the experiment any contaminating flora wereremoved. No non-experimental fauna were observed.

Preparation of wood inoculum

Wood blocks were cut from freshly-felled beech (Fagus syl-vatica) timber (Coed Cymru Hardwood Sawmill, Wentwood,UK) into 2! 2! 1 cm blocks. Blocks with discolouration andknots were discarded. Groups of 20 blocks were double-wrapped in heat-sealed biohazard bags and autoclaved fortwo separate 1 hr sessions each being 24 hr apart. Sterile woodblocks were added to cultures of one isolate each of H. fas-ciculare, P. impudicus, P. velutina and R. bicolor, on 2 % MEA andincubated in the dark at 20 #C for 3 months.

Inoculation of soil trays

All four fungal species were interacted in every possibleinterspecific combination, with 20 soil trays/interaction (total120 soil trays). Mycelium and agar were scraped off each woodblock inoculumbefore addition to soil trays, to prevent growthof soil microbes on the agar medium. To each tray a woodblock of the slower growing of the two fungal species wasadded 9 cm away from a corner along a diagonal betweencorners. A wood block colonised by an opponent was added,9 cm away from the opposite corner, timed such that the fungimet when the mycelia were approximately 8 cmdia. Trays

were weighed and deionised water was added weekly tomaintain that weight.

To half of the trays, collembola were added. For any giveninteraction, when 50 % or more of the fungi had met theopposing fungus, for a minimum of 2 d, 20 F. candida wereadded to each corner of the tray (80/tray). P. armata (80/tray)was used in two additional interactions; R. bicolor againstH. fasciculare and P. impudicus against H. fasciculare. Method-ology for culture and addition of P. armatawas the same as forF. candida.

Images of soil trays were captured as for agar plates butwith the camera at a height of 47 cm and artificial illuminationprovided by two 1 000W spot flood lamps (Gamma 7 Al,Gamma, Chicago USA), each set 60 cm either side of the standand 120 cm above it. Photography commenced on the day ofcollembola addition, t0, and continued every 2 d for the first11 d (t10), then every 4 d until 23 d (t22), every 10 d until 43 d (t42)and finally at 85 d (t84). Outcome of interactions was deter-mined t84 after collembola addition (see below).

Determination of outcome of interactions in soil microcosms

Extension rates of one mycelium growing over another weredetermined by linear regression analysis of extent by timefrom digital images. Mycelial extent was measured as thefurthest visible extent of mycelium along four zones at equalangles through a 90# segment of the mycelium (Fig 1). Unlessremoved through grazing the mycelium at the two centralmeasurements (30# and 60#) was invariably in contact with theopposing mycelium. Cords severed by grazing and not visibly

Fig 1 e Measurement of mycelial radial extent in soilmicrocosms. The direction in which the fourmeasurements(indicated with white single arrows) were taken at t0 andtreach. Measurements were made on both species in everyinteraction.The lengthof thedouble-headedarrow (22.6 cm-internal tray width) was applied to scale all images.

Grazing by collembola affects the outcome of mycelial interactions 3


connected to the wood block were not included inmeasurements.

At the end of the experiment wood blocks that had beenreached by the mycelium of the opposing fungus were har-vested. These blocks were cut in half, three wood chips takenfrom the freshly cut surface, and plated onto MEA and incu-bated for 7 d at 20 #C, in the dark. If only the opposing specieswas re-isolated, the outcome was recorded as total replace-ment. If both fungal species were isolated the result wasrecorded as partial replacement. If only mycelium of theoriginal inoculum was isolated the outcome was recorded asovergrowth by the opponent but not replacement. Results foreach interaction were recorded as overgrowth, partialreplacement or replacement, and expressed as a percentage oftotal reisolations. Where mycelium of one strain overgrewthat of the opponent but did not reach the wood block, theoutcome was reported as partial overgrowth.

Statistical analysis

Statistical comparisons made between mean extension rateswere as follows: (1) the difference in mycelial extent betweengrazed and ungrazed trays across all four measurements atthe final time point (treach; the time when a mycelium reachedthe edge of the tray, which depended on species); (2) thedifference in mycelial extent between grazed and ungrazedtrays when growing toward (or over) the opponent mycelium(30# and 60# measurement) at the final time point (treach); (3)the difference in mycelial extent over time between grazedand ungrazed trays when growing toward (or over) the oppo-nent mycelium; (4) the difference in mycelial extension overtime between grazed and ungrazed trays when growing oversoil (0# and 90#); (5) the difference in mycelial extension overtime when growing over soil compared to when growing overthe opponent mycelium in grazed trays; and (6) the differencein mycelial extension over time when growing over soilcompared to when growing over the opponent mycelium inungrazed trays. This complete analysis was not alwaysappropriate and a framework was developed to determine thesuitable level of analysis for each species in each interaction(Fig 2).

Results

Outcome of interactions in agar culture

H. fasciculare: It was combative, several strains replacing R.bicolor, and being replaced only occasionally by P. velutina andR. bicolor 1. H. fasciculare 4 was, however, sometimes replacedby R. bicolor and P. velutina though not P. impudicus. There weremarked differences between different strains of the samespecies. H. fasciculare 3, for example, replaced R. bicolor 1whereas H. fasciculare 4 did not (Table 1). H. fasciculare 1 wasthe most combative of the four isolates, and H. fasciculare 4was the weakest (Tables 1 and 2). Grazing increased combat-iveness in two isolates (H. fasciculare 2 and H. fasciculare 3) andreduced it in the others (Table 2). H. fasciculare grew as densemycelium from the inoculum and overgrew opponents withthe formation of cords (Supplementary Table 2), occasionally

emerging through the interaction zone from several discretepoints (Fig 3A). H. fasciculare 4 often produced non-linear,apparently disordered, cords when overgrowing other species(Fig 3I). All H. fasciculare isolates produced yellow pigmentalthough H. fasciculare 1 produced pigmentation (Fig 3A and B)only when overgrowing another species. All new growth of H.fasciculare isolates was white, with the exception of the cordsof H. fasciculare 4 when interacting with P. impudicus, whichdeveloped a yellow colour (Fig 3I).

P. impudicus: Although it was overgrown to varying degreesby H. fasciculare 1, 2 and 3, P. impudicuswas strongly combativepartially replacing, mutually replacing or deadlocking with allother species and strains (Table 1). In the presence of otherspecies, the morphology of P. impudicus changed beforecontact occurred - dense cords originated from up to 1 cmbehind the growing front (Fig 3K; Supplementary Table 2). Thismorphological response also occurred in self-pairings; whenP. impudicuswas substantially overgrown it occasionally brokethrough the opposing mycelium at the interaction zone,producing fast growing plumes (Fig 3G).

P. impudicusmycelia darkened in some interactions but didnot produce strong pigmentation (Supplementary Table 2).During interactions with R. bicolor, a zone of lysis wasproduced in the interaction zone as P. impudicus replacedR. bicolor (Supplementary Table 2; Fig 3K and O). Collembolaburrowed within the lytic zones (Fig 3N). Grazing slightlyincreased the overall combativeness of P. impudicus (Table 2).

P. velutina: It was less combative than H. fasciculare andP. impudicus though it occasionally replacedH. fasciculare 2 and 3(Table 1). When overgrowing another mycelium, P. velutinaformed finely branched cords often emerging from a narrowpointof the interactionzone (Fig3J). CombativenessofP.velutinaincreased slightlywhengrazed (Table 1), and rate of overgrowthincreased when grazed cords of P. velutina and P. impudicusovergrew each other (Supplementary Table 2). A dark pigmentpermeated the medium when P. velutina was overgrown andwhen interacting with itself (Supplementary Table 2).

R. bicolor was less combative than H. fasciculare andP. impudicus. R. bicolor 1 was more combative than R. bicolor 2.Combative ability of R. bicolor 1 was reduced when grazedwhereas that of R. bicolor 2 increased slightly (Table 1).Following contact with mycelium of an opposing species,R. bicolor 1 rapidly produced dense aerial hyphae up to about1 cm behind the interacting front (Fig 3L), but this was eitherless marked or absent in R. bicolor 2 (Supplementary Table 2).R. bicolor overgrew as dense, tightly packed, unbranched linearcords (e.g. Fig 3L). When interacting with H. fasciculare andP. velutina (Fig 3M), R. bicolor produced deep red pigment(Fig 3E, F and H), which was more pronounced in R. bicolor 1than in R. bicolor 2 (Fig 3E, F but see H).

Outcome of interactions between extra-resourcemycelia on soil

In ungrazed systems there was never evidence of one myce-lium replacing another on the surface of soil, but there wasoften overgrowth especially by P. velutina and P. impudicus(Table 3; Fig 4), to the extent that the wood block inoculum ofan opponent was sometimes reached and interactions thentook place within the wood (see below). In interactions



between R. bicolor and P. velutina, but not other combinations,cords of the latter grew to both sides of the R. bicolor woodblock forming a complete ring comprising a thick cord inungrazed systems (Fig 4A and B).

In some interactions fungi produced pigments and exudatesat the point of contactwith the opponent (Fig 4J andK). R. bicolorproduced a red pigment along the interaction line when inter-acting with H. fasciculare and small globules of exudate were

visiblewhereR.bicolorcordsmet thoseofP.velutina (Fig4J andK).There was evidence of preferential grazing by F. candida at theinteraction zone, for example with H. fasciculare when inter-acting with either P. velutina or P. impudicus (Fig 4F, G and I).

In grazed systems R. bicolor mycelia were alwayscompletely grazed away by F. candida (e.g. Fig 4D) whereasP. armata apparently had little impact (Fig 5E). P. velutina wassometimes heavily grazed, but not to extinction, especially in

(a)

(b)

(c)(d)

(f)

(g)

(i)

(j)

(h)

A comparison of the mycelial extent across all four measurem ents between grazed trays and ungrazed using a two-sample t-test (at T reach ).

A comparison of the mycelial extent across (or towards) the opponent (30º and 60º measurements Fig 1) between grazed and ungrazed trays using a two-sample t test (at T reach ).

The mycelial extent was measured at three equally spaced time points between t 0 and t reach .

Both the time points and replicates in which mycelium commenced overgrowing the opponent mycelium in the 0º and 90º measurements (Fig 1) were determined. The data were subsequently grouped into two sets (i) extension toward/over opponent mycelium and (ii) extension over soil sets. RM ANOVA was used to compare extension over opponent in grazed and ungrazed trays, and extension over soil in grazed and ungrazed trays.

Data examined to determine whet her overall extension measurement mean was negative (mycelium reducing over time) or positive (mycelium extending over time) at three equally spaced time points between t 0 and t reach .

Repeated Measures (RM) ANOVA co mparing the change in mycelial extent over time in grazed and ungrazed trays across all four measurements.

RM ANOVA was used to compare extension toward opponent in grazed and ungrazed trays using 30º and 60º measurements (Fig 1).

RM ANOVA comparing extension over opponent and over soil within both grazed and ungrazed trays.

Significant difference No significant difference

No further analysis

Mean negative extension Mean positive extension

The observation that fungal extension appeared to be different dependent on whether it was growing across (or toward) the opponent led to the subsequent test in all interactions.

Mycelia sometimes appeared to be extending at different rates over the opponent and over the soil within grazed and ungrazed treatments. To test this the following step was used.

Fig 2 e The framework applied to refine application of statistical tests in analysis of overall extension change during grazedandungrazed interactions.Wheredataviolatednormality aManneWhitneyU-test (insteadof the t-test) or a two-wayANOVAon ranked data (instead of the RM ANOVA) was used. When assumptions were violated a Scheirer Ray Hare test replacedtwo-way ANOVA.



Table 1 e Outcome of interactions 12 weeks after addition of Folsomia candida as grazing treatment

R. bicolor 2 R. bicolor 1 P. velutina P. impudicus H. fasciculare 4 H. fasciculare 3 H. fasciculare 2

Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed

Hf1 r 100 r 100 MR 80PR 20

MR 60PR 20pr 20

r 100 r 100 PR 100 PR 100 D 100 D 100 D 100 D 100 D 100 D 100

Hf2 pr 100 D 20pr 80

pr 100 pr 100 MR 75R 25

MR 75r 25

MR 100 MR 40PR 60

D 100 D 100 D 100 D 100

Hf3 pr 60D 40

pr 50D 50

r 11PR 89

r 22PR 78

MR 22r 33R 44

r 80R 20

D 100 PR 33D 67

D 100 D 100

Hf4 PR 100 PR 100 pr 10PR 40R 50

d 11MR 11PR 22R 56

MR 20D 80

R 100 D 100 D 100

Pi pr 100 pr 100 pr 100 pr 100 D 25PR 50pr 25

pr 100

Pv MR 80D 20

MR 80pr 20

pr 20r 80

MR 20pr 40r 40

Rb1 D 100 D 100

Outcomes weremutual replacement (MR), partial replacement (PR), total replacement (R) and deadlock (D). For outcomes designated PR and R, upper case signifies that replacement was by the funguslisted at the head of the column whereas lowercase signifies replacement by the fungus listed in the row. Numbers refer to percentage of replicates exhibiting a given response. There were 4e10replicates/interaction. Hf¼H. fasciculare, Pi¼ P. impudicus, Pv¼ P. velutina, Rb¼ R. bicolor.

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interactions with R. bicolor (Fig 5A). H. fasciculare was usuallyonly sparsely grazed, except when interacting with P. velutinawhere it was completely removed in grazed systems by 64 d(Fig 5G). In three (of six) interaction combinations, grazing byF. candida altered the extent of overgrowth by mycelia on thesoil surface (Table 3). For example, the mutual overgrowth ofP. velutina and R. bicolor in ungrazed systems shifted tocomplete overgrowth by P. velutina when grazed (Table 3; Fig5A and B). There was greater growth of P. impudicus over R.bicolor when grazed than ungrazed. Interactions involving H.fasciculare were little changed when grazed except wheninteracting with P. velutina, where F. candida grazing shiftedthe balance in favour of the latter (Table 3). There were nodifferences in mycelial overgrowth between ungrazedsystems and those grazed by P. armata (Table 3).

Extension rate of mycelial opponents in soil microcosms

In five interaction combinations the change in mycelial radialextent was significantly different between grazed andungrazed treatments (Table 4, Figs 5 and 6). Of these, in threecombinations,R. bicoloragainstH. fasciculare,P. impudicusandP.velutina, the presence of F. candida resulted in a decrease inmycelial extentofR. bicolor (Fig 5). In theother two interactions,F. candida grazing of P. velutina interacting with eitherH. fasciculare or P. impudicus, both grazed andungrazedmyceliaincreased in size over time (Fig 6). The radial extension of P.velutina (for all four extension measurements taken per repli-cate)was significantly (P& 0.05) less in grazed than inungrazedtreatments when interacting with P. impudicus but not signifi-cantly (P> 0.05) different when interacting with H. fasciculare(Fig 6A and B). P. velutina growth over H. fascicularewas slightlybut not significantly (P> 0.05) faster in grazed systems than inungrazed systems (Fig 6C).Whenover soil and interactingwithH. fasciculare, however, mycelial extension of P. velutina wassignificantly (P& 0.05) faster in ungrazed trays (Fig 6E).

Outcome of interactions within wood inoculain soil microcosms

H. fasciculare often replaced or partially replaced R. bicolor inwood blocks, though was itself often replaced by P. velutina

(Table 5). P. velutina also sometimes replaced R. bicolor. In otherinteractions there was no evidence of replacement even ifmycelial overgrowth on soil had occurred. There was someevidence of changes in the outcome of interaction in woodblocks following grazing: F. candida grazing enhanced theability of P. velutina to replaceH. fasciculare. In thepresence of P.armata,H. fascicularewas less able to replace R. bicolor (Table 5).

Discussion

The outcomes of ungrazed interations in agar and soil weresimilar to those reported in previous studies of the samespecies (Dowson et al. 1988). Importantly, outcomes on agarvaried depending on strain (only single strains were studiedon soil), H. fasciculare 1 being more combative than the otherthree strains. Such intraspecific variation in combativenesshas also recently been reported in the non-cord-formingbasidiomycete, Hericium coralloides (Crockatt et al. 2008). Thus,care must be taken when extrapolating to species based onresults for single strains.

This study provides the first report of effects of inverte-brate grazing on the outcome of mycelial interactions. Effects,however, depended on grazer, F. candida altering both theoutcome and progression of half of the mycelial interactionsstudied, while P. armata had almost no discernable effects onfungal interactions. Thus, outcomes of interactions in thefield, where there are many different species of collembolaand other invertebrates,may differ considerably from those inthe simplified laboratory microcosms.

P. armata is less active than F. candida, with a longergeneration time. Thus, whilst an equivalent biomass of thetwo collembola species was used, the extent of grazer activitymay have been lower with P. armata. Frequently the mostabundant collembola species under natural conditions(Petersen & Luxton 1982), P. armata affects mycelium of otherspecies of fungi (Hedlund et al. 1991), and may affect thebasidiomycetes in the field, if density of grazers is higher.

Previous studieshave revealedeffects of collembola grazingon extension rates of individual mycelia including bothreduction and increase of extension rate (e.g. Bengtsson &Rundgren 1983; Kampichler et al. 2004; Bretherton et al. 2006;

Table 2 e Combative scores of H. fasciculare isolates against other species in agar 12 weeks after addition of Folsomiacandida as grazing treatment

R. bicolor 2 R. bicolor 1 P. velutina P. impudicus Total rowscore

Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed Ungrazed Grazed

H. fasciculare 1 Ungrazed 10 1 10 4 25Grazed 10 0 10 3 23

H. fasciculare 2 Ungrazed 10 4 "2.5 0 11.5Grazed 10 3 2.5 1 16.5

H. fasciculare 3 Ungrazed 3 5 "1.1 0 6.9Grazed 3 5 5.5 0 13.5

H. fasciculare 4 Ungrazed "5 "3.5 0 "5 L13.5Grazed "1 "3 "10 "5 L19

Inverse column score L18 L22 L6.5 L5 L6.4 L8 1 1

Total replacement in all replicates scored 10 points, partial replacement five points and deadlock or mutual replacement zero points. Scores arebased on the outcome of all replicates. Score in the right column is for the isolates listed in the rows. Scores in the bottom row relate to thespecies listed at the head of the columns.



Fig 3 e Morphological and pigment changes during interspecific mycelial interactions in agar, either ungrazed or grazed byFolsomia candida. Hf, Hypholoma fasciculare; Pi, Phallus impudicus; Pv, Phanerochaete velutina; Rb, Resinicium bicolor. Numbersdiscriminate different strains. Images AeM are 9 cmdiam, while in N and O the interaction zone is magnified (2 cm diam).



Tordoff et al. 2006, 2008). In the present study, there wereseveral examples of increases and one example of decrease inextensionrate ingrazedsystemsof interspecifically interactingmycelia. The effect varied depending on where the myceliumwas growing (i.e. across soil or over the opponent mycelium).For example, grazing by F. candida accelerated P. velutinaextension rate when the mycelium was growing over H. fas-ciculare, compared to growing over soil. Differences in exten-sion rate in different mycelial regions have previously beenobserved: Mortierella isabellina, for example, exhibited acceler-ated growth away from the region of grazing in areas wherecollembola (P. armata) were excluded (Hedlund et al. 1991).

The accelerated growth of mycelium across an opponentmycelium only occurred in P. velutina, and only when interact-ing with H. fasciculare. This suggests that the interacting fungirespond differentially to one another and that grazing isa further complicating factor. In contrast, grazing by F. candidaon R. bicolor had a negative impact on mycelial extension rate.The frequent severing of R. bicolor cords by F. candida in allinteractions suggests that R. bicolorwas a preferred food source.HowR. bicolor survives in thefieldwhen it is soheavily damagedby F. candida in microcosm studies remains an unansweredquestion. The microcosms lacked the presence of collembolapredators but, in thefield, highpopulationdensities of F. candidamay attract predators such as Acarina, Coleoptera, such asStaphylinidae and Carabidae, thus limiting mycelial damagethrough grazer population control (Hopkin 1997). In coniferousforests, in which it is more commonly found (Kirby et al. 1990;Woods et al. 2006), R. bicolor cords may be less palatable asmycelium may contain inhibitory compounds such as poly-phenols and terpenes (Rayner & Boddy 1988; Bardgett 2005).Although studies suggesting that fungi utilise resource-derivedfeeding deterrents are scarce, changes in substrate can lead tosubstantial changes in fungal emissions of volatile organiccompounds (Bruce et al. 2000). Thus, the type of wood colonisedmay play a role in enabling fungi to withstand grazing.

P. impudicusandH. fascicularewereusually resilient tograzingwith few, if any,morphological differencesbetween themyceliaof grazed and ungrazed interactions. This contrasts with H.fasciculare growing singly where extension rate was reduced(Harold et al. 2005; Tordoff et al. 2006) and there were smallregions of intense grazing (Kampichler et al. 2004). Provision offoodchoicemayhaveminimised the impact of collembolaonH.fasciculare except when interacting with P. velutina. Here, H.fasciculare mycelium was completely removed by F. candida.

Such complete removal has not been seen with H. fascicularegrowing alone (Kampichler et al. 2004; Harold et al. 2005) sug-gesting that the interactionwith P. velutinamayhavealtered thepalatability of H. fasciculare. Initially, H. fasciculare was onlygrazed in areas where P. velutina had overgrown it. This furthersuggests that interacting with P. velutina increased the palat-ability of H. fasciculare but, as grazing took place throughP. velutina mycelium, that there was active searching forH. fasciculare mycelium by the collembola. Collembola prefercords of low vitality in some fungi (Kaneda & Kaneko 2004),although preference for actively growing hyphae has also beenreported in other species (Moore et al. 1985).

Though intense grazing of mycelia might be expected toimpact negatively on the outcome of interspecific mycelialinteractions, R. bicolor retained possession ofmore wood blockresources when extra-resource mycelia were destroyed thanwhen ungrazed during interactions with both H. fasciculareand P. velutina. This may, however, reflect reduced combat-iveness of the opponent when grazed rather than a directlypositive effect of grazing on R. bicolor.

Grazing on one interacting species may also have an indi-rect effect on the combativeness of the opponent fungus. Forexample, the accelerated growth of P. velutina when grazedlimited the ability of H. fasciculare to overgrow the P. velutinamycelium. With the exception of the interaction with P. velu-tina, H. fasciculare was generally tolerant of F. candida grazing.This may provide a niche advantage, allowing H. fasciculare toproliferate in areas of high mycophagy, where more palatablespecies would be unable to compete. Collembola densities insoil can be very high (Hopkin 1997) but H. fasciculare is ubiq-uitous in forest soils (Rayner & Boddy 1988). Whether theabundance of H. fasciculare can be attributed, even in part, tograzing tolerance is yet to be confirmed.

Previous studies have noted that site of grazing within themycelium depends on fungal species (Tordoff et al. 2006). Withinteracting mycelia additional ‘types’ of grazing site are avail-able. In particular, the interaction zone comprises dead anddying hyphae, leaked hyphal content, pigments, volatile anddiffusible compounds, and mycelium with differentmorphology (e.g. Boddy 2000; Wells & Boddy 2002; Evans et al.2008; Woodward & Boddy 2008). Such sites may be nutrientrich (Wells & Boddy 2002) and contain attractive or inhibitorycompounds. Grazing of H. fasciculare beneath P. velutina hasalready beennoted. Therewas also concentrated grazing in theinteraction zone with P. impudicus though this did not alter the

Table 3 e Outcomes of interactions between extra-resource mycelia on the surface of soil after 50e56 d

Fungal species H. fasciculare (Hf1) H. fasciculare (Hf1) P. impudicus P. velutina

Ungrazed Grazed byF. candida

Ungrazed Grazed byP. armata



R. bicolor (Rb1) P 100 P 100 P 100 P 100 P 100 O 100 O 100 M 100P. velutina o 70 o 100 e e M 100 M 100

M 30P. impudicus o 90 o 100 o 100 o 100

M 10

Outcomes with upper case letters were mutual overgrowth (M), partial overgrowth (P), total overgrowth (O), by the fungus at the head of thecolumn, whereas lowercase signifies overgowth by the fungus listed in the row. Numbers refer to percentage of replicates exhibiting a givenresponse. There were 8e20 replicates/interaction.



outcome of any interaction. The apparent increased density ofhyphae and networking (Rotheray et al. 2008) at the mycelialmargin in P. impudicusmyceliumdoes, however, indicate that itwas not entirely unaffected. The resilience of P. impudicus to

F. candida grazing when growing alone has been established(Tordoff et al. 2006) although, unlike H. fasciculare, P. impudicusalways remainedresilientwhen interactingwithothermycelia.Deadlock in all interactions indicates that, relative to the

Fig 4 eMycelial morphology on soil during interspecific interactions in (B, F, J, K) ungrazed systems, systems grazed by (A, C,E, G, H, I) Folsomia candida or by (D) Protophorura armata. Hf, Hypholoma fasciculare; Pi, Phallus impudicus; Pv, Phanerochaetevelutina; Rb, Resinicium bicolor. Scale bar (10 cm) on image H applies to images AeH. Scale bar (2 cm) on image I applies toimage I alone. Images J and K show pigment and exudate production respectively during interactions.



-4

-3

-2

-1

0

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GrazedUngrazed

Overall extension with P. velutinaE

-4

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-2

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0 2 4 6 8Day

GrazedUngrazed

Mycelial extension toward opponentF

-10-8-6-4-2024

0 4 8 12 16 20 24 28 32

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GrazedUngrazed

Overall extension with P. impudicusC

-10-8-6-4-2024

0 4 8 12 16 20 24 28 32

GrazedUngrazed

Mycelial extension toward opponentD

-10-8-6-4-2024

0 4 8 12 16 20 24 28 32 36

GrazedUngrazed

B Mycelial extension toward opponent

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)m

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GrazedUngrazed

A Overall extension with H. fasciculare

Fig 5 e Mycelial radial extent over time on soil for Resinicium bicolor interactingwith (A, B)Hypholoma fasciculare, (C, D) Phallusimpudicus and (E, F) Phanerochaete velutina, in ungrazed systems (closed symbols) and systems grazed by Folsomia candida(closed symbols). (A, C, E) aremean ± standard error of themean of all four (0#, 30#, 60#, 90#) measurements (Fig 1), and (B, D, F)are the mean of 30# and 60# measurements. Resinicium bicolor interacting with H. fasciculare (A) Scheirer Ray Hare c2[ 0.999,P< 0.001; (B) Two-wayANOVAon ranked data, F3,88[ 15.55, P< 0.001; R. bicolor interactingwith P. impudicus (C) RMANOVAF2.859,74.345[ 4.803, P[ 0.005; (D) RM ANOVA F3.013,36.154[ 6.461, P< 0.001; R. bicolor interacting with P. velutina, (E) SRHc2[ 0.762, P[ 0.238; (F) Two-way ANOVA on ranked data, F3,104[ 2.14, P[ 0.1; critical values are for time3 treatmentinteraction.

Table 4eAnalysis ofmycelial extent in grazed and ungrazed systems. Data are presented for each interaction combinationwith comparisons carried out for each species in all interactions

H. fasciculare (Hf1)grazed by F. candida

H. fasciculare (Hf1)grazed by P. armata

P. impudicus grazedby F. candida

P. velutina grazedby F. candida

Species incolumn

Species inrow

Species incolumn

Species inrow

Species incolumn

Species inrow

Species incolumn

Species inrow

R. bicolor (Rb 1) t22¼ 1.08 t22¼L6.14 t26¼ 0.61 W¼ 200 t22¼ 1.08 t12[L3.61 t26¼"1.32 t26[L3.07P¼ 0.291 P< 0.001 P¼ 0.549 P¼ 0.9085 P¼ 0.291 P[ 0.004 P¼ 0.1 P[ 0.005

P. velutina W¼ 375 t40¼ 2.16 e e t36¼ 0.74 t36[L4.65P¼ 0.351 P¼ 0.037 P¼ 0.463 P< 0.001

P. impudicus W¼ 442.5 t35¼ 0.034 W¼ 85 t16¼ 0.61P¼ 0.387 P¼ 0.734 P¼ 0.398 P¼ 0.55

Where data were not normal, a ManneWhitney U-test (W) was applied. The change in mycelial extent was measured from the time of col-lembola addition (t0) to the point at which one of the interacting mycelia reached the wood block of the opposing fungus (treach). Figures in boldare significant values at P& 0.05.



0

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RGrazedUngrazed

Mycelial extent of P. velutina in

interactions with H. fasciculare

A

0

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GrazedUngrazed

Mycelial extent over opponentC

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GrazedUngrazed

Mycelial extent over soilE

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Over soil

Over opponent

Mycelial extent in ungrazed traysI

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Over soilOver opponent

Mycelial extent in grazed traysG

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GrazedUngrazed

Mycelial extent of P. velutina in

interactions with P. impudicus

B

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GrazedUngrazed

Mycelial extent over opponentD

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Mycelial extent over soilF

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Over soil

Over opponent

Mycelial extent in ungrazed traysJ

0

2

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0 2 4 6 8

Over soilOver opponent

Mycelial extent in grazed traysH

Fig 6 e Mycelial radial extent over timeonsoil for Phanerochaete velutina interactingwith (A, C, E, G, I)Hypholoma fasciculareand(B,D,F,H, J)Phallus impudicus.Measurements (seeFig1)aremean± standarderrorof themeanof: (A,B)mycelial extent ingrazedandungrazedsystemsacrossall four extensionmeasurements (Fig1) (A,F2.443,92.850[ 2.147,P[ 0.112; B,F2.051,151.785[ 24.451,P< 0.001); (C, D) mycelial extent in grazed and ungrazed systems over opponent (C, F2.443,92.850[ 2.147, P[ 0.112;D, F2.125,84.981[ 5.611, P[ 0.004); (E, F)mycelial extent in grazed and ungrazed systems over soil (E, F4,140[ 212.849, P< 0.001;F, F2.534,73.490[ 25.626, P< 0.001); (G, H) mycelial extent over the soil and over the opposingmyceliumwithin grazed systems(G, RMANOVA F2.601,46.819[ 22.264, P< 0.001; H, F3,51[ 3.651, P[ 0.018); (I, J) mycelial extent over soil and over the opposingmyceliumwithin ungrazed systems (I, F3.141,56.541[ 32.797, P< 0.001; J, F1.751,26.262[ 9.835, P< 0.001). All reported criticalvalues are for RM ANOVA time3 treatment interaction.



speciesagainstwhich itwaspaired,P. impudicuswaseffective indefence but not in attack. This contrasts with a previous study(Dowson et al. 1988) where P. impudicus was a poor competitoragainst a similar range of species. The species and strains usedin the present study were, however, different, the microcosmslarger and the experimental period shorter.

Conclusions

Saprotrophic fungi play a critical role in ecosystem functionmaking recalcitrant nutrients available for continued plantprimary productivity. These nutrients tend to be retained inmycelia, but are probably released during mycelial interactions(J.M. Wells & L. Boddy unpub.). Further, invertebrate grazing ofthe microbial communities (including fungi) can increase therateofcarbonmineralisation (Bardgett etal.1993;Coleetal.2000).Thepresent study indicated that collembolamay also playa rolein determining fungal species combativeness during interac-tions with potential effects for species assemblages and diver-sity, andconsequentlymayalsoaffectdecompositionprocesses.The fungal response to collembola grazing during interspecificinteractions appears to vary depending on the combination ofgrazer species and the identity of the interacting fungi. Grazingclearly adds another variable affecting the outcome of inter-specific mycelial interations to those already known, forexample, abiotic environmental conditions (Boddy 2000), inoc-ulumsize (Holmer&Stenlid1993, 1997) andspeciescomposition(Holmer & Stenlid 1993; Boddy 2000; Wald et al. 2004).

Acknowledgements

We thank the Natural Environment Research Council for provi-sion of a studentship (TDR), and the Cardiff University MycologyResearch Group for useful comments on themanuscript.

Supplementary data

Supplementary data associated with this article can be foundin the online version at doi:10.1016/j.funeco.2010.09.001.

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Table 5 e Outcomes of interactions after 80e84 d from wood block reisolations

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Ungrazed Grazed byP. armata



R. bicolor (Rb1) P 40 P 20 R 42 R 29 O 100 O 100 R 20 O 100O 60 O 80 P 29 o 71 P 20

O 29 O 60P. velutina r 70 r 100 e e M 100 M 100

R 10P 10O 10

P. impudicus o 100 o 100 o 100 o 100

Outcomes weremutual overgrowth (M), partial replacement (P), total replacement (R) and overgrowth (O). For outcomes designated PR, R and O,uppercase signifies replacement was by the fungus listed at the head of the column whereas lowercase signifies replacement by the funguslisted in the row. Numbers refer to percentage of replicates exhibiting a given response. There were four to 10 replicates per interactiontreatment.



http://dx.doi.org/doi:10.1016/j.funeco.2010.09.001

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Grazing by collembola affects the outcome of interspecific

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