Plant and Soil 180: 147-158. 1996.

@ 1996Kluwer Academic Publishers. Printed in the Netherlands.147

Spatial distribution of ectomycorrhizal mats in coniferous forests of thePacific Northwest, USA

Robert P. Griffiths1,Gay A. Bradshaw2,Barbara Marks1and George W. Lienkaemper21Department of Forest Science, Oregon State University, Corvallis, OR 97331, USA * and 2Forestry SciencesLAboratory,Pacific Northwest Research Station, USDA ForestService, 3200 Jefferson Way,Corvallis, OR 97331,USA

Received 15 May 1995. Accepted in revised fonn 20 December 1995

Key words: ectomycorrhizal mats, geographic information system, geostatistical analysis, spatial patterns

Abstract

Ectomycorrhizal mats in forest soils have a wide global distribution and have been noted as potentially importantelements in forest soil nutrient cycling. To elucidate the relationship between ectomycorrhizal mats and theirenvironment, we undertook field studies and spatial analyses of mat distributions at different spatial scales.

We used two experimental approaches to study mat-forming ectomycorrhizal fungi in coniferous forests of thePacific Northwest in the United States. In the first approach, ectomycorrhizal mats and other forest floor featureswere mapped in 2 x 10 m plots and digitized into a geographical information system (GIS) for spatial patternanalysis. In order to examine larger-scale phenomena, a second approach involving other sites was taken; soil coreswere taken along 30-m transects, and distance to the closest living potential host tree was calculated for each core.

Mat patterns were studied at two scales: (1) within-stand level (i.e. variability attributed to distribution of other

mat species, forest floor attributes, and understory vegetation); and (2) stand level (i.e. variability expressed along asuccessional gradient). Mat distribution was influenced by: (1) the proximity of one mat to another; (2) the distancefrom the mat to the closest living tree; (3) the density ofliving trees in a stand; and (4) the successional stage of thestand. .

Although GIS analysis indicated that mats of different morphologies did not physically overlap, there was atendency for clustering of mats. No apparent correlations were observed between forest floor features and matslocated within the 2 x 10 m grids. On the scale of tens of meters, mats decreased with distance from the closestpotential host tree. Spatial patterns of mat distributions in harvested sites suggest that these mats may persist atleast 2 years after their host trees have been cut. For Gautieria mats, total mat area, size, and frequency differedwith stand age.

This study has demonstrated the importance of both spatial scaling and forest stand age when the naturaldistribution of mycorrhizal fungi is examined. Results suggest the need for mat research directed at higher-orderscales (e.g. stand and watershed) that will provide accurate information for managing forests to ensure their survivaland normal function.

Introduction layers and upper soil horizons of forest soils through-out the world (Castellano, 1988).This study examinesmat-forming ectomycorrhizal fungi such as those inthe genera Gautieria and Hysterangium, which pro-duce hypogeous sporocarps (truffle fruiting bodies).These mats alter the chemical and physical proper-ties of forest soil, producing localized habitats forunique assemblages of soil organisms (Cromack et

Ectomycorrhizal fungi play an important role in pre-serving species diversity by providing host trees withnecessary nutrients from mineral soil and soil orga-nic matter (Read, 1993). Some ectomycorrhizal fungiform dense, visible mats commonly found in the litter

. FAX No: + 15037371393

148

aI., 1988; Griffiths et aI., 1994; Neal et aI., 1964).They increase nutrient availablity to their host trees byweathering mineral soils and decomposing forest floorand soil organic matter (Griffiths et al., 1991a, 1994)and enhance survival of Douglas-fir seedlings underenclosed canopies (Griffiths et al., 1991b). Ectomyc-orrhizal mats occur in high concentrations (Cromacket aI., 1979) and have an essentially global distribu-tion, from boreal to semi-tropical forests (Castellano,1988). Thus, these fungi appear to play an importantrole in forest ecosystems.

Ectomycorrhizal mats are excellent systems forstudying ectomycorrhizal-soil interactions becausetheir hyphae form bundles that develop into rhi-zomorphs. In fungal mats, the rhizomorphs can bepresent in high numbers, so that up to 50% of thedry weight of mat soils can be made up of these rhi-zomorphs (Ingham et aI., 1991). By comparing chem-ical and biological characteristics of soils with highconcentrations of rhizomorphs (mat soils) with adja-cent soils with no obvious mat structure, we have beenable to determine the roles these fungi may play in for-est soils (Griffiths et aI., 1990; Griffithsand Caldwell,1992). In particular, we intensively studied mats pro-duced by two genera of ectomycorrhizal fungi, Gau-tieria and Hysterangium. These studies have beenconducted in several physiographies: the coniferousforests of the Pacific Northwest region, a eucalyptusforest in Northern California, a deciduous forest in thesouthwestern US, and a mixed conifer-hardwoodstandin Alaska (Griffiths et aI., 1991a)..

Our previous studies suggest that fungi in thesetwo genera have different and distinct functions in for-est ecosystems (Griffiths and Caldwell, 1992). Fungiof the genus Gautieria weather soil minerals, result-ing in the release of nutrients for possible use by thehost tree (Griffiths et al., 1994). In contrast, fungi ofthe genus Hysterangium seem best adapted to decom-posing organic matter releasing organic nitrogen andphosphorus for use by the host. Within the conifer-ous forests examined in this study-in Oregon's centralCascades (USA)-Gautieria and Hysterangiummats arefound on the roots of Douglas-fir (Pseudotsuga men-ziesii), in some cases growing adjacent to each otheron the same root (Griffithset al., 1991b). In all of thesestudies, mats were identified to species by the use ofsporocarp morphology (Griffiths et aI., 1991b).

Little is known about the' factors influencing matdistribution at any spatial scale, Although significantefforts have been directed at characterizing above-ground forest systems at the landscape scale, little

--

research has been conducted on belowground systems(G Bradshaw,D Perry and TBell, unpub. results). Thisstudy is the first that attempts to identify the distribu-tion of mat-forming mycorrhizal fungi in a spatiallyexplicit manner using a geographical information sys-tem (GIS) for the analysis.

To date, the only direct studies of ectomycorrhizalmat distribution have been at the 5 x 5m plot scale.Thefew stand-level sporocarp distribution studies (Luomaet aI., 1991)have not included estimations of mat dis-tribution patterns in their design. Unfortunately, defin-ing mat distributions by the sporocarp approach hasdrawbacks. Although sporocarp presence is a positiveidentifying feature of a given ectomycorrhizal fungus,it gives little information about the quantitative extentof mats, and, for several reasons, sporocarp absencedoes not prove mats are not present (Luoma et al.,1991).

Although there have been no direct observationsof mat distribution on either a regional or a water-shed scale, studies suggest that mycorrhizal mat dis-tribution may be influenced by factors at higher-orderscales, such as: (1) vegetation succession (Last et al.,1987; Read, 1993); (2) the distribution of specificplant species (Molina et aI., 1992); (3) soil type (Read,1993); and (4) the availability ofpropagules. At theselarger scales, mat distribution patterns are most likelyto be influenced by factors affecting vegetation distri-bution patterns, such as climate, disturbance type, anddisturbance patterns.

Somewhat more information is available on matdistribution patterns at the stand level, but again, itis based on the collection of sporocarps produced bymat-forming fungi. These studies have shown that thedistribution of mat-forming fungi can be influenced bystand age and soil moisture (Luoma et aI., 1991) andlocal climate (Hunt and Trappe, 1987). These resultssuggest that at this scale, and presumably at the water-shed level, mat distribution may be affected by micro-climate, as influenced by slope, aspect, and elevation.

Somewhat more is known about factors influenc-ing mat distribution patterns at the individual plotscale. While studying ectomycorrhzal colonization ofseedling roots, Harvey et al. (1987) found a direct cor-relation betweenectomycorrhizal fungal establishmentand the organic content of the soil. Fogel (1976), whostudied hypogeous sporocarps in a Douglas-fir stand,found a relationship between sporocarp presence anddistance to the nearest live Douglas-fir stem, with max-imum concentrations at about 160 em from the nearesttree.

At this scale there have been several direct studies

of ectomycorrhizal mat distribution patterns. Some ofthe earliest work showed that fungal mats (presumed tobe mycorrhizal) covered up to 25% of the forest floorin a Finnish coniferous forest (Hintikka and Naykki,1967).However, this study did notmention spatial pat-tern relative to other forest floor features except that thevegetation in mat-colonized soil consisted of speciestypical of nutrient-poor soils. In a separate study of thedistribution of Hysterangium crassum (setchellii) matsin 5 x 5 m plots in the coniferous forests of the Paci-fic Northwest, Cromack et aI. (1979) found that up to27.4% of the forest floorwas colonized by H. crassum(mean 15%) and up to 17%of the top IOcmofmineralsoil (by volume) was colonized by this fungus (mean9.6%).

At the finer scales, ectomycorrhizal mats occurredat the bases of the Pacificyew (Taxusbrevifolia), west-ern hemlock (Tsuga heterophylla), and, vine maple(Acer circinatum) with much greater incidence than incontrol plots (Griffiiths et aI., 1995), and trees tallerthan 1.5 m had a higher incidence of mats at theirbases than smaller trees. In general, mat occurrenceand tree diameter were positively correlated (Griffithset al., 1995).

Our objective in this study was to quantify the first-order spatial distribution of ectomycorrhizal mats atthe within- and between-stand scales. We expected, atthese scales, to determine the extent to which rocks,coarse wood debris, stumps, understory and overstorytrees, and stand age influenced the presence of mats.We used two experimental approaches: (1) we mappedmats and other forest floor features in gridded plotslocated in young, mature, and old-growth Douglas-firforests; and (2) we took cores to determine thepresenceof mats relative to the closest overstory tree.

Materials and methods

Site descriptions

For the mapping study, three sites of each age class(young, mature, and old growth) were chosen in andnear the H J Andrews Experimental Forest (HJA) inthe central Cascade Mountains of Oregon. The youngstands were all 35-40 years old and had had similarplot preparation, seedling planting regimes, and standthinning schedules. The mature stands grew up afterextensive natural fire events 90-125 years ago, andtrees in the old-growth stands were more than 400

149

years old. All age classes were dominated by Douglas-fir and grew on similar soils.

For the coring study, two locations were chosen fortransects; both sites were within 18 km of the HJA inforests dominated by Douglas-fir. Each site included acontrol and a "green tree retention" (GTR) treatment.

The Titan ITsite (440 12' 30" N and 1220 15' 00"W) was flat to slightly sloping with a northwest aspectand an elevation of 670 m. The control was a 125-year-old stand of Douglas-fir that originally had a densityof 200 trees per hectare. This site was thinned in 1976to a density of 68 trees per hectare, approximately35% of its original density. The GTR site had beenharvested 2 years before this study. The site was notburned after harvest; however, woody debris was piledinto windrows and burned. Mature green trees wereleft on the site at a concentration of 1 tree per hectareto provide refugia for animals and birds.

The second coring site, called the "Santiam Y" andlocated 20 km north of the Titan ITsite at 440 25' 00"N and 1220 00' 00" W, had little to no slope and anelevation of 1060 m. The control for this site was astand of old-growth Douglas-fir where some trees hadbeen removed 11 years before the study; however, itretained the essential structural characteristics of anold-growth forest. On the contrasting GTR site, pre-pared 3 years before the study, the concentration ofremaining mature trees was 4 per hectare.

Mapping and coring protocol

For the mat-mapping study, three 2 x 10 plots werechosen in each of the three sites per age class, for a totalof 27 plots. Plots were located by the same procedureused in another study (Griffiths et aI., 1995). A singledie was thrown in order to determine the direction anddistance of the lower left comer of the gridded plotfrom an arbitrary baseline at least 20 m from the edgeof the stand. Plots were flagged at 0.5 m intervals andraked to a depth of 5 cm. To-scale drawings of the type,size, and location of all ectomycorrhizal mats, rocks,logs, stumps, and all trees and shrubs were recordedin the field on hand-drawn maps with the flagged gridused as a guide.

Field identification of these mats was based onprevious studies in which we identified these matsto species using sporocarp analyses (Griffiths et al.,1991b). We found that in the geographical area usedin this study, we could field identify Gautieria matsbased on mat morphology essentially 100%of the timeand Hysterangium >90% of the time. With this back-

150

ground, we were able to identify the two mat typesfound in the field (Gautieria and Hysterangium) bymat morphology. Gautieria mats were those that wererestricted to the top portion of the mineral soil and typ-ically very dry, almost powdery in consistency. Thesefungal mats caused the soils they colonized to have alighter color than adjacent soils that had not been col-onized, which was another field identification feature(Griffiths et al., 1991b). Hysterangium mats were typ-ified by relatively coarse white to cream rhizomorphsnormally found in the litter and/or top of the mineralsoil (Griffiths et al., 1991b). In the discussion of ourresults, "Hysterangium" will be understood to includethose other few fungi that form similar mats. Bothtypes of mats are sufficiently dense and their edgessufficiently well defiined that mapping them was notdifficult. The same field crew was used throughoutthe mat mapping work, reducing interpretation errors.The locations of neighboring dominant overstory treeswere also noted. Twenty-seven maps were made, onefor each plot. These maps were used to generate digi-tized maps for the computer analysis described below.

In the coring study, mats were identified in corestaken along transects. At each site, a 30-m transectline was mapped and flagged every 25 cm, startingfrom a living mature or old-growth tree. A stainlesssteel corer with a diameter of 4.8 cm and a length of30 cm was used to take 4.8 x 10 cm cores. The coreswere extruded into plastic bags and transported to thelaboratory in an ice cooler. All cores were scored forthe presence and type of mat as well as the presenceor absence of decayed wood. If there was any doubtabout the existence or type of mat present in a core,the ground adjacent to the core was examined for matpresence. Alternate cores were saved for assays ofmoisture content measured by methods reported byGriffiths et al. (199la). The locations of all of theclosest large (mature or old-growth) green trees werenoted for calculating distances (:1:25 cm) from eachcore to the closest tree.

Mat map construction and statistical analyses

Data on mat size, shape, and location were dig-itized with a GIS (Arcllnfo, Environmental Sys-tems Research Institute). Separate digital maps wereconstructed for each mat type (Gautieria and Hys-terangium) and for all other forest floorattributeswith-in the plot-rocks, coarse woody debris (CWD-stumps,surface logs, and buried logs), and plants (vine maple,Pacificyew, and rhododendron (Rhododendronmacro-

phyllum». All features were considered as potentialcontributors to mat patterns at the two scales. Spatialstatistics and pattern indices were calculated for eachmat map in order to quantify mat distribution by matspecies, spatial correlations of mats with other forestfloor features, and stand age. Estimates of total matareas (MA), number of mats (NM), mean mat size(MMS), mat size standard deviation (MSSD), meannearest neighbor (MNN), and mean shape index (MSI)were calculated with FRAGSTATS(K McGarigal andB Marks, FRAGSTATS:Spatial pattern analysis pro-gram for quantifying landscape structure, PNW Tech-nical Report, PNW-GTR-351). These indices werechosen to provide estimates of general mat quantity,size, size variability, configuration, and distributionrelative to other mats.

An analysis of variance (ANOYA)was conductedon the variables MA, NM, MMS, MNN, MSSD, andMSI (PC Statgraphics; STSC Inc., Rockvillle, MD)in order to identify statistically significant differencesamong mats as a function of species and stand age.Yariables not exhibiting a normal distribution (MMS,MSSD) were log transformed. Interactions betweenmat type and stand age were analyzed for all vari-ables (only MA and MSSD showedsecond-level inter-actions). Least significant difference (LSD) values atthe 95% confidence level were calculated accordingly.Where there were no second-level interactions, LSDswere estimated for each mat type by stand age. Inthe coring study, the nonparametric Spearman Rankcorrelation was used to demonstrate the significanceof the correlation between distance from tree and thepresence of mats.

A "C" program calculated the empirical autocor-relation function (or semivariogram) for both mapsand core transects for each mat type; C was usedinteractively to calculate a spatial cross-correlationfunction for the gridded map data and provide mea-sures of spatial correlation between substrate variables.Althoughboth data sets were generally found to satisfythe condition of local stationarity (see Isaaks and Sri-vastava, 1989, for definitions of geostatistical terms),there were some cases where trend and anisotropy (i.e.values of semivariogram differing according to thedirection of calculation) at larger lags were observed;in these instances, higher-lag information was disre-garded. Otherwise, no preanalysis corrections (e.g.detrending) were performed. The semivariogram pro-gram used a maximum lag distance of 33% (33% ofrows and columns in an image).

.~. _-II)..tI........~

20o

Young OldGrowth

Figure 1. Intra- and intelSpecies comparisons of mean distancesbetween mats for different age stands. There were second-levelinteractions between stand age and both mat types as determined

by multifactor ANOVA. Groups sharing the same letter are not sig-nificantly different.

Results

In the mapping study, at the within-stand scale, the spa-tial cross-correlation function indicated that very littlephysical overlap occurred between Gautieria and Hys-terangium. Statistically significant second-level inter-actions by stand age and mat type were found in themean distances between mats (Fig. 1). The largestdistances were observed between Gautieria and Hys-terangium mats in young stands, and the next largestbetween these mats in old growth. Distances betweenmats of the same species did not differ significantlywith stand age (Fig. 1).

Frequency histograms of different classes of dis-tances suggest that in the young stands, Gautieriamatsstart out as clusters with a relatively narrow range ofdistances between mats (Fig. 2a); the most commonrange is from 10 to 20 cm. In the mature stands, thedistance between mats becomes greater as new matloci become established, resulting in a wider range ofdistances between mats (Fig. 2b). In the old-growthforest, more mats become established and the spacingagain resembles that found in the young stand (Fig.2c). The pattern for Hysterangium mats suggests thatas the stands mature, there are fewer occasions whenspacing between mats is wide; i.e. the spacing is morehomogeneous with increasing stand age (Figs. 2d-2f).

There was no correlation between rocks and thepresence of Gautieria mats, and nocorrelation betweenburied logs and Hysterangium mats. In fact. nearestneighbor and cross-correlation results showed no sig-

151

nificant correlations between presence of Gautieria orHysterangium mats and any of the features in the plots,including understory trees.

In the coring study, our objective was to determinewhether there was a correlation between the presenceof mats and distance from the closest potential host(generally speaking, mature or old-growth Douglas-fir). We found an inverse relationship between the per-centage of cores having mats and the distance to theclosest potential host tree (r =-0.212, p < 0.0001 forthe TItan II site; r =-0.334, p < 0.0001 for the Santi-.am Y). This relationship is shown in Figure 3, wherein the control sites (Fig. 3a), the percentage of coreswith mats decreased with distance from the closest tree(combined data set from both sites). Within each of thefirst three l00-em increments, 48% of cores containedmats; beyond that. the frequency generally decreased,with the lowest frequency in the range of 600 to 700em from the closest tree.

The pattern in GTR plots (Fig. 3b) for all coreswithin the first 600 cm was essentially the same as thatin the control plots. However, thehighest percentage ofmats in the cores nearest the trees was only about 28%.Beyond 600 em, mat frequency once again increased,with the original decreasing pattern repeated between700 and 1000 cm. There was then another increasein frequency between 1000 and 1100 em. With theexception of the interval between 1400 and 1500 em,this pattern of increasing and decreasing mat frequencyoccurred within two more intervals of approximatelythe same width (at 1000 to 1600em and 1700 to 2200em). Data (not shown) of GTR transects from bothsites show the same trend in all transects to varyingdegrees.

As shown above, there were large differences inthe percentages of cores with mats among stands withdifferent ages or treatments. These differences weremost extreme at the Santiam Y site; in the control site(an old-growth stand), 53.4% of the cores had mats,but in the GTR site only 14.2% had mats. Similarly,distribution patterns in the mapping study showed thatin young stands, the total area covered by Gautieriamats was relatively small compared with that occu-pied by Hysterangium; these latter mats varied greatlyin size and appeared to have an irregular distribution(Fig. 4a). In the old-growth stand, Gauteria mats cov-ered a greater total area than Hysterangium mats, andboth seemed to have a more regular distribution (Fig.4b). When all data for total mat areas per plot wereconsidered, Gautieria showed significantly less totalarea than Hysterangium in young stands (Fig. Sa). In

1

120 IE

100

C SOQ)Q)

SOCD

Biis

15215

12 a GautiB~Young Fores1, 25

9

..CD.,!3(3ScS.,is'0

gCD::J

1

b Gautien.Malure

o50

C GautiBda-OkI Growth

40

3D

d Hysterangium- Young FOres1

e HystBtangium-Malure

f HysterangiUlll-Old Growth

50 100 150 2DD 250 300

Distances BetwB8n Mals (by 1o-cm incremenls)

2DD 250 3DD

Figure 2. Frequency histograms of distances ~een mats. Distances between Gautieria mats in a young, b mature, and c old-growth stands,and between Hysterangium mats in d young, e mature, and r old-growth stands.

mature stands, the two species exhibited very similartotal areas. In old-growth stands, the total area for Gau-tieria mats was significantly greater than in young andmature stands. No significant trends were observed forHysterangium mats by stand age. The area covered byboth mat types in these plots ranged from 10% of thetotal area in the young stand to 20% in the old growth.

To determine whether the increase in total Gau-tieria mat area with stand age (Fig. 5a) was causedby an increase in the number of mats per plot or anincrease in mat size, we measured both of these factors(Figs. 5b and c). Like total mat area (Fig. 5a), the num-ber of Gautieria mats per plot increased significantlywith stand age, but there was no comparable increase inHysterangium mat numbers (Fig. 5b). Mean Gautieriamat size showed essentially the same pattern; i.e. Gau-tieria mat size increased significantly with stand age,but there was no comparable increase in Hysterangiummat size (Fig. 5c).

We were also interested in assessing mat size vari-ability by stand age for both types of mats (Fig. 6a).

Gautieria mats showed a significant increase in matsize standard deviation (MSSD) with stand age, butHysterangium mats did not. Analyzing the mean shapeindex (MSI) allows quantification of mat shape regu-larity for different stand ages (Fig. 6b). MSI measuresthe average complexity of patch shape compared witha circle; MSI equals 1.0 for a circle and increaseswithout limit as the patch shapes become more irreg-ular. The only significant successional trend in MSIwas an increase with stand age in Gautieria mats (Fig.6b), where mats in old growth were significantly morecomplex'than those in young stands.

Discussion

The study focused on four factors that could influencemat distribution at different scales: (1) intraspecies and

interspecies interactions (Le. between-mat influences);(2) non-vegetative forest floor features; (3) neighbor-ing vegetation; and (4) stand age. Spatial variability

o 200 400 600 800 1000120014001600 180020002200

Distance to Closest Tree (em)

Figure 3. The percentage of cores containing mats as a functionof distance to the closest tree on a control sites and b "Green tree

retention" (GTR) sites in the coring study.

was examined at two scales: at the intra- (or within-)and inter- (or between-) stand levels. The study wasundertaken with the assumption that processes func-tioning at higher spatial orders (i.e. greater than theplot size) did not contribute to measured patterns.

The mat mapping study was our first attempt atdocumenting factors influencing ectomycorrhizal matdistribution patterns. The results of this study demon-strated the need to conduct studies at different scalesand with differentdesigns if we were to obtain a clearerunderstanding of the factors affecting distributions. Alater study that specifically looked at the associationsbetween mats and understory vegetation demonstrateda high incidence of mats at the base of understory trees(Griffithset al.. 1995);this trend had not been observedin the original mapping study where there were too fewunderstory trees to show a consistent trend. The cor-ing study reported in this paper was our attempt tobetter understand larger-scale patterns of mat distribu-tions. This study showed that the size of the original

a Young Stand

,

153

b Old-growth Stand

.

~...~ . ..::.~:.Gautiena 12m

II Hysterangium

Figure 4. A graphic representation of the size, shape, and distributionof Gautieria and Hysterangium mats in typical 2 x 10m plots in a:a young Douglas-fir stand and b: an old-growth stand.

grid was too small to show the influence of individualoverstory trees on mat distributions.

Influence of intraspecies and inter species interactions

Earlier studies have indicated that mats tend to be

clustered (R P Griffiths. unpubl. data). These obser-vations suggest that a component of intra-stand vari-ability in mat distribution may be attributed to thepresence (or absence) of other mats. Using the spa-

50

40

30

20

>:u 10cCD:>0'

,g::.!! 0 100 200 300 400 500 600 700!!...CD 40ucCD

a.'Iii 30

20

10

154

f- 0.12CDN

en 0.10

1ii::: 0.08cas~ 0.06

0.04

0.02

3.0

2.5

a MatAreaIIIGautieria. HysterangiumLSD-1.09

c

2.0

1.5

1.0

0.5

o18

16b Mat Number

B

12

14 LSD-7.51

10

8

6

4

2

o

0.18J C MatSize

0.16

0.14

oYoung Mature Old Growth

Figure 5 a: The total mat area, b: number of mats and c mean mat

size per 2 x 10m plot for both mat types at each succ:essional stage;means of 9 plots per stage. In a, groups sharing the same letter arenot significantly different. In b and c, there were no second-levelinteractions by stand age or type; upper case letters show Gautieriamat comparisons by stand age, and lower case letters indicate thatthere were no significant differences by stand age for Hysterangiummats.

~~ 0.20o,.,<II'5Q)

C 0.16"E<II"0c

c7J 0.12Q)N

Ci.i

iii 0.08:tc<IIQ)

:t 0.04

)(Q)

~8. 1.26III.cenc<IIQ):t

0.24

o1.32

bMSI

1.30

B1.28

1.24

1.22

1.20Young Mature Old Growth

Figure 6 a: The meanmat size standard deviationMSSD andb: meanshape index (MSI) for each 2 x 10 m plot for both types of matsat each successional stage; means of 9 plots per stage. Significantdifferences are shown as in Figure 5b and c.

tial cross-correlation function calculated from the dig-itized mapped mats and nearest neighbor estimations(FRAGSTATS),we calculated the influence of one maton the presence of another. The lack of overlap foundbetween species supports a phenomenon frequentlyobserved in the field; i.e. Gautieria and Hysterangiummats are ItlUtuallyexclusive, but they can be foundadjacent to each other.

Influence of non-vegetative forest floor features

A central objective of our mapping rocks and decayingwood was to determine whether these features influ-enced mat distributionwithin the2 x 10m plots. In pre-vious studies, Gautieria mats were often found in highconcentrations in rocky soils (R P Griffiths, unpubl.

observ.); this distribution might beexpected from Gau-tieria biogeochemistry (Griffithsand Caldwell, 1992).When the chemistry of Gautieria mat soil solutionsand that of adjacent soils with no obvious mats arecompared, the Gautieria soils show very high concen-trations of organic acids and higher concentrations ofa range of ions than the non-mat soils (Griffithset al.,1994).From these observations, Griffiths et al. (1994)concluded that these mats are responsible for acceler-ating mineral soil weathering. We hypothesized thatwithin the grids, rocks would increase the frequencyof Gauteria mats. However, our GIS analysis of forestfloor features showed no apparent relationship betweenthe presence of rocks and the distribution patterns ofGautieria mats.

We also expected to find a relationship between thepresence of CWD in advanceddecay states and the dis-tribution of Hysterangium mats. In the field, we haveoften observed that Hysterangium mats are associatedwith highly decayed buried CWD and litter. Similar-ly, Harvey et ai. (1979) discovered a strong positivecorrelation between the occurrence of ectomycorrhizalfungi and advanced decay state wood during a studyof ectomycorrhizal fungal distributions in Montanaforests. Laboratory studies of exoenzymeactivity asso-ciated with Hysterangium-colonized soils showed thatenzyme activities were much higher than in non-matsoils and were also generally higher than in Gautieriamat-soils (Griffiths and Caldwell, 1992). Althoughthese observations suggest that Hysterangium matsmay be well adapted to decomposing organic matter,we did not see a correlation between buried logs andthe presence of Hysterangium mats.

In fact, nearest neighbor and cross-correlationresults showed no significant correlations betweenpresence of Gautieria or Hysterangium mats and anyof the features in the plots. It is still possible, however,that correlations do exist but that the number of plotsor the type of analysis did not show these correlations.It is also possible that mat distribution is controlledat scales larger than a few meters, swamping out anylocalized relationships.

Influence of neighboring trees

To determine how both understory and overstory(potential host) trees influenced mat distribution, wehave taken two different approaches.The firstapproachwas to specifically look for mats in plots at the basesof understory trees and compare the incidence of matsin those plots with mats in control plots (without trees)

155

of the same size (Griffiths et aI., 1995). The secondapproach was the coring experiment conducted afterthe mat mapping phase of the present study.

The first approach showed that mats were morelikely to be found at the bases of understory trees thanin control plots without trees. In that tree-plot study(Griffiths et al., 1995), almost 1,500 tree plots and anequal number of control plots were studied for the pres-ence of ectomycorrhizal mats. Ten of the 12sites werewithin 12 km of the sites used in the current study.More than 75% of the understory tree plots containingPacificyew, vine maple, or western hemlock had ecto-mycorrhizal mats associated with them, as opposedto only 50% in control plots (Griffiths et aI., 1995).Although this result demonstrates that mats are morecommonly found at the bases of understory trees, nosuch correlation was observed in the mapping portionof the current study.

In the coring study, the inverse relationshipbetween the percentage of cores having mats and thedistance to the closest potential host tree showed thatmat distribution patterns in our mapped 2 x 10m plots(on the scale of a few meters) may be driven, in part,by a largerpattern caused by the presence of host trees.One explanationfor the "periodicity" found in the GTRplots may be related to an increased number of activeroots near the drip line of the canopy for the remainingmature trees. However, this explanation does not ade-quately account for the repeating pattern seen between1100and 1600cm and between 1700and 2200 cm (Fig.3). We have generally assumed that once the originaltrees have been harvested, energy from the host treewould be cut off and the mats would soon disappear.Because the GTR sites had been harvested at 2 (TitanII site) and 3 (Santiam Y) years, we did not expect themat pattern to approximate the spacing in the originalstand. However, it is possible that these mats are main-taining themselvessaprophytically or are supported byalternate hosts (Read, 1993).

Influence of stand age

Prior to this study, we hypothesized that as a Douglas-fir stand evolved, Gautieria and Hysterangium matswould develop at about the same rate, with Gautieriamats providing the trees with P by weathering themineral soil and Hysterangium mats providing N andP by decomposing litter and soil organic matter. Inessence, our predictions matched the response of theGautieria mats to stand age, but not the response ofHysterangium (Fig. 5a). Although P can be a limiting

156

a Coalescence of smaller mats.

b Deformitydue to rocks. etc.

Young Mature Old Growth

Figure 7. Possible mechanisms by which Gautieria mats may fonn colonies with stand age. a: Individual smaller colonies coalesce into largercolonies. b: As mats get larger they grow against rocks, stumps, buried logs, and other forest floor features and become disfigured.

factor for tree growth in these forests, N is the primarylimiting nutrient in most forest ecosystems (Cole andRapp, 1981). Early colonization by Hysterangium inthe young stands suggests that N may be extracted fromlitter early in stand succession. The slower Gautieriamat development may reflect an abundance of P, if weassume that mat formation is regulated in some wayby P availability.

On the basis of total mat area alone, we cannotdetermine whether the increase in total Gautieria matarea with increasing stand age is attributable to anincrease in mat number or in mean mat size; furtherclues to factors influencing mat distribution may comefrom the GIS analyses. At least some of the increase,however, is due to an increased number of mats (Fig.5b), although there was also a significant increase inmean mat size (Fig. 5c). Although the stand age differ-ences observed in Hysterangium mats were not statis-tically significant, the trends are clear. The reduction

in Hysterangium mat area occurring in the transitionfrom young to mature stands (Fig. 5a) was caused bya decrease in the mean mat size (Fig. 5c), even thoughthere was an increase in the number of mats (Fig. 5b).These results indicate that the relationships betweenmat size or numberand stand age are very different forthese two types of ectomycorrhizal fungi.

Patterns of Hysterangium mat distribution also maybe explained in terms of the distribution of active rootsand the fact that the two mat types do not occur in thesame location. The p~tchiness of the Hysterangiummats in the young stands (Fig. 4a), which had beenthinned to approximately a third of their original den-sity, may be due to the patchiness of active roots orof litter distribution. The development of smaller andmore evenly sized Hysterangium mats in old-growthsoils (Fig. 4b) may be due to an increase in competitionfrom Gautieria for the same sites.

When analyzed in the context of mean mat size(Fig. 5c), the MSSD data (Fig. 6a) suggest that Gau-tieria mats may start out in young stands as small dis-tinct entities of similar size, but as stand age increases,they join to form larger mats, resulting in a greaterrange of sizes (K Cromack, pers. commun.; Fig. 7a).There was a significantly greater amount of mat sizevariability in young stand Hysterangium mats than inGautieria mats (Fig. 6a; see also sample mat distribu-tions in Fig. 4).

The trend observed in MSI (Fig. 6b) reflects thepattern expected from the coalescence of two or moreGautieria mats to form larger mats with a more irregu-lar shape (Fig. 7a); a similarresult could occur iflargermats came into contact with rocks or other forest floorelements that could distort their shapes (Fig. 7b).

Conclusions

This study suggests that forest management practicesmay significantly influence colonization patterns ofectomycorrhizal mats in coniferous forests. For exam-ple, the total area of all mats was greater in old-growth forests than in clear-cut units containing fewold-growth trees. Once a forest has been harvested,the reestablishment of mats at different stages of forestsuccession may vary significantly for different mat-forming fungi. The negative correlation between dis-tance from nearest potential host tree and the presenceof mycorrhizal fungi clearly shows that the presenceof host trees is important to mat distribution patterns.The concentration and pattern of trees remaining at thestand or watershedscale, along with microclimatic fac-tors, may be the strongest predictors of mat distributionat these scales.

If mat distribution patterns across the landscape areto be understood, future studies must focus on exam-ination of microclimate and vegetation characteristicsat larger (i.e. coarser) scales. For instance, theability ofthese mats to act as propagules for colonization of thenext generation of trees is not understood at this time.Another important focus for future work should be todetermine whether colonization of trees in a regen-erating stand by mat-forming fungi depends more onmats in adjacent stands or on remnant mats from theoriginal stand. Thus, an understanding of the effects ofspatial configuration on regeneration across scales willbe integral for conserving forest productivity.

157

Acknowledgements

We thank the National Science Foundation for finan-cial support fromgrants BSR-8717849, BSR-9106784,BSR-8717849, and BIR-8900461 (Research Experi-ences for Undergraduates (REU) and the USDA For-est Service, Pacific Northwest Research Station Sup-plemental Agreement Number PNW 92-0289 withOregon State University. The authors would like tothank A Chadwick, S Goldsmith, A Thompson, andthe 1992 REU students (J Guardino, V Guerrero, CMcClung, L Paige, K Patterson, N Petty, M Robatzekand C Torgersen) for technical assistance and JaneThomas for editing the manuscript. We are also grate-ful for assistance from theco-investigators for the REUprogram at the H J Andrews Experimental Forest, JBeatty, A McKee and A Moldenke. This contributionfrom the Andrews Forest Ecosystem Research Groupis Paper 3066, Forest Research Laboratory, OregonState yniversity.

References

Castellano M A 1988 The taxonomy of the genus Hysterangium(Basidiomycotina, Hysterangiaceae) with notes on its ecology.Ph.D. thesis. Oregon State University, Corvallis, OR, USA. 238p.

Cole D and Rapp M 1981 Elemental cycling in forest ecosystems.In Dynamic Properties of Forest Ecosystems. Ed. D E Reichle.

pp 341-409. Cambridge University Press, Cambridge, UK.Cromack K Jr, Fichter B L, Moldenke A M, Entry J A and Ingham

E R 1988 Interactions between soil animals and ectomycorrhizalfungal mats. Agric. Ecosyst. Environ. 24,161-168.

Cromack K. Sollins P, Grausten W C, Speidel K. Todd A W, SpycherG, Li C Y and Todd R L 1979 Calcium oxalate accumulation and

soil weathering in mats of the hypogeous fungi HysterangiumcrasSUffl. Soil Bioi. Biochem. II 46~8.

Fogel R 1976 Ecological studies of hypogeous fungi. II. Sporocarpphenology in a western Oregon Douglas-fir stand. Can. J. Bot.54, 1152-1162.

Griffiths R P, Baham J E and Caldwell B A 1994 Soil solution chem-

istry of ectomycorrhizal mats in forest soil. Soil BioI. Biochem.26,331-337.

Griffiths R P and Caldwell B A 1992 Mycorrhizal communitiesin forest soils. In Mycorrhizas in Ecosystems. Eds. D J Read,D H Lewis, A H Fitter and I J Alexander. pp 98-105. CABInternational, Oxon, UK.

Griffiths R P, Caldwell B A, Cromack K Jr and Morita R Y 1990

Douglas-fir forest soils colonized by ectomycorrhizal mats. I.Seasonal variation in nitrogen chemistry and nitrogen cycle trans-formation rates. Can. J. For. Res. 20, 211-218.

Griffiths R p, Caldwell B A, Ingham E R, Castellano M A and

Cromack K Jr 1991a Comparison of microbial activity in ecto-mycorrhizal mat communities in Oregon and California. BioI.Fertil. Soilll, 196-202.

Griffiths R P, Castellano M A and Caldwell B A 1991b Ectomyc-orrhizal mats formed by Gautieria monticola and Hysterangium

158

setchellii and their association with Douglas-fir seedlings, a casestudy. Plant and Soil 134, 255-259.

Griffiths R p, Chadwick A C, Robatzek M, Schauer K and Schaffroth

K A 1995 Association of ectomycorrhizal mats with Pacific yewand other understory trees in coniferous forests. Plant and Soil173,343-347.

Harvey A E. Jurgensen M F, Larsen M J and Graham R T 1987Relationships among soil microsite, ectomycorrhizae, and naturalconifer regeneration of old-growth forests in westem Montana.Can. J. For. Res. 17,58-62.

Harvey A E. Larsen M J and Jurgensen M F 1979 Comparativedistribution of ectomycorrhizae in soils of three western Montanaforest habitat types. For. Sci. 25, 350-358.

Hintikka V and Naykki 0 1967 Notes on the effects of the fungusHydnellum ferrugineum (Fr.) Karst. on forest soil and vegetation.Commun. Inst. For. Fenn. 62, 1-23.

Hunt G A and Trappe J M 1987 Seasonal hypogeous sporocarpproduction in a western Oregon Douglas-fir stand. Can. J. Bot.65,438445.

Ingham E R, Griffiths R P, Cromack K and Entry J A 1991 Compari-son of direct versus fumigation-flush microbial biomass estimatesfrom ectomycorrhizal mat and non-mat soils. Soil BioI. Biochem.23, 465-472.

I'urchl8er' h.. ,,~"" Fo...."rvlce h,. , ' UG8

Isaaks E H and Srivastava R M 1989 An Introduction to AppliedGeostatistics. Oxford University Press, Oxford, UK.

Last F T, Dighton J and Mason P A 1987 Successions of sheathingmycorrhizal fungi. Trends Ecol. Evol. 2,157-161.

Luoma D L, Frenkel R E and Trappe J M 1991 Fruiting of hypo-

goous fungi in Oregon Douglas-fir forests: seasonal and habitatvariation. Mycologia 83, 335-353.

Molina R, Massicotte H and Trappe J M 1992 Specificity phenomenain mycorrhizal symbioses: community-ecological consequencesand practical implications. In Mycorrhizal Functioning: An inte-grative Plant-Fungal Process. Ed. M FAllen. pp 357-423. Chap-man and Hall, New York, NY, USA.

Neal J L Jr, Bollen W B and Zak B 1964 Rhizosphere microflora

associated with mycorrhizae of Douglas-fir. Can. J. Microbiol.10,259-265.

Read D J 1993 Plant-microbe mutualisrns and community structure.

In Biodiversity and Ecosystem Function. Eds. E-D Schulze andH A Mooney. pp 181-209. Springer-Verlag, Berlin, Germany.

Section editor: J H Graham