Comparison of ectomycorrhizal- basidiomycete communities in red spruce versus northern hardwood forests of West Virginia

G. F. BILLS' Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA, U.S.A. 24061

G. I . HOLTZMAN Department of Statistics, Virginia Polytechnic Institute and State University, Blacksburg, VA, U.S.A. 24061

AND

0. K. MILLER, JR. Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA, U.S.A. 24061

Received January 25, 1985

BILLS, G. F., G. I. HOLTZMAN, and 0. K. MILLER, JR. 1986. Comparison of ectomycorrhizal-basidiomycete communities in red spruce versus northern hardwood forests of West Virginia. Can. J. Bot. 64: 760-768.

Sporocarps of Basidiomycetes belonging to families containing some species known to form ectomycorrhizae were enumer- ated in 12 plots (16 X 16 m) subdivided into contiguous 2 X 2 m quadrats during the growing seasons of 1981 - 1983. Plots were distributed equally between homogeneous second-growth red spruce stands and heterogeneous northern hardwood stands in southeastern West Virginia. A few major species accounted for most of the abundance, while most species fruited rarely, but abundance and phenology varied broadly from year to year, apparently in response to rainfall and temperature. Fungal species composition, spatial frequency, and sporocarp density in the two forest types differed as would be expected in light of the symbiotic nature of the fungi and trees considered. Of 54 fungal species encountered over 3 years, 19 occurred exclusively in spruce plots, 27 occurred exclusively in hardwood plots, and 8 occurred in both forest types. In both forest types, approxi- mately 40% of the species were Russulaceae. Species frequency and sporocarp abundance were greater in spruce plots than in hardwood plots. The Shannon-Wiener index, the dominance-diversity curve, the species-area curve, and ordination confirmed that fungal species richness, equitability, and diversity were greater in the mixed-hardwood plots, which hosted many rare fungal species, than in the single-species coniferous plots, which were dominated by a few ubiquitous fungal species.

BILLS, G. F., G. I. HOLTZMAN et 0 . K. MILLER, JR. 1986. Comparison of ectomycorrhizal-basidiomycete communi- ties in red spruce versus northern hardwood forests of West Virginia. Can. J. Bot. 64: 760-768.

Les auteurs ont effectut des observations dans 12 stations (16 x 16 m), subdivistes en quadrats contigiis de 2 x 2 m, au cours des saisons de croissance de 1981 - 1983; ils ont tnumtrt les sporocarpes de Basidiomycktes appartenant B des familles contenant des esptces reconnues comme ectomycorhiziennes. Les places tchantillons ttaient rtparties tgalement entre des stations homogknes d'ipinette rouge en regtntration et des stations htttrogknes d'espkces feuillues nordiques; elles ttaient toutes situtes dans le sud-est de la Virginie de l'Ouest. Quelques espkces dominantes sont responsables de la majeure partie de l'abondance, alors que la majoritt des espkces n'ont fructifit que rarement; l'abondance et la phinologie ont varit largement d'une annie B l'autre, apparemment en rtaction aux prtcipitations et B la temptrature. La composition en espkces fongiques, le frtquence spatiale et la densitt des sporocarpes dans les deux types de forkt diffkrent, comme on pouvait s'y attendre selon les relations symbiotiques qui existent entre ces champignons et les espkces d'arbres considirtes. Parmi les 54 espkces de champignons observies au cours des 3 annies, 19 ont t t i retrouvtes exclusivement dans les parcelles avec tpinette, 27 se sont avtrtes exclusives aux parcelles en forkt feuillue alors que seulement 8 ttaient communes aux deux types de station. Dans les deux types de forkt, les Russulacies constituaient environ 40% des espkces. La frtquence des espkces et l'abondance des sporocarpes ttaient plus grandes dans les parcelles en tpinettes que dans celles en espkces feuillues. L'index Shannon- Wiener, la courbe de dominance-diversitt, la courbe espkce-surface ainsi que I'ordination confirment que la diversitt est plus grande dans la for& mixte dtcidue laquelle contient plusieurs espkces fongiques rares, que la forkt monosptcifique B tpinette, laquelle est dominie par quelques espkces fongiques ubiquistes.

[Traduit par la Revue]

Introduction The ectomycorrhizal - basidiomycete communities of red

spruce stands and of nearby mixed-hardwood stands in south- eastern West Virginia were observed during the 1981 - 1983 growing seasons. This report summarizes and compares spe- cies composition, richness, equitability, diversity, abundance, and fruiting phenology in the two communities, taking into account both spatial and temporal (year to year) variation. The ultimate objective was to provide a biogeographic basis for comparing basidiomycete communities in similar coniferous and hardwood forests.

Most earlier quantitative studies of macrofungal communi- ties have focused on sporocarp biomass or density in standard

'Present address: Mycology, Building 01 l A , BARC-West, Beltsville, MD, U.S.A. 20705.

reference areas, because the naturally occurring thalli of Basidiomycetes cannot be delimited in a direct manner, except in rare cases (e.g., Cotter and Bills 1985). The critical assump- tion of many of these studies was that the relative productivity of sporocarps in some way reflected their relative dominance, mycelial biomass, or resource utilization. Positive correlation between sporocarp biomass and mycelia biomass has been found in single-species studies (Laiho 1970; Newel1 1984; Cotter and Bills 1985) and in one study of the combined spe- cies of an entire community (Menge and Grand 1978). How- ever, there is no reason to believe that the ratio of sporocarp numbers to mycelial biomass is uniform among species. Sporocarp productivity is undoubtedly influenced by many factors whose effects vary broadly among species. Therefore, in addition to sporocarp density, we considered the spatial "frequency" of each species, i.e., the number of small

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BILLS ET AL. 76 1

TABLE 1. Biweekly rainfall (centimetres) at Marlinton,* WV (U.S. Forest Service)

Weeks 1981 1982 1983

June 1-15 June 16-30 July 1 - 15 July 16-31 August 1-15 August 16-31 September 1 - 15 September 16 - 30

Total

*At 15 to 20 km west of the study area, elevation 650 m.

quadrats in which fruiting of the species occurred, as a mea- sure of mycelial activity and ubiquity.

Materials and methods The study areas were located near the eastern edge of the ungla-

ciated Allegheny Plateau in Pocahontas Co., WV, within the Monon- gahela National Forest (boundaries 38'17' N, 38'07' N, 80'22' W, 80°i2' W). Sites were located on ridge crests (elevation 1200- 1350 m) on shallow, rocky, well-drained, sandy-loam or clay-loam soils. Within the spruce stands, soil pH ranged from 3.3 to 3.8, and mean soil organic matter content was 12.3 + 3.6% SD (n = 23). Within the hardwood stands, soil pH ranged from 3.3 to 4.5 and mean soil organic matter content was 10.6 + 3.4% SD (n = 20). Precipi- tation patterns for each growing season were estimated from U.S. Forest Service data (Table 1). Frost-free periods range from 88 to 145 days (Edens 1973). All stands were second growth (55-75 years old, Table 2). In spruce stands there was a sparse to dense shrub layer of Vaccinium erythrocatpon, suppressed spruce seedlings, and ferns. An extensive ground cover of bryophytes, especially the leafy liverwort Bauania trilobata (L.) S. F. Gray, was often present. Herbaceous plants, including ferns and young Acer stems, were abundant in the understories of the hardwood stands.

Twelve permanent 16 x 16 m plots were established on ridge crests of three different mountains: Black Mountain (spruce plots 1 and 2, hardwood plots 3 and 4), Kennison Mountain (spruce plots 7 and 8, hardwood plots 5 and 6), and Rocky Knob (spruce plots 9 and 10, hardwood plots 11 and 12). Spruce plots were selected to exclude as many other woody species as possible. Hardwood plots were se- lected to be close to the spruce plots, without including any red spruce. In each plot, diameter at breast height of all stems greater than 2 cm was estimated (Table 2) and mapped, and fern, bryophyte, and spruce seedling cover was estimated (Bills 1985). Because hardwood plot 3 was destroyed in the spring of 1983, estimates for 1983 were based on the five remaining hardwood plots.

All sporocarps of basidiomycete families containing some species known to form ectomycorrhizae (Watling 1982; Miller 1983) were counted. Thus, some species whose ecological role is uncertain were included, e.g., Clavulina cristata, Cys todem amianthinum, Boleti- nellus merulioides, Entoloma spp., and some Hygrophorus spp. Ecto- mycorrhizal roots of red spruce seedlings collected near sporocarps of Clavulina cristata were examined and found to have hyphae and tissues similar to those of the sporocarps. Riffle (1973) was unable to obtain mycorrhizal synthesis between Cys todem cinnabarina and Pinusponderosa, H. V. T. Cotter (unpublished) was unable to obtain synthesis between Fraxinus pennsylvanica Marsh and Boletinellus merulioides, and some Hygrophorus species are thought to be nonmy- corrhizal (Miller 1983). A sporocarp of Clavulina cristata was de- fined as a separate stem completely surrounded by the surface of the litter or the bryophyte layer, although the stems may have been fused below ground. Long-lived sporocarps that could have been counted twice (e.g., Sc le rodem citrinum, large Lactarius spp.), sporocarps

needed for identification, and voucher specimens were removed from the plots. Representative voucher specimens of all fungi are deposited at Virginia Polytechnic Institute.

Each plot was subdivided into 64 contiguous 2 X 2 m quadrats and was visited 8 to 10 times per growing season at 7- to 17-day intervals. On each visit, the number of sporocarps of each species in each quadrat was recorded. These counts were analyzed in terms of sporo- carp density to maintain continuity with earlier studies and in terms of species frequency and percent frequency to quantify the spatial extent of mycelial activity. "Sporocarp density" is the number of sporo- carps per unit area. "Species frequency" is the number of quadrats in which the species fruited one or more times during the 3-year period. "Percent frequency," the percentage of the total number of quadrats (6 x 64 = 384) in each forest type in which a species occurred, i.e., 100 times the species frequency divided by i84, is a measure of species ubiquity. Pielou (1977) suggested using presencelabsence in contiguous quadrats (i.e., species frequency) for studying the spatial pattern of sessile organisms (e.g., fungal thalli) when there are no natural sampling units and no clearly delimited individuals. To de- scribe the year to year variability of the extent of fruiting, "yearly percent frequency," the percentage of quadrats in which a species occurred in a given year, was tabulated also. Note that if a species fruited in the same quadrat in different years, then the frequency of that species is necessarily less than the sum of its yearly frequencies.

Comparison of species richness and equitability between the two forest types was accomplished by means of the Shannon-Wiener index of diversity, namely, H' = -E,P, log,P,, where PI is the probability of sampling the ith species among all species (Shannon and Weaver 1949). To summarize and compare the plot to plot varia- tion of species composition, principal-component analysis (PCA) was used to order the rows and columns of the species x plots matrices of Table 2 (basal area of trees) and Table 3 (fungal percent frequency), as recommended by Gauch (1982).

Results Species diversity

Fungal species richness was comparable between forest types (Table 4), but the two forest types exhibited little overlap in fungal species composition (Table 3). Of the 54 species encountered over 3 years, 19 (35%) occurred exclusively in spruce plots, 27 (50%) occurred exclusively in hardwood plots, and 8 (15%) occurred in both forest types (Table 3). The family Russulaceae accounted for more species than any other family in both forest types: 39% of the species in hardwoods plots and 44% of the species in spruce plots. The mean number of species per plot was not significantly different between spruce and hardwood plots (Table 4). The similarity in slopes of the species -area curves (Fig. 1) also indicated compara- bility in species richness, although the initial slope of the hardwood curve was slightly steeper because a greater number of rare species were found in hardwood plots than in spruce plots.

Shannon-Wiener diversity (H'), based on either species frequency or sporocarp density, was greater for hardwood plots than for spruce plots, because of the greater number of species and the greater equitability among species (Table 4). Species equitability was greater in the hardwood plots than in the spruce plots because of the large number of rare species among hardwoods. The dominance -diversity curve (Greig- Smith 1983) confirmed that a high proportion of the species appeared rarely and the equitability was greater among the hardwood species (Fig. 2). The proportion of the quadrats with no species was much higher in the hardwoods (59%) than in the spruce (15%), as shown in Table 5.

Ordination of plots based on fungal percent frequency clearly separated the hardwood plots from the spruce plots

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TABLE 2. Basal areas (square metres per hectare) of tree species

Plots*

Spruce Hardwood

Tree speciest 7 2 8 1 0 9 1 6 5 1 1 1 2 4 3

Picea rubens Acer saccharurn Fagus grandifolia Prunus serotina Quercus rubra Fraxinus arnericana Betula alleghaniensis Acer rubrurn Acerpensylvanicurn - - - - - - - - - <1 <1 - Prunuspensylvanicurn - - - - - - - - - - - <1 Sorbus arnericana - < 1 - - - - Ilex rnontana < 1 - - - - - p u p - - -

NOTE: Ordination of the species and plots by principal-component analysis (Gauch 1982). -, absence of the species.

*I6 x 16 m. tVascular plant nomenclature follows that of Strausbaugh and Core (1978).

because of the taxonomic discontinuity in fungal species be- tween the two forest types (Table 3). Ordination also indicated greater similarity in fungal composition among the spruce plots than among the hardwood plots (Bills 1985). The spruce plots were more uniform in fungal composition: nine fungal species were common to all spruce plots; only two species were com- mon to all hardwood plots (Table 3). Moreover, the standard deviation and range of the number of species per plot was greater among the hardwood plots than among the spruce plots (Table 4).

Abundance Sporocarp density ranged from 319 to 19108 sporocarps

ha-'. year-' in the spruce plots compared with 352 to 2129 sporocarps . ha-' . year-' in the hardwood plots. Over the 3-year sampling period, 85% of the spruce quadrats and 41 % of the hardwood quadrats were occupied by ectomycon-hizal species. The major species listed in Table 6 accounted for 88% of the frequency and 96% of the sporocarp density of all species in spruce plots. Those listed in Table 7 accounted for 66% of the frequency and 75% of the sporocarp density of all species in hardwood plots.

Year to year variation For most species, frequencies and densities were highest

during the 2nd year, and lowest during the 3rd year (Tables 6 and 7; Fig. 3). Some species did not fruit every year, espe- cially in the 3rd year (Tables 6 and 7; Fig. 4). The species which exhibited the greatest frequency or sporocarp density were not the same every year. Because of the severe drought during July and August of 1983 (Table l) , species frequencies and sporocarp densities were, in general, much higher in all 12 plots during 1981 and 1982 than during 1983 (Tables 6 and 7; Fig. 3).

during the 1st and 3rd years, sporocarp density declined sharply after the first of August because of late-summer drought. Both forest types exhibited a strong peak of sporo- carp density in early September of the second season. Heavy rainfall in late August appeared to be necessary for dense late-summer fruiting. In the abundant 1982 season, sporocarp production peaked in late August and early September for most species, while for a few species, e.g., Amanita jlavoconia Boletus badius, Russula granulata, and Russula krombholzii, the peak occurred earlier (Fig. 4).

Length of sampling period Seventeen (47 %) of the species in the hardwood plots and 15

(56%) of the species in the spruce plots were found in 1981. If only 1982, the year with the greatest density and frequency, had been observed, 30 (89%) of the hardwood species and 24 (89%) of the spruce species would have been found. Only 12 (33%) of the total species in the hardwood plots and 7 (26%) of the total species in the spruce plots were found in 1983. No additional species were found during 1983. Limited observa- tions of the plots during 1984 yielded one sporocarp of an indeterminate Russula that had not been found in 198 1 - 1983.

Discussion Several of the species found in the spruce plots had been

described earlier in the mycological literature as fruiting under "spruce," presumably red spruce, in eastern North America. These species include Amanita jlavoconia (Hesler 1960), Boletus badius (Snell and Dick 1970), Tylopilus felleus (Snell and Dick 1970), Luctarius deceptivus (Hesler 1945; Hesler and Smith 1979), L. oculatus (Burlingham 1908), L. sordidus (Burlingham 1908; as Lactaria turpis (Weinm.) Fr.), L. vina- ceorufescens (Burlingham 1908; as Luctaria theiogala (Bull.) Fr.), Russula granulata (Single 1957; Bills 1984), and Russula

Fruiting phenology clarojlava ( ~ d l s and Miller 1984). Luctarius lignyotellus was For both forest types, the fruiting season for ectomycon-hizal described from a red spruce forest in Tennessee (Hesler and

fungi began in early July and extended into late September or Smith 1979) and has not been reported elsewhere. The remain- early October. (Fig. 3). The end of the first two fruiting sea- der of the species in the spruce plots have apparently never sons coincided with the advent of heavy frosts or snowfall. In been reported fruiting in association with red spruce. the 3rd year, prolonged drought in combination with cold A high proportion of the species diversity in both the spruce weather ended the fruiting season prematurely. In both forests and hardwoods was attributable to species of the Russulaceae.

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TABLE 3. Percentage of quadrats* occupied by ectomycorrhizal-basidiomycete species? (percent frequency)

Plots$

Spmce Hardwood

Basidiomycete species 9 2 8 7 1 1 0 1 1 1 2 3 4 6 5

Lactarius oculatus (Pk.) Burl. Clavulina cristata (Fr.) Schroet. Boletus badius Fr. Lactarius vinaceorufescens Smith Amanita jlavaconia Atk. Lactarius lignyotellus Smith & Hesl. Inocybe umbrina Bres. Lactarius sordidus Pk. Amanita inaurata Secr. [=A. cecilae

(B. & Br.) Bas] Russula granulata (Pk.) Pk. Amanita filva (Schaeff.) Pers. Russula silvicola Shaffer Russula aquosa LeClair Cortinarius sp. 1 Lactarius deceptivus Pk. Cortinarius paleacus Fr. Lactarius camphoratus (Fr.) Fr. Cystodem amianthinum (Fr.) Fayod Cantharellus tubaeformis Fr. Entoloma sp. 2 Laccaria laccata (Scop.) Berk. &

Bres., sensu lato Tylopilus felleus (Fr.) Karst. Russula densifolia Secr., sensu Shaffer Lactarius gerardii Pk. Paxillus involutus (Batsch.) Fr. Cortinarius sp. 3 Russula clarojlava Grove Russula heterophylla (Fr.) Fr. ? Lactarius griseus Pk. Russula subfoetens Smith ? Amanita strangulata Fr., sensu Bres. Boletus afinis Pk. ? Entoloma sp. 1 Hygrophorus sp Russula crustosa Pk. Hygrophorus punecius (Fr ) Fr. Russula virescens (Schaeff.) Fr. Russula operta Burl. Entoloma murraii (B. & C ) Sacc. Amanita vaginata (Bull.) Vitt. Hygrophorus jlavescens

(Kauff.) Smith & Hesl. Russula redolens Burl. Hygrophorus psittacinus (Fr.) Fr. Lactarius thejogalus (Bull.) Fr. Entoloma salmoneum (Pk.) Sacc. Phylloporus rhodoxanthus (Schw .) Bres. Inocybe sp. Entoloma lagenicystis Hesl. Boletus chrysenteron Fr. Russula krombholzii Shaffer Sclerodem citrinum Pers. Hygrophorus cantharellus (Schw.) Fr. Lactarius cinereus Pk. Boletinellus merulioides (Schw .) Mumll

NOTE: Ordination of the species and plots by principal component analysis (Gauch 1982). -, absence of the species. *2 x 2 m contiguous quadrats, 64 quadmtslplot. '(Criteria for including species are explained under Materials and methods. $16 x 16 m plots.

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764 CAN. 1. BOT. VOL. 64, 1986

TABLE 4. Basidiomycete-species richness and diversity in spruce versus mixed hardwood

stands

Forest type

Spruce Hardwood

No. of plots sampled (n) No. of species Specieslplot

Maximum Minimum Mean SD

Diversity (HI)*** Frequency Density

NOTE: ', not significantly different, P > 0.10; ", signifi- cantly different, 0.05 < P < 0.10; "*, Shannon-Wiener index H' based on species frequency and on sporocarp density.

AREA, M?

FIG. 1. Species-area curve for spruce ( A ) and hardwood (@) plots. The total number of species in the sample areas was plotted against increasing areas of contiguous quadrats. When 256 m2, the size of one contiguous plot, was reached, additional plots were chosen randomly and their species added.

This might be the case in many boreal or temperate forests dominated by ectomycorrhizal trees. Certain genera of ecto- mycorrhizal Basidiomycetes commonly found in other conifer- ous forests were absent from the red spruce forests, including species of Tricholoma, Hygrophorus (sections Hygrophorus, Camarophyllus) , Gomphidius, Chroogomphus, and Suillus.

Many of the species of the hardwood plots are common to the deciduous forests of northeastern North America (Miller 1973). Entoloma lagenicystis is known only from North Carolina and Tennessee (Hesler 1967). Prior to this study, Russula redolens was known only from the type locality in Vermont (Bills 1984). Russula operta (? = R. pusilla Pk.) is a poorly known species described from northern hardwood forests of Vermont. A few of the species from our hardwood stands have been reported to be associated with specific woody hosts, e.g., Boletinellus merulioides with Fraxinus spp. (Snell and Dick 1970; Cotter and Miller 1985; Cotter and Bills 1985), Lactarius cinereus with Fagus grandifolia, and Lactarius thejogalus with Betula spp. (Hesler and Smith

TABLE 5. Distribution of the number of specieslquadrat

No. of quadrats No. of

specieslquadrat Spruce Hardwood

0 1 2 3 4 5 6 7

Total Total occupied Mean SD

SPECIES SEOUENCE

FIG. 2. Dominance-diversity curve for spruce (0) and hardwood ( W ) plots. Most frequent species to least frequent species are ordered from left to right.

1979). Scleroderma citrinum, which fruits in association with many woody plants, consistently produced sporocarps near Quercus rubra. Laccaria laccata, Lactarius camphoratus, and Russula granulata had the widest amplitudes in habitat of any of the major species, and all three were found fruiting in most plots.

Direct comparison of the results of different studies are diffi- cult to interpret, because of difference in stand composition, age, climate, and so forth. Nonetheless, the numbers of spe- cies found in spruce (27) and hardwoods (35) are compatible with numbers reported by other investigators. Hora (1959) reported 25 species and Richardson (1970) reported 12 species belonging to ectomycorrhizal families fruiting in Scots pine plantations. Fogel (1976) found 24 ectomycorrhizal hypo- geous fungi in a Douglas-fir stand. A Swedish stand of Nor- way spruce had 25 species fruiting (Wkterlund and Ingelog 1981). Stands of Quercus and Quercus-Fraxinus in Great Britain produced 4 to 11 species (Hering 1966). In addition, the numbers of epigeous species fruiting in various spruce stands is comparable to the number of types of ectomycorrhi- zae observed on spruce. Wojciechowska (1960) described 16 "form genera" of ectomycorrhizae on Norway spruce within its northern range in Poland. Thirty-seven "form genera" of ectomycorrhizae were observed throughout the range of Nor-

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,*04 HARDWOOD

TABLE 6. Year to year variation in abundance of major* ectomycorrhizal -basidiomy- cete species in spruce plots

Yearly % Yearly density frequency (sporocarpslha)

% Species frequency 1981 1982 1983 1981 1982 1983

Lactarius oculatus Clavulina cristata Boletus badius Lactarius vinaceorufescens Amanita flavoconia Lactarius lignyotellus Inocybe umbrina Russula granulata Amanita inaurata Lactarius camphoratus

*The 10 most frequent species.

TABLE 7. Year to year variation in abundance of major* ectomycorrhizal-basidiomy- cete species in hardwood plots

Yearly % Yearly density frequency (sporocarpslha)

% Species frequency 1981 1982 1983 1981 1982 1983

Lactarius camphoratus Russula granulata Boletinellus merulioides Sclerodenna citrinum Laccaria laccata Russula krombholzii Hygrophorus cantharellus Lactarius thejogalus Lactarius cinereus Boletus chrysenteron

*The 10 most frequent species

JUL. A& SEP. OCT. DATE

FIG 3. Spomcarp phenology of all species in hardwood and spruce plots during 1981 (A) , 1982 ( 0 - l ), 1983 ( 0 . . 0 ) . Note differ- ences in magnitudes of y-axes.

way spruce in Poland (Dominik 1961). Thomas et al. (1983) observed 25 types of ectomycorrhizae in 1-year-old Sitka spruce plantations.

Some doubt exists as to whether the concept of minimal area can be applied to fungal communities (Christensen 1981). An adequate species -area curve for macrofungi cannot be deter- mined at a single point in time. The species -area curves de- rived from retrospective examination of our frequency data resembles Christensen's (1981) species-isolates curves for soil fungi. In her studies, repeated isolations of soil fungi within one plant community continued to yield additional spe- cies with no tendency for the species-area curve to level off. Fogel (1976) determined the minimal sampling area for hypo- geous fungi in a Douglas-fir stand during peak sporocarp pro- duction to be 100 m2. Amolds (1981) concluded that fungal species numbers continued to increase in grasslands at plot sizes up to 400 m2 and that a plot size of 1000 m2 may be necessary to ensure an adequate sample size.

The number of ectomycorrhizal species fruiting in a small area might reflect the minimal number of available niches in the rhizosphere, but few estimates of ectomycorrhizal species density in small (< 10 m2) areas are available. Several species of ectomycorrhizal fungi can occupy a very small root surface area, and up to seven ectomycorrhizal fungi have been isolated from a single 4-year-old Pinus elliottii tree (Zak and Marx 1964). Deacon et al. (1983) reported at least five types of ectomycorrhizae occurring within a 7 m radius of a young birch. These estimates of species density are within the range

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210-1

Lactarlus ocularus

spruce 150-

90-

30-

...

Clavulcna cristara

- t - -A- - - -L_- 4

35-

Lactarius l lgnyoteilus spruce

2 5

15-

/I

. 'A

I I I I I I

4 0-

lnocybe u m b r l n a

spruce

(a . .a). Note

of the maximum of seven species of fungi fruiting in a single 2 X 2 m quadrat reported here.

Sporocarp densities in our spruce plots (319 to 19 108 sporocarps . ha-' . year-'), were within the range of sporocarp densities of ectomycorrhizal fungi in other coniferous forests. Richardson's (1970) estimates ranged from 8 750 to 20 250 sporocarps . ha-' year-', and Fogal's (1976) estimates ranged from 11 052 to 16 753 sporocarps . ha-' . year-'.

An impression of the overall pattern of fruiting phenology is difficult to gain from 3 years of data. The late summer drought of 1981 and 1983 contributed to the high variation in pheno- logy. The 1982 season had adequate rainfall during July and August and presented a phenological pattern similar to those

described for other temperate and boreal plant communities (Wilkins and Hams 1946; Lange 1948; Richardson 1970; Petersen 1977). All these studies show the typical strong peak of productivity near the end of the season.

Although only one additional species was found after the 3rd year, it is difficult to judge how many additional species would have been found had more years been sampled. Fogal (1976) sampled 98 % of the hypothetical number of hypogeous species of a Douglas-fir forest in a 3-year period. Arnolds (1981, 1982) observed most of his grassland sites for 3 years but observed some selected sites for up to 6 years. Based upon these 6-year observation periods, he concluded that 3 years of sampling yielded 75 -92 % of the total species. However, dur-

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ing these extended sampling periods, the vegetation of the grasslands changed significantly, which may have contributed to subsequent additions to the mycoflora. Lange (1978) recorded 266 mycorrhizal species in a series of vegetation types over a 10-year period in Denmark. During any given season, 2 1-59 % of these species were observed to fruit.

The frequency of species in contiguous quadrats is well es- tablished in plant ecology as a measure of the abundance of organisms lacking clearly delimited individuals. The addi- tional challenge mycologists face is that the bulk of the fungal organism, th; thallus, invisible in the undisturbed natural habitat. However, the presence of the sporocarp indicates the presence of the thallus. Hence, the frequency of quadrats con- taining sporocarps is an estimate, albeit usually an underesti- mate, of the frequency of quadrats containing the species. If the quadrats were observed often enough, the observed species frequency would be close to the unknown actual frequency. ~ndeed, as the intensity (in time) of sampling increased, spe- cies frequency would be expected to increase at an ever decreasing rate and eventually approach the unknown actual frequency. Moreover, if the quadrats were small enough rela- tive to the size of the organism, percent frequency could be taken as a measure of ubiquity. This is the way "cover" is used in plant ecology. To determine how often the quadrats should be observed, gnd how small they should be, willrequire further imaginative research along the lines of Cotter and Bills (1985).

Sporocarp density, on the other hand, is a measure of sporo- carp abundance, which is not the same as species abundance. The data of Tables 6 and 7 illustrate this point in two ways. First, comparison of species frequency and sporocarp density indicates that the list of major species would be somewhat different if species were ranked by density. For example, the sporocarp density of Clavulina cristata was greater than that of hctarius oculatus, but L. oculatus had a higher frequency, i.e., it fruited in more quadrats and therefore was more ubiqui- tous in the spruce plots. Second, there is a great deal of varia- tion in the ratio of sporocarp density to species frequency, i.e., the density of sporocarps in occupied quadrats: Arbitrarily taking the first three species in Table 6 as an example, we find, in occupied quadrats over the 3-year period, 8491 Lactarius oculatus sp&ocarps/ha, 3 1 802 ~ l ~ v u l i n a cristata sporo- carpstha, and 3943 Boletus badius sporocarpstha. This gross variation from species to species in the "intensity of fruiting" diminishes the applicability of sporocarp density in compara- tive studies.

In summary, this study provides base-line data on the abun- dance, diversity, phenology , and year to year variation of ecto- mycorrhizal fungi fruiting in homogeneous red spruce stands and in heterogeneous northern hardwood stands- The fungal species composition, frequency, and sporocarp density of the two forkst types differed as would be expected in light of the symbiotic nature of the fungi and plants considered. Fungal species richness, equitability, and diversity were greater in the mixed-hardwood plots, which hosted many rare fungal spe- cies, than in the single-species coniferous plots, which were

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dominated by a few ubiquitous species. The results suggest that species frequency in small con-

tiguous quadrats might be more appropriate than sporocarp density for comparison of the relative activity or ubiquity of fungal species in plot studies. Interplot similarities and differ- ences in fungal species composition were quantified objec- tively by principal-component analysis of species frequencies.

This is one of many ordination techniques that can be used in future studies of the response of fungal communities to vegeta- tional or environmental gradients, and for describing fungal community structure in complex vegetation landscapes.

Acknowledgements We thank the personnel of the U.S. Forest Service, Gauley

and Marlington Ranger Districts, Monongahela National Forest, for their cooperation, and Dr. W. Carter Johnson for advice regarding data analysis and the manuscript. We also thank several members of the Virginia Polytechnic Institute and State University mycology lab who assisted with data col- lection and made comments on the manuscript. Finally, two anonymous referees were extremely helpful.

ARNOLDS, E. 1981. Ecology and coenology of macrofungi in grass- lands and moist heathlands in Drenthe, the Netherlands. Part 1. Introduction and synecology. Bibl. Mycol. 83: 1 -407.

1982 Ecology and coenology of macrofungi in grasslands and moist heathlands in Drenthe, the Netherlands. Part 2. Auto- ecology. Part 3. Taxonomy. Bibl. Mycol. 90: 1-501.

BILLS, G. F. 1984. Southern Appalachian Russulas. 11. Mycotaxon, 21: 491-517.

1985. Ecological and taxonomic studies of the Russulaceae and other ectomycorrhizal Basidiomycetes in the high-elevation forests of the Southern Appalachians. Ph.D. dissertation, Virginia Polytechnic Institute and State University, Blacksburg, VA.

BILLS, G. F., and 0. K. MILLER, JR. 1984. Southern Appalachian Russulas. I. Mycologia, 76: 975 - 1002.

BURLINGHAM, G. S. 1908. A study of the Lactariae of the United States Mem. Torrey Bot. Club, 14: 1 - 109.

CHRISTENSEN, M. 1981. Species diversity and dominance in fungal communities. In The fungal community. Edited by D. T. Wicklow and G. C. Carroll. Marcel1 Dekker, Inc., New York. pp. 201 -232.

COTTER, H. V. T., and G. F. BILLS. 1985. Comparison of spatial patterns of sexual and vegetative states of Boletinellus merulioides. Trans. Br. Mycol. Soc. 85(3): 520-524.

COTTER, H. V. T., and 0 . K. MILLER, JR. 1985. Sclerotia of Boleti- nellus merulioides in nature. Mycologia, 77(6): 927-931.

DEACON, J. W., S. J. DONALDSON, and F. T. LAST. 1983. Sequences and interactions of mycorrhizal fungi on birch. Plant Soil, 71: 257-262.

DOMINIK, T. 1961. Studium nad mikotrofizmem swierka pospolitego - Pice excelsa (Lam.) Lk. w Polsce. Inst. Bad. Lesn. Pr. 1961, 209: 1-24.

EDENS, D. L. 1973. The ecology and succession of Cranberry Glades, West Virginia. Ph.D. dissertation, North Carolina State University, Raleigh.

FOGEL, R. 1976. Ecological studies of hypogeous fungi. 11. Sporo- carp phenology in a western Oregon Do~glas-Fir stand. Can. J. Bot. 54: 1152-1162.

GAUCH, H. G. 1982. Multivariate analysis in community ecology. Cambridge University Press, New York.

GREIG-SMITH, P. 1983. Quantitative plant ecology. 3rd. ed. Univer- sity of California Press, Los Angeles.

HERING, T. F. 1966. The tenicolous higher fungi of four Lake Dis- trict woodlands Trans. Br. Mycol. Soc. 49: 369-383.

HESLER, L. R. 1945. Notes on Southern Appalachian fungi. VII. J. Tenn. Acad Sci. 20: 363-372.

1960. Mushrooms of the Great Smokies. University of Tennessee Press, Knoxville.

1967. The genus Entolorna in southeastern North America. Beih. Nova Hedwidgia, 23: 1 - 196.

HESLER, L. R., and A. H. SMITH. 1979. North American species of Luctarius. University of Michigan Press, Ann Arbor.

HORA, F. B. 1959. Quantitative experiments on toadstool production in woods. Trans. Br. Mycol. Soc. 42: 1-15.

Can

. J. B

ot. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y M

ount

Roy

al U

nive

rsity

on

05/2

1/13

For

pers

onal

use

onl

y.

768 CAN. I. BOT. VOL. 64, 1986

LAIHO, 0. 1970. Parillus involutus as a mycorrhizal symbiont of forest trees. Acta For. Fenn. 106: 1-72.

LANCE, M. 1948. The agarics of Maglemose. Dan. Bot. Ark. 13: 1-141.

1978. Fungus flora in August, ten years observations in a Danish beech wood district. Bot. Tidsskr. 73: 21 -54

MENGE, J. A., and L. F. GRAND. 1978. Effect of fertilization on production of epigeous basidiocarps by mycorrhizal fungi in loblolly pine plantations. Can. J. Bot. 56: 2357-2362.

MILLER, 0. K., JR. 1973. Mushrooms of North America. 2nd ed. E. P. Dutton, New York.

1983. Ectomycorrhizae in the Agaricales and Gasteromy - cetes. Can. J Bot. 61: 909-916.

NEWELL, K. 1984. Interaction between two decomposer Basidiomy- cetes and a collembolan under Sitka spruce: distribution, abun- dance and selective grazing. Soil Biol. Biochem. 16: 227-233.

PETERSEN, P. M. 1977. Investigations on the ecology and phenology of the macromycetes in the arctic. Medd. Groen. 199: 1-72.

PIELOU, E. C 1977. Mathematical ecology. Wiley, New York. RICHARDSON, M. J. 1970. Studies on Russula emetica and other

agarics in a Scots pine plantation. Trans. Br. Mycol. Soc. 55: 217-229.

RIFFLE, J. W. 1973. Pure culture synthesis of ectomycorrhizae on Pinus ponderosa with species of Amanita, Suillus, and Lactarius. For. Sci. 19: 242-250.

SHANNON, C. E., and W. WEAVER. 1949. The mathematical theory of communication. University of Illinois Press, Urbana.

SINGER, R. 1957. New and interesting species of Basidiomycetes. V. Sydowia Ann. Mycol. 11: 141-272.

SNELL, W. H., and E. A. DICK. 1970. The Boleti of Northeastern North America. J. Cramer, Lehre, Federal Republic of Germany.

STRAUSBAUGH, P. D., and E. L. CORE. 1978. The flora of West Virginia. 2nd ed. Seneca Books, Inc., Grantsville.

THOMAS, G. W., D. ROGERS, and R. M. JACKSON. 1983. Changes in the mycorrhizal status of Sitka spruce following outplanting. Plant Soil, 71: 319-323.

WASTERLUND, I., and T. INGELOG. 1981. Fruit body production in some young Swedish forests with special reference to logging waste. For. Ecol. Manage. 3: 269-294.

WATLING, R. 1982. Taxonomic status and ecological identity in the Basidiomycetes. In Decomposer Basidiomycetes: their biology and ecology. Edited by J. C. Frankland, J. N. Hedger, and M. J. Swift. Cambridge University Press, Cambridge. pp. 1-32.

WILKINS, W. H., and G. C. M. HARRIS. 1946. The ecology of larger fungi. V. An investigation in the influence of rainfall and tempera- ture on the seasonal production of fungi in beechwood and pinewood. Ann. Appl. Biol. 33: 179-188.

WOJCIECHOWSKA, H. 1960. Studies on the mycotrophy of the spruce (Picea excelsa Lk.) in its northern range with particular regard to the mycotrophy of plant communities in the Forest District Sad- lowo, Subdistrict Lipowo near Biskupiec Reszilski. Folia For. Pol. Ser. A. Lesn. 2: 123 - 166. (Translated from Polish.)

ZAK, B., and D. H. MARX. 1964. Isolation of mycorrhizal fungi from roots of individual slash pines. For. Sci. 10: 214-221.

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