ectomycorrhizal sporocarp succession and production during early primary succession on mount fuji

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Research

Blackwell Publishing Ltd.

Ectomycorrhizal sporocarp succession and production

during early primary succession on Mount Fuji

Kazuhide Nara, Hironobu Nakaya and Taizo Hogetsu

Asian Natural Environmental Science Center, The University of Tokyo, 1-1-8 Midori-cho, NishiTokyo, Tokyo 188-0002, Japan

Summary

• The species composition, succession and biomass production of ectomycorrhizal(ECM) sporocarps were studied during early primary succession on Mount Fuji,Japan, with special reference to developmental stages and the growth of associatedhosts.• Weekly sporocarp surveys were conducted over 2 yr on a volcanic desert, wherethe total vegetation coverage was about 5%. We also quantified the growth of asso-ciated hosts in terms of size, photosynthesis, and leaf N and P concentration.• A total of 11 450 sporocarps of 23 species were recorded. They were associatedalmost exclusively with an alpine dwarf willow,

Salix reinii

. Two

Laccaria

and one

Inocybe

species were the first colonizers; subsequent fungal species were addedas the host grew. There was no evidence of any fungus disappearing and beingreplaced in the sere of ECM fungal succession.• The biomass production of ECM sporocarps was exceptionally large, in general,and amounted to 19% of leaf biomass in the most productive associations. AnnualECM sporocarp production in individual ECM associations was strongly correlatedwith the growth of the associated host, especially with the photosynthetic rate,which appeared to be determined by leaf N and P concentration.

Key words:

ectomycorrhizal fungi (ECM), early primary succession, volcanic desert,fungal succession, alpine dwarf willow (

Salix reinii

), photosynthesis, sporocarpproduction, leaf N concentration.

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Author for correspondence:

Kazuhide Nara

Tel: +81 424 655601

Fax: +81 424 655601

Email: [email protected]

Received:

29 August 2002

Accepted:

22 November 2002

doi: 10.1046/j.1469-8137.2003.00724.x

Introduction

The succession of vegetation is an important concept interrestrial ecology. Many studies, using a variety ofapproaches, have been conducted worldwide but, until a fewdecades ago, most studies had neglected the existence ofmycorrhizal fungi. With increasing awareness of theimportance of mycorrhizal functions in nutrient and wateruptake, the effects of mycorrhizal fungi on vegetationsuccession began to be studied (Miller, 1979; Reeves

et al

.,1979). The majority of these studies targeted herbaceousplant species in combination with vesicular–arbuscularmycorrhiza (VA) mycorrhizal fungi. A basic model of earlyprimary succession has been developed to demonstrate thatnonmycotrophic plants are followed by mycotrophic plants,and that succession is driven, in the main, by the invasion ofVA mycorrhizal fungi, facilitating nutrient and water uptake(e.g. Allen & Allen, 1984).

Ectomycorrhizal (ECM) host plants are typically observednot only in climax forests but also during early primarysuccession (Allen

et al

., 1992; Helm & Allen, 1995). Becauseavailable nutrients such as nitrogen (N) and phosphorus (P)are quite limited at this stage, symbiosis with ECM fungi issupposed to be advantageous for the survival and growth ofhost plants, as in the case of VA mycorrhizal fungi. Species ofECM fungi are quite diverse and vary in host range. Further-more, different ECM fungi have different effects on a hostspecies. To evaluate the effects of ECM fungi on host growthand competition during early primary succession, it is impor-tant to determine the existing ECM species or communitiesat this stage.

As many ECM fungi produce conspicuous sporocarps,sporocarp production has been studied in a variety of foreststo obtain information about existing ECM fungal species.Several researchers have studied ECM sporocarp commun-ities during early primary succession. Allen

et al

. (1992) noted


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that no ECM sporocarps were observed until 10 yr after theeruption of Mount St Helens, although some ECM treespecies had already invaded. Glacier fronts are another areawhere primary succession occurs. Helm

et al

. (1996) notedthat species of

Inocybe

,

Laccaria

and

Hebeloma

were the mostcommon sporocarps associated with host species of Salicaceaein early successional stages at Exit Glacier (Alaska, USA).Jumpponen

et al

. (1999, 2002) reported the presence of 13ECM sporocarps at the front of Lyman Glacier (Washington,USA). Because none of these studies have quantitative descrip-tions, more detailed investigations are needed to understandthe ECM sporocarp communities in early primary succes-sional sites.

The ECM sporocarp community associated with a pioneerhost species can be assumed to change along with the host asit ages and develops, even in the early stages of primary suc-cession. Models of ECM sporocarp succession correspondingto tree growth were developed from investigations in temper-ate forests and plantations, particularly for fungi in associationwith

Betula

,

Picea

and

Pinus

(Mason

et al

., 1982, 1983;Deacon

et al

., 1983; Fleming, 1983; Fleming

et al

., 1984;Last

et al

., 1984; Dighton

et al

., 1986). The models includedthe initial appearance of ‘early stage fungi’, the subsequentappearance of ‘late-stage fungi’ and aspects of soil develop-ment, such as the increase of organic matter and N content,which is supposed to greatly affect the sporocarp succession.However, most of ECM sporocarp succession studies havebeen conducted in secondary successional sites where soils aremore or less already developed.

Succession of ECM sporocarps in primary succession hasbeen reported in only a few studies. Jumpponen

et al

. (1999,2002) noted that ECM sporocarp succession at the retreatingglacier followed the early to late-stage model, and that fungalspecies increased with host vegetation development. In thesestudies, sporocarp production was quite rare and insufficientas a basis for discussion of the sere of ECM sporocarp com-munities. The succession of ECM sporocarps after volcaniceruptions has not yet been studied during early primarysuccession. To construct a successional model for ECMsporocarps during early primary succession, further intensivestudy in more appropriate sites is needed.

The relationship between host growth and ECM sporocarpproduction gives some indication of the role of ECM associ-ations in nature, and has been illustrated in several studies.Defoliation or tree girdling, which reduces the supply ofassimilates underground, decreases sporocarp production ofECM fungi (Last

et al

., 1979; Högberg

et al

., 2001). Thus,host growth activities, such as photosynthesis, are assumed tohave a great impact on sporocarp production. Hendrix

et al

.(1985) noted that transplanted loblolly pines that producesporocarps of

Pisolithus

are twice the height and diameter ofthose not associated with sporocarps. Host growth might becorrelated with production of the associated sporocarps. Therelationship between ECM sporocarp production and the

growth of an individual host has never been studied duringearly primary succession. Scattered vegetation patches, whichare usually observed in early successional sites, enable us toidentify easily an individual host associated with each ECMsporocarp. At such sites, we can investigate the relationshipbetween sporocarp production and host growth in individualassociations. These investigations may improve our know-ledge of ECM associations in nature.

In the present study, we investigated the sporocarp produc-tion of ECM fungi in a volcanic desert on Mt Fuji, Japan,where the vegetation is still in the early stage of primarysuccession. We quantitatively described the sporocarp compo-sition at this site and proposed a model of ECM sporocarpsuccession in an early primary successional site. Host treegrowth parameters such as leaf biomass, photosynthesis andleaf nutrient concentrations were also quantified to determinethe relationship between host growth and the production ofthe associated sporocarps. The significance of ECM symbiosesin the early stage of primary succession is discussed.

Materials and Methods

Research site

Mount Fuji, the highest and most famous mountain in Japan,erupted in 1707, and its south-eastern side was completelycovered with scoria (i.e. tephra, typically 2–30 mm indiameter), up to 10 m deep. The existing vegetation wascompletely destroyed, and is now recovering. While the treeline is generally located at 2500 m above sea level on the othersides of the mountain, it is located at around 1300 m onthe south-eastern side and continues to rise after 300 yr ofvegetation recovery (Fig. 1). Our research site is locatedbetween 1500 m and 1600 m above sea level (35

°

20

′

N,138

°

48

′

E), and is in the upper montane zone or the lowersubalpine zone. Vegetation in this area is patchily distributed,and the total vegetation coverage is approximately 5%,indicating the early stages of primary succession. Severalperennial herbs belonging to Polygonaceae, Asteraceae andBrassicaceae were the first colonizers because of their abilityto adapt to the unstable scoria surface (Masuzawa, 1997).

Polygonum cuspidatum

plays an important role in subsequentvegetation succession. This species forms large patches, up to10 m in diameter, by vegetative and sexual reproduction, thusproviding stable habitats for subsequent plant species on theunstable scoria desert (Adachi

et al

., 1996). Many pioneerherbaceous and woody species grow in these patches. Weestablished a research quadrat (100

×

550 m) for oursporocarp surveys.

At 1400 m above sea level on the south-eastern side ofMt Fuji, the annual mean air temperature is 8.6

°

C, and themonthly mean temperature ranges from

−

1.9

°

C in January to19.1

°

C in August (Tateno & Hirose, 1987). Mean annualprecipitation at Tarobo (altitude 1300 m on the same slope)

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is 4854 mm, which is considerably more than the 1650 mmthat falls at Kawaguchiko (northern foothills, altitude800 m). The high precipitation at Tarobo is mainly due to itslocation between the wet, warm air masses from the sea to thesouth and the cool air masses flowing down across the north-ern slope (Ohsawa, 1984). The soil at a depth of 5 cm remainsmoist throughout the fruiting seasons because of the highprecipitation and scoria substrates. More soil nutrients areavailable within the vegetation patches than on the bareground. With the development of the vegetation patches, theamount and forms of soil N have been changed dramaticallydue to bacterial activity and the N preferences of existingplants (Hirose & Tateno, 1984).

Vegetation

Within the research quadrat, 159 vegetation patches werelarger than 50 cm in diameter. These patches were mappedusing a survey laser instrument (Criterion 400; LaserTechnology, CO, USA) (Fig. 2). Many smaller patches of

Polygonum weyrichii

var.

alpinum

were distributed amongthe 159 vegetation patches, but they were excluded from thisstudy because their total coverage was small and no ECMassociations were observed during our preliminary study.Each vegetation patch that we investigated was numbered andthe plant species, and their coverage in each patch, wererecorded in August 2000. In order to identify the host speciesthat produced ECM sporocarps, plant species compositionwas compared between sporocarp-producing and non-producing patches. Five different root systems of each of the10 plant species that were predominant in coverage within

sporocarp-producing patches were collected and theirmycorrhizal formation was examined under a dissectingmicroscope.

Sporocarp survey

A total of 34 sporocarp surveys were conducted from May toNovember in 2000 and 2001. We surveyed weekly from lateJune to middle October in both years, because almost allECM sporocarps are produced in these seasons. Each surveycovered the entire quadrat, and required 1–3 d to complete.Each sporocarp was marked with a small flag to avoid doublecounting, and to record spatial distribution for future

Fig. 1 Location of the research site established in an area of early primary succession on Mount Fuji, Japan.

Fig. 2 The spatial distribution of vegetation patches in the quadrat with reference to ectomycorrhizal symbionts. Each circle represents a vegetation patch. Closed circles indicate vegetation patches containing Salix reinii. The patches in which ectomycorrhizal sporocarps were recorded in 2000 or 2001 are flagged. The occurrence of ectomycorrhizal sporocarps completely coincides with the presence of S. reinii in vegetation patches.


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research. Because most of the sporocarps were producedwithin or close to the vegetation patches, the number ofsporocarps of each species was summed to give a total for eachpatch during each survey. These figures were used to estimatethe annual sporocarp production of each patch.

The macroscopic characteristics of ECM sporocarps atvarious developmental stages were recorded, and specimensof all species were freeze-dried (FDU-540; EYELA, Tokyo,Japan) for microscopic observation, future DNA analysis anddeposition in a public museum. Microscopic characteristicswere observed using the procedure of Breitenbach andKränzlin (1991). The nomenclature generally followed Hansenand Knudsen (1992, 1997). Because there were no regionalmonographs of ECM fungal taxa in association with alpinedwarf willows in Japan, we used specific literature of otherregions and world monographs for the identification of thefollowing genera:

Cortinarius

(Brandrud

et al

. 1990–98),

Hebeloma

(Breitenbach & Kränzlin, 2000),

Inocybe

(Stangl,1989),

Laccaria

(Mueller, 1992),

Russula

(Sarnari, 1998),

Sclero-derma

(Guzman, 1970) and

Leccinum

(Lannoy & Estades,1995). Species belonging to Entolomataceae were excludedfrom the present study because their ECM status at the researchsite was uncertain and some species appeared to be saprophytic.

The mean dry weight of sporocarps of each species wasdetermined from 20 fully developed sporocarps, or from allsporocarps for those species with less than 20 sporocarps. Themean dry weight was multiplied by the number of sporocarpsto calculate the biomass production of each species.

Quantification of

Salix reinii

status

The area covered by

S

.

reinii

was a parameter of its size andconsidered to be a good index of its developmental stage inour research site (Lian

et al

., 2003). Thus, the cover of

S. reinii

in each vegetation patch was measured with a digital plani-meter on photographs that were taken from 7 m above thepatch, and used as an index of host size.

To investigate the relationship between sporocarp produc-tion and host growth, nine patches with similar amounts of

S. reinii

cover were selected. The whole-leaf biomass of

S. reinii

in each of the nine patches was estimated from the dry weightof leaves harvested from a square (20

×

20 cm) in the centerof the

S. reinii

coverage, in October 2000. We also randomlysampled five current-year shoots from each of the nine patchesin November 2000, and recorded the length and number ofwinter buds for each shoot. To measure photosynthesis in

S. reinii

, we randomly chose five fully developed canopy leavesin each of the nine patches. The photosynthetic rate of eachleaf was measured on a fine day in August 2000 with a port-able photosynthesis system (LI-6400; LiCor, Lincoln, NE,USA). Fixed chamber conditions were used with saturatedlight (25

°

C, 400 p.p.m. CO

2

, 1500 µmol m

−

2

s

−

1

light inten-sity with a red and blue LED combination). The area and dryweight of each leaf were recorded after photosynthesis was

measured. The N and P concentrations of each leaf were thencolorimetrically determined after digestion with H

2

SO

4

andH

2

O

2

using the indophenol blue method and the ascorbicacid deoxidizing molybdenum blue method, respectively. InNovember 2000, six soil cubes (10

×

10

×

10 cm) weresampled from each patch, three from the periphery and threefrom the inside, and 200 root tips within each sample wererandomly collected. The rate of ECM formation (number ofmycorrhizal root tips/200 root tips

×

100) was determinedunder a dissecting microscope.

Statistics

The statistical analyses were performed with the SPSS 11.0software package (SPSS, Chicago, IL, USA) for Windows. Allregression relationships were fitted using a least-squaresregression, and their statistical significance was tested. Thedata on host parameters, such as current-year shoot length,winter bud number, photosynthesis, leaf N and Pconcentrations, and mycorrhizal formation are presented asmeans

±

SE. These data were tested for statistically significantdifferences among the nine selected patches by one-wayanalysis of variance, and Tukey’s multiple comparison testwas applied when appropriate. Spearman’s rank correlationcoefficients were used to evaluate the relationship between theECM sporocarp production and the host parameters.

Results

Host species

A total of 19 herbaceous plant species and eight tree specieswere confirmed in 159 vegetation patches in the researchquadrat (Table 1).

Polygonum cuspidatum

and the alpine

P

.

weyrichii

var

. alpinum

were observed in 155 and 104patches, respectively. Several species belonging to Rosaceaeand Cyperaceae were also found in many patches. Thefamilies, such as Polygonaceae, Rosaceae and Cyperaceae,have been described to have some ECM herbaceous speciesin other geographical areas (Massicotte

et al

., 1998). Any ofabove herbaceous species did not form ectomycorrhizae in ourresearch site (Table 1). Woody species were a relatively minorconstituent.

Salix reinii

and

Spiraea japonica

var.

alpina

wereobserved in 37 and 30 patches, respectively.

As a result of weekly sporocarp surveys over 2 yr, ECMsporocarps were found in 38 of the 159 patches (Fig. 2). Themost apparent difference in plant species compositionbetween the sporocarp-producing and nonproducing patcheswas in

S. reinii

(Table 1). Of 38 patches in which mycorrhizalsporocarps were recorded, 37 contained

S. reinii

. The remain-ing patch with mycorrhizal sporocarps had

Salix bakko

. Ofthe 10 major plant species that dominated the sporocarp-producing patches (Table 1), nine species did not have ecto-mycorrhizae;

S. reinii

was the exception.

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The area covered by S. reinii in each patch varied greatly,ranging from a several-year-old seedling of 0.016 m2 to largebushes over 50 m2. Although S. reinii was the exclusivelydominant host plant for ECM fungi in our early successionalsite, the total area covered by this species was only 502 m2, lessthan 1% of the whole quadrat.

The subsequent successional tree species, Betula ermaniiand Larix kaempferi, were observed on only four and threepatches, respectively. These species were minor constituentson the patches, and were always accompanied by S. reinii. Thetotal area covered by B. ermanii and L. kaempferi was 0.77 m2

and 0.85 m2, respectively.

Species composition of ECM sporocarps

The ECM sporocarps appeared between July and Novemberin both years. In total, 11 450 sporocarps of 23 species wererecorded over 2 yr (Table 2). The total sporocarp production in2001 was significantly lower than in 2000, probably becauseof the severe above-ground disturbance from avalanches andwindstorms that occurred in the winter between the twofruiting seasons.

Cortinariaceae was the most species-rich family, with 12species. Inocybe was the most species-rich genus, with sevenspecies, although some of them were quite rare. Hebeloma,Laccaria and Russula were the next species-rich genera; eachcontained three species. Boletus and Cantharellus were alsofound, but were rare. Leccinum was observed under thecoverage of B. ermanii surrounded by S. reinii.

Laccaria laccata was the most abundant species, pro-ducing 3955 (43% of the total) and 762 (34% of the total)sporocarps in 2000 and 2001, respectively. Although smallnumbers of its sporocarps were found throughout the fruitingseasons, there was a conspicuous production peak in summerof each year. In a single survey at the peak of 2000, the sporo-carp number of L. laccata exceeded 90% of the annual pro-duction. Sporocarps of Laccaria amethystina and Laccariamurina were also abundant, and their production peakswere quite similar to that of L. laccata. Cortinarius decipensand Hebeloma mesophaeum sporocarps were also majorspecies, and their production peaks were in late autumn.Inocybe lacera and Scleroderma bovista were major species thatdid not have prominent production peaks. A substantialnumber of their sporocarps were found continuously

Table 1 Plant communities in sporocarp-producing and nonproducing patches on the volcanic desert of Mount Fuji

SpeciesSporocarp-producingpatches (n = 38)

Sporocarp-nonproducingpatches (n = 121) Total (n = 159)

Woody speciesSalix reiniia 37 0 37Spiraea japonicaa 17 13 30Rosa fujisanensis 7 1 8Betula ermanii 4 0 4Larix kaempferi 3 0 3Ligustrum obtusifolium 1 1 2Salix bakko 1 0 1Weigela decora 1 0 1Herbaceous speciesPolygonum cuspidatuma 34 121 155Cirsium purpuratuma 31 89 120Arabis serrataa 30 83 113Polygonum weyrichii var. alpinuma 24 80 104Campanula punctata var. hondoensis 32 62 94Calamagrostis hakonensisa 29 59 88Picris hieracioides ssp. japonica 24 60 84Artemisia princeps 29 54 83Miscanthus olygostachyusa 30 52 82Aster ageratoides ssp. ovatusa 30 35 65Clematis stansa 22 20 42Anaphalis margaritacea 18 16 34Senecio nemorensis 15 18 33Angelica hakonensis 11 17 28Hedysarum vicioides 16 6 22Carex doenitzii 8 6 14Fragaria nipponica 1 1 2Artemisia pedunculosa 0 1 1Cirsium effusum 0 1 1

Figures indicate the number of patches in which each species appeared. aIndicates the 10 predominant species in sporocarp-producing patches; five root systems of each were investigated for mycorrhizal formation.

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throughout the fruiting seasons, from July to November, ofboth years.

The total biomass production of all ECM sporocarps in thequadrat amounted to 3089 g and 1563 g in 2000 and 2001,respectively. Among all ECM species, S. bovista dominatedthe dry weight. This species amounted to 2505 g (81% of thetotal) and 1430 g (92% of the total) dry weight for 2000 and2001, respectively (Table 2). In comparison, the other specieswere minor constituents in terms of dry weight.

Succession of ECM sporocarps with host development

The species composition of ECM sporocarps changedaccording to host size enlargement (Fig. 3). Inocybe laceraappeared in association with hosts whose size ranged from0.016 m2 to 154 m2. Sporocarps of L. laccata and L. amethy-stina were observed under hosts larger than 0.034 m2 and0.15 m2, respectively. There were six patches in which the areacovered by hosts was smaller than 0.5 m2. These small andyoung hosts had only one or two of the three ECM species,I. lacera, L. laccata and L. amethystina, and were not associatedwith other ECM fungal species. Thus, these three species werefirst-stage fungi that appear first on the sere of the ECMfungal succession during early primary succession on Mt Fuji.

The number of sporocarps on these first-stage fungi increasedmonotonically with the increase of host size (Fig. 4a–c).

Sporocarps of L. murina and S. bovista appeared first inassociation with larger hosts (> 0.6 m2) (Fig. 3), and usuallyin the area surrounding each vegetation patch. These fungiwere usually accompanied by members of the first-stage fungi,indicating that L. murina and S. bovista were second-stagefungi in the sere of the ECM fungal succession. The numberof sporocarps on these second-stage fungi also increasedmonotonically with host size development (Fig. 4d,e).

With further increases in host size, Hebeloma spp. (> 1.2 m2),Cortinarius spp. (> 2.1 m2), Russula spp. (> 2.4 m2) and Inoc-ybe sp. 4 (> 2.4 m2) appeared (Fig. 3). Sporocarps of thesespecies were always observed inside each vegetation patch,where organic materials accumulated. These fungi were usu-ally accompanied by the first- and second-stage fungi. Thus,species of Hebeloma, Cortinarius, Russula and Inocybe sp. 4were relatively late-stage fungi in the sere of the ECM fugalsuccession in our early successional site. The number ofsporocarps on these late-stage fungi also increased with hostsize development (Fig. 4f–h). As new fungal species joinedthe existing fungal communities, the number of ECM sporo-carp species increased along with host development (Fig. 5).Thirteen species were associated with the largest S. reinii.

Table 2 Ectomycorrhizal sporocarps recorded during early primary succession on Mount Fuji

species

2000 2001

Number Patch Dry weight (g) Number Patch Dry weight (g)

Boletus pulverulentus Opat. 1 1 0.58 0 0 0Boletus cf. rubellus Krombh. 18 6 18.99 10 2 10.55Cantharellus cibarius Fr. 5 1 0.26 0 0 0Cortinarius alboviolaceus (Pers. Fr.) Fr. 4 1 0.64 0 0 0Cortinarius decipens (Pers. Fr.) Fr. 472 14 18.36 15 4 0.58Hebeloma leucosarx Orton 27 2 14.87 15 3 8.26Hebeloma mesophaeum (Pers.) QuÈl. 1265 20 171.18 42 10 5.68Hebeloma pusillum Lange 23 4 1.95 7 1 0.59Inocybe acuta Boud. 1 1 0.23 0 0 0Inocybe calospora Quèl. a a a 60 1 1.72Inocybe dulcamara (Pers.) Kumm. 95 1 31.84 41 1 13.74Inocybe fastigiata (Schaeff.) Quèl. 0 0 0 1 1 0.14Inocybe lacera (Fr.) Kumm 435 25 14.49 171 16 5.69Inocybe sp. 1 a a a 10 1 0.15Inocybe sp. 2 31 8 0.74 28 4 0.67Laccaria amethystina Cooke 1214 21 125.91 412 13 42.73Laccaria laccata (Scop. Fr.) Berk. & Br. 3955 25 123.81 762 19 23.85Laccaria murina Imai 535 28 13.41 56 9 1.40Leccinum scabrum (Bull. Fr.) S.F. Gray 2 1 5.95 0 0 0Russula norvegica Reid 24 5 5.01 0 0 0Russula pectinatoides Peck 18 6 27.09 11 4 16.55Russula sororia (Fr.) Romell 14 6 8.67 0 0 0Scleroderma bovista Fr. 1063 22 2504.97 607 22 1430.40Total 9202 38 3088.93 2248 31 1562.72

Data in the Number and Dry weight columns indicate the total number and the total dry weight, respectively, of sporocarps of each species in the quadrat. Data in the Patch columns indicate the total number of patches in which each species was recorded. aInocybe calospora and Inocybe sp.1 were not distinguished from Inocybe lacera in 2000.


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ECM sporocarp production related to host growth

The biomass production of ECM sporocarps in each patchranged from 0.27 g to 1208 g dry weight over 2 yr, andincreased with host size (Fig. 6). In association with mid-sizedhosts (2–10 m2), however, sporocarp productivity variedgreatly; several ‘unproductive patches’ produced less than 1 gof sporocarp dry weight, and many ‘productive patches’produced more than 50 g.

To determine the possible causes of this large variation, wechose nine patches that had mid-sized hosts for further inves-tigation. The total dry weight of the ECM sporocarps in thenine selected patches ranged from 0.41 g to 264 g in 2000(Table 3).

No significant correlation between host size and sporocarpbiomass was observed in these nine patches (Table 3). Even inthe unproductive patches, a large part of the host root tipswere ectomycorrhizae. Their mycorrhizal formation rateswere not significantly different from those in productivepatches (Table 3).

In the most productive of the nine patches, sporocarpbiomass recorded in 2000 amounted to 264 g, or 19% of thehost leaf biomass. This was followed by patches 120 and 61,which had sporocarp biomass of 9% and 8% of the leafbiomass, respectively. The sporocarp production in the leastproductive patch was only 0.41 g, or 0.1% of the host leafbiomass, a ratio that was 140 times lower than that of the mostproductive patch.

The host leaf biomass, the length of a current-year shoot,and the number of winter buds on a current-year shoot, were

also significantly correlated with ECM sporocarp production(Table 3).

Leaf N concentration of each host ranged from 1.8 ± 0.1%to 2.9 ± 0.1%, and was significantly higher in the productivepatches than in the unproductive patches (Table 3). Leaf Pconcentration ranged from 0.10 ± 0.01% to 0.20 ± 0.02%,and was also significantly higher in the productive patchesthan in the unproductive patches (Table 3).

Host photosynthetic rate ranged from 0.082 ± 0.006 to0.217 ± 0.009 µmol CO2 s

−1 g−1 leaf dry weight, and wassignificantly higher in productive than in unproductive patches(Table 3). Furthermore, a significant correlation was con-firmed between sporocarp production and the photosyntheticrate of their associated hosts in the nine patches (Table 3).

The relationship between photosynthetic rate and leaf Nconcentration is shown in Fig. 7a. The photosynthetic rate ofeach leaf increased linearly with leaf N concentration, andthe correlation was statistically significant. The leaf N concen-tration ranged from 1.62% to 3.19%, and was low in theunproductive hosts and high in the productive hosts.

The photosynthetic rate also increased linearly with leafP concentration, and the correlation was statistically signifi-cant (Fig. 7b). The P concentration of the productive hostsexceeded 0.15%, and photosynthetic rates were higher than0.15 µmol CO2 s

−1 g−1 leaf dry weight. These values wereclearly higher than for the leaves of the hosts with low andmiddle productivity.

The species composition of ECM sporocarps was appar-ently different between the productive and unproductivepatches (Table 3). Scleroderma bovista was recorded primarily

Fig. 3 The recruitment of ectomycorrhizal fungal species with host size enlargement. Each mark represents sporocarp occurrence in relation to the associated host size. Only major fungal species are shown. The x-axis, shown logarithmically, indicates the area covered by Salix reinii in each vegetation patch.


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in the productive patches and H. mesophaeum was relativelyfrequent in the unproductive patches, although the number ofsporocarps in the latter was quite limited.

Discussion

Ectomycorrhizal fungal communities during early primary succession

An alpine dwarf willow, S. reinii, was the exclusively dom-inant host species of ECM fungi in our early successionalsite on Mt Fuji, despite occupying less than 1% of the groundarea. This alpine dwarf willow is usually distributed up toan elevation of 3000 m on Mt Fuji. Our research quadrat issituated on the south-east slope, where the effects of the lasteruption are evident, and it is located at the upper limit ofthe species. B. ermanii and L. kaempferi also formed ecto-mycorrhizae and produced some sporocarps. However, thetotal ground area covered by both of these species was 0.003%,and their contribution to overall sporocarp production wasnegligible compared with that of S. reinii.

In the present study, 23 ECM fungal species, represent-ing 11 450 sporocarps, were confirmed predominantly in

association with S. reinii. Each species had a relatively shortfruiting period and a different peak season. More than half ofthe annual sporocarp production by each fungal species wasoften counted during a single survey. Thus, weekly surveysthroughout the entire fruiting season are essential to obtain anaccurate account of sporocarp composition and productivity,as suggested by Vogt et al. (1992). Because our surveys coveredthe whole fruiting season, with measurements taken at weeklyintervals, the fungal list obtained should reflect the genuinefeatures of sporocarp production at our study site (Table 2).Long-year research is also recommended to assess fungalspecies (Vogt et al., 1992); however, this would greatly dependon site conditions. In our research site, the recorded specieswere almost same between each of the two years, and 2247 outof 2248 sporocarps belonged to the species that had beenrecorded in 2000. These results indicate that the two yearswould be enough for the evaluation of ECM sporocarp com-position in our research site, probably because of the favorableenvironmental conditions for sporocarp formation in ourresearch site.

No other studies to date have described comparable fungalcommunities during early primary succession after a volcaniceruption. In another example of primary succession, Jumpponenet al. (1999, 2002) reported 13 ECM fungal species at the

Fig. 5 The number of ectomycorrhizal species in relation to the associated host size. The x-axis, shown logarithmically, indicates the area covered by Salix reinii in each vegetation patch. The y-axis represents the number of confirmed ectomycorrhizal species in each vegetation patch in 2000 and 2001. The correlation is statistically significant (P < 0.01).

Fig. 6 The biomass production of ectomycorrhizal sporocarps in relation to associated host size. The x-axis, shown logarithmically, indicates the area covered by Salix reinii in each patch. The y-axis, shown logarithmically, represents the total ectomycorrhizal sporocarp biomass produced in each vegetation patch in 2000 and 2001. The correlation is statistically significant (P < 0.01).

Fig. 4 The number of sporocarps of each ectomycorrhizal fungal species or group in relation to host size. The x-axis, shown logarithmically, indicates the area covered by Salix reinii in each vegetation patch. The y-axis represents the total number of sporocarps on each species recorded in each vegetation patch in 2000 and 2001. The R-values followed by * and ** indicate significant correlation at P < 0.05 and P < 0.01, respectively. (a) Inocybe lacera; (b) Laccaria laccata; (c) Laccaria amethystea; (d) Laccaria murina; (e) Scleroderma bovista; (f) Hebeloma spp.; (g) Cortinarius spp., (h) Russula spp.


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front of the retreating Lyman Glacier. There, many ECMhost species, including members of Abies, Alnus, Larix, Picea,Pinus, Salix and Tsuga, readily became established from adja-cent ridges in a short period after the deglaciation. In our earlysuccessional site, S. reinii was exclusively dominant as the hostplant, and had associations with at least 22 species of ECMfungi. Ectomycorrhizal fungi might be more diverse thanpreviously thought during early primary succession.

Fig. 7 The relationships between photosynthetic rate and the concentration of leaf nitrogen (a) and phosphorus (b) of Salix reinii with reference to the production of associated ectomycorrhizal sporocarps. Closed circles indicate leaves collected from patches in which ectomycorrhizal sporocarp production was relatively high, open triangles indicate those from patches with middle productivity, and open squares indicate those from unproductive patches. The R-values in (a) and (b) indicate statistically significant correlation (P < 0.01).

Tabl

e 3

Ecto

myc

orrh

izal

spo

roca

rp p

rodu

ctio

n in

rel

atio

n to

var

ious

hos

t gr

owth

par

amet

ers

Patc

h N

o.

Spor

ocar

pbi

omas

s(g

)H

ost

size

(m2 )

Leaf

bio

mas

s(k

g pe

r pa

tch)

Phot

osyn

thes

is(×

10−3

µm

ol C

O2

s−1 g

−1 le

af d

ry w

t)

Cur

rent

yea

rsh

oot

(CY

S) (

cm)

Win

ter

bud

Num

ber

(/C

YS)

Leaf

Nco

ncen

trat

ion

(%)

Leaf

Pco

ncen

trat

ion

(%)

Myc

orrh

izal

rat

e(%

root

tip

s)M

ycor

rhiz

al s

poro

carp

s in

200

0Sp

ecie

s (n

umbe

r) (

%)

8426

4.06

4.39

1.39

217

± 9

a24

.5 ±

2.6

a20

.4 ±

2.3

a2.

9 ±

0.1

a0.

19 ±

0.0

1 ab

67.8

± 4

.8 a

Sb(1

09)

L(19

2) I(

15)

H(4

) C

(7)

6114

2.72

3.87

1.82

176

± 10

ab

27.7

± 1

.2 a

18.2

± 0

.7 a

2.5

± 0.

2 ab

c0.

20 ±

0.0

2 a

73.2

± 4

.9 a

Sb(6

0) L

(10)

H(7

)12

092

.15

4.31

1.04

196

± 13

ab

11.4

± 0

.6 b

c10

.4 ±

0.8

bc

2.7

± 0.

2 ab

0.16

± 0

.00

abc

67.2

± 6

.0 a

Sb(3

6) L

(16)

I(1)

C(1

)13

643

.53

10.3

04.

3215

8 ±

5 bc

14.2

± 0

.6 b

14.6

± 1

.0 a

b2.

5 ±

0.1

abc

0.15

± 0

.01

bcd

54.1

± 8

.0 a

bSb

(16)

L(1

20)

I(19

) R

(1)

104

8.24

2.79

0.48

106

± 2

d6.

1 ±

0.7

cd6.

8 ±

1.0

cd2.

0 ±

0.1

d0.

11 ±

0.0

0 cd

42.0

± 1

0.9

abSb

(3)

L(4)

B(1

)11

38.

033.

450.

6091

± 1

1 d

6.5

± 1.

1 cd

5.8

± 0.

6 cd

1.8

± 0.

1 d

0.11

± 0

.00

cd59

.3 ±

8.7

ab

L(1)

H(4

) B(

7)11

10.

643.

150.

0710

9 ±

13 c

d5.

0 ±

0.9

cd7.

6 ±

1.1

cd2.

1 ±

0.1

bc0.

12 ±

0.0

1 cd

59.4

± 2

.6 a

bL(

1) I(

1) H

(4)

C(1

)11

20.

642.

630.

0490

± 7

d2.

7 ±

0.4

d4.

2 ±

0.4

d2.

0 ±

0.1

d0.

12 ±

0.0

0 cd

54.1

± 6

.8 a

bL(

1) R

(1)

143

0.41

8.67

0.30

82 ±

6 d

3.0

± 0.

5 d

3.2

± 0.

8 d

2.0

± 0.

1 d

0.10

± 0

.01

d28

.7 ±

6.4

bH

(3)

r s0.

301

0.81

2*0.

912*

0.92

1*0.

912*

0.68

90.

833*

0.73

5

*Sig

nific

ant

corr

elat

ion

at P

< 0

.01.

Eac

h fig

ure

in c

olum

ns 5

–10

indi

cate

s a

mea

n ±

SEM

. Fig

ures

fol

low

ed b

y di

ffer

ent

lett

ers

with

in a

col

umn

are

stat

istic

ally

diff

eren

t by

Tuk

ey’s

HSD

tes

t (P

< 0

.01)

.r s

is th

e Sp

earm

an’s

rank

cor

rela

tion

coef

ficie

nt p

aire

d w

ith s

poro

carp

bio

mas

s. A

bbre

viat

ions

for t

he m

ycor

rhiz

al fu

ngi a

re a

s fo

llow

s: B

, Bol

etus

cf.

rube

llus;

C, C

orti

nari

us s

pp.;

H, H

ebel

oma

spp.

; I, I

nocy

be s

pp.,

L, L

acca

ria

spp.

; R, R

ussu

la s

pp.;

Sb, S

cler

oder

ma

bovi

sta.


Research 203

Species of Cortinarius, Hebeloma, Inocybe, Laccaria andRussula dominate alpine and arctic dwarf willow stands (Graf,1994; Gardes & Dahlberg, 1996) or S. repens stands (van derHeijden et al., 1999). Because a significant number of sporo-carps of these genera were also observed at our site, differentSalix species might have some similarities in ECM fungalcommunities. Although S. bovista, (as well as other Sclero-derma species) has rarely been reported in association withSalix species, it was one of the dominant fungal species at oursite, comprising 14.6% of the total number and 84.6% of thetotal dry weight of all ECM sporocarps. Species of Sclero-derma are usually observed in disturbed areas, or on immaturesoil (Ingleby et al., 1985). The dominance of S. bovista wouldpartly be due to the early successional conditions, as well asgeographical factors and different host species.

In the present study, we investigated the sporocarp com-munity of ECM fungi in the early stage of primary succession.The presence of sporocarps indicated the undergroundpresence of their ectomycorrhizae; however, the reverse is notalways true. In many cases, an abundance of above-groundECM fungi does not reflect an abundance of ectomycorrhizaeunderground (Horton & Bruns, 2001; Zhou & Hogetsu,2002). The sporocarps obtained would be important keys tounderground ECM communities, providing their DNA tobe matched with ECM root tips.

Succession of ECM sporocarps during early primary succession

Ectomycorrhizal sporocarps were observed within eachvegetation patch and its surrounding area. The vegetationpatches were sparsely distributed on the volcanic desert, andtherefore, individual associations between hosts and ECMsporocarps were clearly identified. Salix reinii grows to form adwarf patch within a vegetation patch, and its coverage areaincreases by vegetative growth of each genet and recruitmentof new genets (Lian et al., 2003). Thus, the coverage area isnot only an index of its developmental stages but also anacceptable index of the periods after the first colonization.The periodic aerial photographs that show vegetation patchenlargement in the last 40 yr strongly support this. Thesefeatures in our research site enabled us to investigate thesuccession of ECM sporocarps along with the developmentalstages of a single host species, S. reinii, during early primarysuccession on Mt Fuji.

In the sere of ECM sporocarps, the first-stage fungi (L. laccata,L. amethystina and I. lacera) were joined with the second-stage fungi (L. murina and S. bovista), and later the relativelylate-stage fungi (Hebeloma spp., Cortinarius spp. and Russulaspp.) appeared together with the first- and second-stage fungi.Small hosts (< 0.5 m2) were always observed in a small area onthe periphery of vegetation patches. The fungal communitiesassociated with these small hosts were simple, being domi-nated by one or two first-stage fungi. Along with host size

increment, S. reinii extends its root both inside and outsidevegetation patches over several meters. The second-stage fungiwere usually observed on the outsides of each patch, where nolitter had accumulated. The relatively late-stage species wereobserved only inside the vegetation patches, where some litterhad accumulated. The soil N content is known to increasewith development of vegetation patches, accompanied by ashift from inorganic to organic N (Tateno & Hirose, 1987).The succession of ECM sporocarps may be driven by thediversification of soil conditions created by the host growthand the different preference among ECM fungi to the soilenvironment.

The above successional model of ECM sporocarps was ableto explain the absence of second-stage and relatively late-stagefungi in association with small hosts. However, this might alsobe explained by the lower probability of finding sporocarps inthe small sampling area of small-size hosts, which was incom-parably smaller than that of large-size hosts. To evaluate thispossibility, we tested the null hypothesis that a fungal species(or group) is distributed evenly over the whole S. reinii cover-age and the absence of a species results from the lower collect-ing chance there. In this hypothesis, the probability that asingle sporocarp of a species is not observed in any of the smallhost is (1 − AS/AT), where AS is the total host area of the small-size hosts, which are smaller than the smallest host producingsporocarps of this species, and AT is the total area of all hostswithin the quadrat. Thus, if N is the total number of recordedsporocarps of this species during 2000 and 2001, the prob-ability that no sporocarp appears in any of the small hosts isPspecies = (1 − AS/AT)N. Although PL. murina (0.22) and PRussula

spp. (0.39) were greater than 0.05, PCortinarius spp., PHebeloma spp.

and PS. bovista were 0.0090, 0.0048 and 0.014, respectively, andless than 0.05. Thus, at least, the sporocarp absence of thelatter three fungal taxa in smaller hosts could not be explainedsimply by the lower probability of finding sporocarps in thesmall sampling area of these hosts at the P < 0.05 level ofsignificance.

The number of sporocarps of each major ECM fungalspecies or group monotonically increased with host size devel-opment, and every regression in Fig. 4 is statistically signifi-cant by the test of the regression (P < 0.05). In this figure, thex-value at which each regression line crosses with y = 1 isregarded as the expected smallest size in which sporocarps ofeach species are recorded (AE). The AE of I. lacera, L. laccata,L. amethystina, L. murina, S. bovista, Hebeloma spp., Corti-narius spp. and Russula spp. are 0.000, 0.040, 0.158, 0.307,0.001, 1.135, 2.194 and 2.272 m2, respectively. Although theAE value of S. bovista is smaller than the values of two first-stage fungi, the AE value of L. murina is larger than the valuesof all first-stage fungi and smaller than the values of the relat-ively late-stage fungi. The AE values of the relatively late-stagefungi are larger than the values of both the first-stage fungiand the second-stage fungi. Thus, the order of AE values ofabove fungal taxa except S. bovista is consistent with the


Research204

observed sequential appearance of ECM sporocarps alongwith the host size development (Fig. 3). These AE results,combined with the Pspecies results, would further support theECM sporocarp succession model presented above.

There was no indication of fungal replacement in the ECMsporocarp succession in our early successional site. Sporocarpsof all major fungal taxa did not decrease and become morenumerous with host size increment (Fig. 4). The ECM fungalsuccession in secondary successional sites usually consists ofthe decrease or replacement of some fungal species. Sporocarpobservations around transplanted birch trees have demon-strated a clear serial change in sporocarp species; initially anearly stage species, H. crustuliniforme, appears and is graduallydecreased in number and replaced with the late-stage species,Lactarius, Cortinarius and Russula (Last et al., 1984). Similarreplacements or decrease of ECM fungi in association withmany other tree species have also been described (Dightonet al., 1986). Despite the limited information about the ECMfungal succession during early primary succession, the lack offungal replacement is also noted on the forefront of theretreating Lyman Glacier ( Jumpponen et al., 2002). Althoughthe mechanisms of species replacement in fungal successionremain unclear, competition between ECM fungi could be afactor (Wu et al., 1999). The lack of species replacement ofECM fungi at our early successional site might indicate thatthere has been little or no competition in combination withlimited inoculum supply of new competitors in a vast barrendesert.

Sporocarp production of ECM fungi during early primary succession

The annual sporocarp biomass production by ECM fungi perhectare of S. reinii coverage was estimated to be 61.5 kg dryweight in 2000 calculated from all hosts in our quadrat. Thisindex was raised to 633 kg calculated from the sporocarpproduction in the most productive host. No comparable dataare available for other areas in early primary succession. Theannual biomass production of epigeous sporocarps per alpinedwarf shrub coverage is 0.004–0.021 kg ha−1 dry weight atalpine mire communities (Senn-Irlet, 1993). Sporocarpproduction of ECM fungi has been studied more in temperateforests, in which host trees have incomparably larger biomassthan dwarf shrubs. Annual dry weight production of epigeousmycorrhizal sporocarps is 0.014–6.8 kg ha−1 in Scots pineforests, 0.02–15 kg ha−1 in spruce forests, and 23–24 kg ha−1

in Pacific silver fir forests (Vogt et al., 1992). Thus, the figureestimated for ECM sporocarps associated with S. reinii isexceptionally large. This large sporocarp production suggestshuge production of spores by species compatible with S. reiniiand tolerant of the severe environmental conditions there. Inearly primary succession after volcanic eruption, colonizableECM spores from distant forests are quite limited (Allen et al.,1992). Therefore, the large sporocarp production in our

research site would be indispensable to improve ectomy-corrhiza formation on incoming and existing S. reinii bysupplying a huge number of colonizable spores on-site.

In the most productive of the nine patches investigatedintensively, annual sporocarp production amounted to 264 gdry weight (i.e. 19% of the host leaf biomass) (Table 3). Thisfigure is surprisingly large in comparison with sporocarpproduction in other forest stands; for example, epigeoussporocarp production was 0.2% and 0.1% of leaf biomass ina 23-yr-old and a 180-yr-old Abies amabilis forest, respectively(Vogt et al., 1982). The biomass of hyphae and mycorrhizalsheaths is hundreds of times larger than the sporocarp biomass,and the turnover of fungal components is relatively rapid(Forgel & Hunt, 1979; Vogt et al., 1982). Thus, the fungalcontribution to carbon and nutrient cycling even in thoseforest ecosystems is large despite such small proportions ofsporocarps relative to the total forest biomass (Vogt et al., 1982).Our results suggest that the contribution of mycorrhizal fungito carbon and nutrient cycling during early primary succes-sion could be much greater than previously thought.

There is a large variation in photosynthetic rates of S. reinii,ranging from 0.082 ± 0.006 to 0.217 ± 0.009 µmol CO2 s

−1 g−1

leaf dry weight among nine similar-size hosts (Table 3).The ECM sporocarp biomass production of the highestphotosynthesizing host was 264 g, which was 644 timesgreater than that of the lowest one, and the biomass produc-tion of ECM sporocarps was significantly correlated with thephotosynthetic rates among similar-size hosts (Table 3). Ecto-mycorrhizal sporocarp production appears to be determinedby host photosynthetic rate even during early primary succes-sion, as demonstrated in vitro (Lamhamedi et al., 1994) andin forest stands (Last et al., 1979; Högberg et al., 2001).

In addition to the ECM biomass production, the speciescomposition of ECM fungi was apparently different betweenactively photosynthesizing hosts and low-photosynthesizinghosts (Table 3). This may indicate that photosynthate supplyto ECM fungi influences ECM sporocarp communities. Scle-roderma bovista was dominant in actively photosynthesizinghosts, but not in low-photosynthesizing hosts. Because thehabitats of S. bovista have no litter accumulation and anextremely low organic matter in soil, its carbon appears to bemostly derived from host photosynthates. A sporocarp ofS. bovista was exceptionally large (e.g. 75 times heavier than thatof L. laccata in dry weight) and it would need a lot of photo-synthates for fruiting. The low-photosynthesizing hosts couldnot support the sporocarp formation of this species. Althoughthe number of sporocarps was small in low-photosynthesizinghosts, Hebeloma spp. and B. cf. rubellus, which mainly appearedon relatively humus-rich soil inside vegetation patches, wererelatively dominant. These species might have the ability touse other carbon sources in addition to the photosynthates ofS. reinii.

The photosynthetic rate of each S. reinii leaf increasedlinearly with leaf N and P concentration (Fig. 7). This result


Research 205

indicates that leaf nutrient status would be the main limitingfactor of the photosynthetic activity of S. reinii, takingaccount of our research site conditions, such as the sufficientrainfall, mild temperature and enough sunlight in growthseasons. Furthermore, the leaves having higher photosyn-thetic rates with higher concentrations of N and P distinctlybelonged to the hosts that produced larger amounts of sporo-carps (Fig. 7). It is supposed that nutrient supply from ECMfungi is essential to active photosynthesis of hosts, and con-versely enough photosynthate supply from hosts is indispens-able for the activity of ECM fungi. Our results may indicatethat the magnitude of such bidirectional interaction coulddetermine the activity of both symbionts in each ECM asso-ciation and, as a result, be expressed in its ECM sporocarpproduction.

Acknowledgements

This work was supported in part by a grant from PROBRAINand Grants-in-Aid from the Ministry of Education, Culture,Sports, Science and Technology of Japan.

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