Fungal decomposition of Abies needle and Betula leaf litter

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Cooke and Rayner 1984). The abilities of fungi to decompose leaf ..... their ligninolytic activity (Robert and Chen 1989,. Almendros et al 1992). Values of L/C for ...

Mycologia, 98(2), 2006, pp. 172–179. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897

Fungal decomposition of Abies needle and Betula leaf litter Takashi Osono1 Hiroshi Takeda

decompose leaf litter have been examined by pureculture tests (reviewed in Osono et al 2003; Osono 2003; Koide et al 2005a, b). These studies showed that fungi were divided into three functional groups based on their substrate utilization. Lignocellulose decomposers attack both lignin and carbohydrates in various proportions, which result in a significant mass loss of litter. Cellulose decomposers preferentially attack carbohydrates with a slight or negligible loss of lignin. Sugar fungi rely on soluble sugars and are unable to disolve the structural polymers. Subalpine forests in temperate area of the northern hemisphere are characterized by slow decomposition and high accumulation of soil organic matter (Edmonds 1984; Zech et al 1990; Tian et al 1997, 2000; Prichard et al 2000). This has been attributed to lower resource quality of leaf litter of dominant conifers such as Abies than in broadleaf trees such as Betula (Vogt et al 1980, Stump and Binkley 1993, Tian et al 2000). The relative increase of lignin content in decomposed materials, which was attributable to the faster decomposition of holocellulose than lignin decomposition by decomposer communities (Tian et al 2000), also will contribute to the accumulation of recalcitrant soil organic matter (Takeda 1998). However few studies have been conducted regarding the potential ability of diverse fungi to decompose holocellulose and lignin in subalpine leaf litter and the effect of resource quality between litter types on fungal decomposition. The reduced activity of fungi to decompose litter under relatively low temperature is another responsible factor (Bisset and Parkinson 1980, Taylor and Jones 1990, Nakatsubo et al 1997, Reichstein et al 2000, Uchida et al 2000, Gonzalez and Seastedt 2001). Tian et al (2000) found that decomposition of holocellulose and lignin showed a clear seasonal pattern, which was faster in summer than in other seasons. These indicate the necessity to study the response of fungal decomposition to temperature, but the effects of temperature on the ability of fungi to decompose leaf litter are not well known (Thormann et al 2004). In this study we investigated and compared the ability of 29 fungal species in the basidiomycota, ascomycota and zygomycota to decompose subalpine leaf litter. Abies needle and Betula leaf litter were used as materials. Abies needle litter was characterized by lower resource quality to fungi (i.e. higher lignin content and lower nutrient contents, than Betula leaf litter [Tian et al 1998, 2000]). Incubation was done

Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8520, Japan

Abstract: The effect of litter type and incubation temperature on the ability of fungi to decompose leaf litter of subalpine trees was examined by a pureculture test. Mass loss of Abies needle and Betula leaf litter and utilization patterns of lignin and carbohydrates were investigated under two temperature conditions (20 C and 10 C) and compared for 29 species in basidiomycetes, ascomycetes and zygomycetes. The decomposing ability was generally higher in basidiomycetes than in ascomycetes and zygomycetes. Mass loss (% original mass) of litter was higher in Betula than in Abies and higher at 20 C than at 10 C. The 29 fungi were divided into lignocellulose decomposers, cellulose decomposers and sugar fungi based on their substrate utilization in Abies and Betula litter. Mass loss of lignin and carbohydrates by lignocellulose and cellulose decomposers was higher in Betula than in Abies. Mass loss of carbohydrates was higher at 20 C than at 10 C, but the temperature did not influence mass loss of lignin, indicating lignin decomposition by fungi was less sensitive to temperature than carbohydrate decomposition. Lignin/ carbohydrate loss ratio (L/C) of Collybia spp. that caused selective delignification was lower at 20 C than at 10 C. These results indicate that the decomposability of litter, lignin and carbohydrate was different between Abies and Betula and that temperature affected not only the rate at which fungi decompose litter but also the ability of fungi to use lignin and carbohydrates. Key words: birch, carbohydrate, fir, fungi, lignin, subalpine coniferous forest INTRODUCTION

Fungi play an important role in plant litter decomposition in forest ecosystems through soil nutrient recycling and build-up of soil organic matter (Swift et al 1979) because they decompose the lignocellulose matrix in litter that other organisms are unable to decompose (Kjøller and Struwe 1982, Cooke and Rayner 1984). The abilities of fungi to Accepted for publication 18 Feb 2006. 1 Corresponding author. E-mail: [email protected]

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OSONO AND TAKEDA: FUNGAL DECOMPOSITION OF SUBALPINE LITTER

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TABLE I. Mass loss (% original mass) of Abies needle and Betula leaf litter decomposed at 20 C and 10 C by fungi in vitro. Values indicate means 6 standard errors Abies Fungus

20 C

Code

Basidiomycetes Mycena polygramma Collybia dryophila Trametes versicolor Basidiomycete B822 Collybia butyracea Kuehneromyces mutabilis Collybia peronata Laetiporus sulphureus Basidiomycete PI1027 Fomitopsis pinicola Fuscoporia obliqua Fomes fomentarius

IFO33011 NBRC100095 IFO30340 B822 IFO30747 IFO30748 NBRC100096 IFO30745 PI1027 IFO8705 IFO8681 FO2

11.1 6 13.8 6 12.0 6 nt1 1.9 6 7.7 6 9.2 6 2.2 6 2.5 6 2.2 6 20.8 6 20.1 6

Ascomycetes Geniculosporium sp.2 Discosia artocreas Truncatella augustata Pestalotiopsis neglecta Trichoderma viride Penicillium glabrum Chalara longipes Trichoderma polysporum Aureobasidium pullulans Volutella ciliata Cladosporium cladosporioides Unidentified hyphomycete Geniculosporium sp.1 Tysanophora penicillioides Paecilomyces farinosus

6BVS21 IFO31883 IW2 8AL31 8BV31 10AF12 IW3 8BL15 IW4 8BL102 8BL12 10BL52 6BL92 IW1 6BLW91

4.9 6 4.8 6 nt nt 3.2 6 nt 2.8 6 nt 1.0 6 20.2 6 nt nt 0.1 6 0.7 6 nt

Zygomycetes Umbelopsis ramanniana Mortierella alpina

8AL43 10AL82

1

nt nt

Betula 10 C

4.1 1.0 0.5 0.9 0.8 1.1 0.6 0.1 0.1 0.0 0.2 0.3 0.3

0.9 0.3 0.1 0.6

0.6 0.3

2.5 6 0.2 6 8.3 6 nt 21.6 6 3.4 6 22.5 6 21.8 6 21.7 6 21.1 6 22.6 6 21.5 6 0.1 6 20.3 6 nt nt nt nt nt nt nt nt nt nt 21.7 6 21.8 6 nt nt nt

20 C

4.2 0.3 0.5 0.1 0.6 1.0 0.7 0.1 0.2 0.4 0.4 0.8 0.4

0.4 0.2

10 C

44.1 39.0 35.6 34.6 21.1 19.2 19.2 14.4 6.9 3.8 2.1 20.8

6 6 6 6 6 6 6 6 6 6 6 6

4.8 5.4 2.4 1.4 4.5 2.4 1.7 2.2 0.9 0.5 1.1 0.2

25.5 6 9.9 6 30.5 6 nt 21.4 6 10.7 6 2.7 6 22.5 6 20.9 6 22.0 6 21.7 6 22.2 6

15.5 12.4 10.2 7.4 5.2 4.8 3.9 3.3 2.0 1.7 0.2 0.1 0.1 20.8 22.5

6 6 6 6 6 6 6 6 6 6 6 6 6 6 6

0.3 0.5 1.0 0.4 1.0 0.5 1.0 0.8 0.3 0.9 1.0 0.4 0.9 1.0 0.4

6.4 6 0.9 6 nt nt nt nt nt nt nt nt nt nt 21.7 6 21.8 6 nt

1.5 6 0.6 0.3 6 0.3

0.9 0.8 2.2 0.6 1.0 0.4 0.8 0.1 0.6 0.7 0.4 0.8 0.3

0.0 0.9

nt nt

nt, not tested.

under two temperature conditions (20 C and 10 C) that represented the uppermost and intermediate values, respectively, of temperature range during the snow-free growing season when litter decomposition occurs most actively in a subalpine forest (Tian et al 2000). Fifteen of the 29 test fungi that showed marked ability to decompose litter were examined further for their ability to decompose lignin and holocellulose in litter. Fungi were isolated either from sporocarps or decomposing leaves collected in a subalpine coniferous forest in central Japan or obtained also from culture collections. MATERIALS AND METHODS

Source of fungi and litter.—Fungal isolates of 29 species were used in the test, including 12 basidiomycetes, 15

ascomycetes and 2 zygomycetes (TABLE I). Fomes fomentarius and two unidentified basidiomycete species coded B822 and PI1027 were obtained from basidiocarps occurring on dead wood on a study site in the subalpine Abies-Betula forest on Mount Ontake, Gifu, central Japan in Oct 2000. The study site is 2050 m a.s.l. Mean annual temperature is approximately 2 C and annual precipitation is approximately 2500 mm. Further details of the site were described in Mori et al (2004). The other nine basidiomycetes were obtained from a culture collection (IFO/NBRC, Chiba, Japan). Mycena polygramma, Collybia dryophila, Collybia butyracea, and Collybia peronata (litter decomposing basidiomycetes), and Trametes versicolor, Kuehneromyces mutabilis, Laetiporus sulphureus, Fomitopsis pinicola, Fuscoporia obliqua, and Fomes fomentarius (wood decomposing basidiomycetes) were common in subalpine forests (Imazeki et al 1987, Takahashi 1991). Mycena polygramma, three Collybia

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MYCOLOGIA

species, T. versicolor, and L. sulphureus also were used in the previous decomposition tests (Osono and Takeda 2002a, b, 2003; Osono et al 2003; Fukasawa et al 2005). Wood-decomposing fungi were used in the present study because some of them have vigorous ability to decompose lignin and (or) cellulose in plant residues (Eriksson et al 1990, Worrall et al 1997) and would be useful to evaluate the effects of litter type and incubation temperature on lignocellulose decomposition. Most of the ascomycete and zygomycete strains were isolated from Abies needles and Betula leaf litter collected from the subalpine forest floor in Jun, Aug and Oct 2000 by means of the washing method according to Osono and Takeda (2001b). Discosia atrocreas was obtained from the culture collection (IFO/NBRC). Truncatella augustata, Chalara longipes, Aureobasidium pullulans and Tysanophora penicillioides occurred frequently on Abies needles (Aoki et al 1990, Iwamoto and Tokumasu 2001, Iwamoto unpublished data) and these strains were provided from the culture collection of Dr S. Iwamoto (Tsukuba University, Japan). Freshly fallen needle litter of Abies species (A. veitchii and A. mariesii) and leaf litter of Betula species (B. ermanii and B. corylifolia) were collected from the the subalpine forest floor in Oct 2000. Species within Abies or Betula were not distinguished from each other because fallen leaves looked quite similar in their morphological characteristics so that they were identified simply to genus. Litter was oven-dried at 40 C 1 wk and preserved in vinyl bags until the experiment was started. Decomposition test.— Abies needle or Betula leaf litter (0.5 g) was sterilized by exposure to ethylene oxide gas at 60 C for 6 h. The sterilized litter was placed on the surface of Petri dishes (9 cm diam) containing 20 mL 2% agar. Inocula for each assessment were cut out of the margin of the previously inoculated Petri dishes on 2% malt-extract agar (malt extract 2% and agar 2% [w/v]) with a sterile cork borer (6 mm diam) and placed on the agar adjacent to the leaves, one plug per plate. The plates were incubated 3 mo at 20 C or 10 C in the dark. The plates were sealed firmly with laboratory film during incubation so that moisture did not limit decomposition on the agar. After incubation the leaves were retrieved, oven-dried at 40 C 1 wk and weighed. The initial litter also was sterilized, oven-dried at 40 C 1 wk and weighed to determine original mass. Mass loss of litter was determined as a percentage of the original mass. Four plates were prepared for each isolate, and four uninoculated plates served as a control. The duplicated leaves then were combined and used for chemical analyses as describe below. The incubation regimes of 20 C and 10 C adopted in this study represented the uppermost and intermediate values, respectively, of temperature range during the snow-free growing season (May–Oct) when litter decomposition occurred most actively in the subalpine site (Tian et al 2000). Chemical analyses.— Litter samples were ground in a laboratory mill (0.5 mm screen). The amount of

lignin in the samples was estimated by means of gravimetry, using hot sulfuric acid digestion (King and Heath 1967). Samples were extracted with alcoholbenzene at room temperature (15–20 C), and the residue was treated with 72% sulfuric acid (v/v) for 2 h at room temperature with occasional stirring. The mixture was diluted with distilled water to make a 2.5% sulfuric acid solution and autoclaved at 120 C for 60 min. After cooling the residue was filtered and washed with water through a porous crucible (G4), dried at 105 C and weighed as acid-insoluble residue. The filtrate (autoclaved sulfuric acid solution) was used for total carbohydrate analysis. The amount of carbohydrate in the filtrate was estimated by means of the phenol-sulfuric acid method (Dubois et al 1956). A total of 1 mL of 5% phenol (v/v) and 5 mL of 98% sulfuric acid (v/v) were added to the filtrate. The optical density of the solution was measured by a spectrophotometer at 490 nm, using known concentrations of D-glucose as standards. Total N content was measured by automatic gas chromatography (NC analyzer SUMIGRAPH NC900, Sumitomo Chemical Co., Osaka, Japan). Lignin/carbohydrate loss ratio (L/C) is a useful index of substrate-use pattern of each fungal species (Osono and Takeda 2002b, Osono et al 2003). L/C of each fungal species was calculated according to the equation: L=C ~ mass loss of lignin (% of original lignin mass)= mass loss of carbohydrates (% of original carbohydrate mass) Statistical analysis.—Two-way ANOVA was performed for 15 of 29 species to evaluate the difference in mass loss of litter using litter type (Abies and Betula) and incubation temperature (20 C and 10 C) as independent variables. Two-way ANOVA also was performed for a further five of the 15 species to evaluate the difference in mass loss of lignin and carbohydrates using litter type and incubation temperature as independent variables. Methods are described in Osono et al (2003). RESULTS

Initial chemical property.—Lignin content in Abies needle litter (41.5%, w/w) was similar to that in Betula leaf litter (42.7%), whereas carbohydrate content was higher in Abies (35.6%) than in Betula (31.3%). Nitrogen content was lower in Abies (1.06%) than in Betula (1.32%). Mass loss of litter.—Abies needle litter loss ranged from 20.8% to 13.8% at 20 C and from 22.6% to 8.3% at 10 C and that of Betula leaf litter ranged from 22.5% to 44.1% at 20 C and from 22.5% to 30.5% at 10 C (TABLE I). Mass loss was generally higher in Betula than in Abies, higher at 20 C than at 10 C and higher in litter decomposed by basidiomycetes than by ascomycetes and zygomycetes.

OSONO AND TAKEDA: FUNGAL DECOMPOSITION OF SUBALPINE LITTER

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TABLE II. Results of two-way ANOVA evaluating the difference in mass loss rate of litter, lignin and carbohydrates using litter type (Abies and Betula) and incubation temperature (20 C and 10 C) as independent variables F value

Litter Lignin Carbohydrates

N

Litter type

Incubation temperature

Litter type x incubation temperature

151 52 52

10.3** 6.7* 22.8***

10.3** 1.5ns 4.0+

1.4ns 0.2ns 0.6ns

*** P , 0.001, ** P , 0.01, * P , 0.05, +P , 0.10, ns non significant. 1 Data of M. polygramma, C. dryophila, T. versicolor, C. butyracea, K. mutabilis, C. peronata, L. sulphureus, basidiomycete PI1027, F. pinicola, F. obliqua, F. fomentarius, Geniculosporium sp.2, D. atrocreas, Geniculosporium sp.1 and T. penicillioides were used. 2 Data of M. polygramma, C. dryophila, T. versicolor, K. mutabilis and Geniculosporium sp.2 were used.

The results of two-way ANOVA indicated that mass loss of litter for the 15 selected species was significantly higher in Betula than in Abies and higher at 20 C than at 10 C (TABLE II).

litter decomposed by 15 species (nine basidiomycetes and six ascomycetes) that caused mass loss of litter more than 5.0% (TABLE III). Mass loss of lignin in Abies ranged from –4.2% to 36.0% at 20 C and from 0.9% to 13.3% at 10 C and that in Betula ranged from –1.9% to 72.8% at 20 C and from 20.4% to 32.9% at 10 C. Mass loss of carbohydrate

Lignin and carbohydrate decomposition.—Mass losses of lignin and carbohydrates were measured for the

TABLE III. Mass loss (% original mass) of lignin and carbohydrates in Abies needle and Betula leaf litter decomposed at 20 C and 10 C by 15 selected fungi and lignin to carbohydrate loss ratio (L/C) Lignin Abies Fungus

20 C

Basidiomycetes Mycena polygramma 7.0 Collybia dryophila 36.0 Trametes versicolor 10.0 Basidiomycete B822 nt1 Collybia butyracea 4.1 Kuehneromyces 4.5 mutabilis Collybia peronata 26.2 Laetiporus 0.9 sulphureus Basidiomycete 0.2 PI1027 Ascomycetes Geniculosporium 20.5 sp.2 Discosia artocreas 24.2 Truncatella nt augustata Pestalotiopsis nt neglecta Trichoderma viride 1.5 Penicillium glabrum nt

Carbohydrate Betula

Abies

Betula

Abies

Betula

10 C

20 C

10 C

20 C

10 C

20 C

10 C

20 C

10 C

1.4 13.3 9.8 nt nt 5.2

38.3 72.8 30.9 41.9 28.9 20.7

26.6 32.9 32.5 nt nt 15.2

16.6 11.4 16.6 nt 2.5 12.2

5.5 0.0 13.2 nt nt 7.3

66.8 27.7 60.9 45.8 33.3 26.7

38.0 6.4 48.1 nt nt 19.9

0.4 3.2 0.6 nt 1.6 0.4

0.3 * 0.7 nt nt 0.7

0.6 2.6 0.5 0.9 0.9 0.8

0.7 5.2 0.7 nt nt 0.8

nt nt

48.2 1.5

nt nt

12.6 5.0

nt nt

2.3 38.0

nt nt

2.1 0.2

nt nt

21.3 0.0

nt nt

nt

0.3

nt

5.4

nt

15.3

nt

0.0

nt

0.0

nt

0.9

5.9

20.4

8.2

4.8

40.4

31.4

20.1

0.2

0.2

0.0

20 C

10 C

nt nt

20.8 21.9

nt nt

9.0 nt

nt nt

33.8 28.9

nt nt

20.5 nt

nt nt

0.0 20.1

nt nt

nt

0.1

nt

nt

nt

20.3

nt

nt

nt

0.0

nt

nt nt

1.5 4.0

nt nt

3.9 nt

nt nt

11.0 12.2

nt nt

0.4 nt

nt nt

0.1 0.3

nt nt

* L/C was not calculated because of no mass loss of carbohydrates. nt, not tested.

1

L/C

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in Abies ranged from 2.5% to 16.6% at 20 C and from 0.0% to 13.2% at 10 C and that in Betula ranged from 2.3% to 66.8% at 20 C and from 6.4% to 48.1% at 10 C. Mass loss of lignin and carbohydrates was generally higher in Betula than in Abies and higher at 20 C than at 10 C. Mass loss of lignin was higher in litter decomposed by basidiomycetes than by ascomycetes, whereas that of carbohydrates was not markedly different between basidiomycetes and ascomycetes. The two-way ANOVA indicated that mass loss of lignin for the five selected species was significantly higher in Betula than in Abies but the effect of temperature was not significant (TABLE II). Mass loss of carbohydrates for the five selected species was also significantly higher in Betula than in Abies and significantly but only marginally higher at 20 C than at 10 C (TABLE II). Substrate use.—L/C in Abies ranged from 20.5 to 3.2 at 20 C and from 0.2 to 0.7 at 10 C (TABLE III). Collybia dryophila caused undetectable mass loss of carbohydrates in Abies so that L/C was not calculated. L/C in Betula ranged from 20.1 to 21.3 at 20 C and from 0.0 to 5.2 at 10 C. Collybia species (C. dryophila, C. butyracea, C. peronata) generally had high L/C values showing selective delignification. Mycena polygramma, T. versicolor, basidiomycete B822 and K. mutabilis showed simultaneous decomposition of lignin and carbohydrates and (or) greater decomposition of carbohydrates than lignin. Laetiporus sulphureus, basidiomycete PI1027 and six ascomycete species showed selective loss of carbohydrates with negligible mass loss of lignin. L/C of M. polygramma, K. mutabilis, C. peronata and Discosia atrocrea was lower in Abies than in Betula, whereas L/C of C. butyracea and Trichoderma viride was higher in Abies than in Betula. L/C of C. dryophila, T. versicolor, L. sulphureus, basidiomycete PI1027 and Geniculosporium sp.2 were not markedly different between Abies and Betula. L/C of Collybia dryophila was lower (i.e. this fungus decomposed lignin in preference to carbohydrates, less so at 20 C than at 10 C both in Abies and Betula) whereas, L/C of M. polygramma, T. versicolor, K. mutabilis and Geniculosporium sp.2 were not markedly different between 20 C and 10 C.

DISCUSSION

Litter decomposing ability.—Our results indicate that many fungi species have some ability to decompose Abies needle and Betula leaf litter. The results that decomposing ability was generally higher in

basidiomycetes than in ascomycetes or zygomycetes and that the fungi tested here were divided into three functional groups, lignocellulose decomposers, cellulose decomposers and sugar fungi, based on their substrate use in Abies and Betula litter, are consistent with previous studies (e.g. Osono and Takeda 2002b, Osono et al 2003). High rates of decomposition were limited to members of basidiomycetes such as M. polygramma, Collybia spp., T. versicolor and K. mutabilis. These fungi were regarded as lignocellulose decomposers of Abies needle and Betula leaf litter. They also have shown an ability to decompose both lignin and carbohydrates in other litter types (Lindeberg 1946, Hering 1967, De-Boois 1976, Dix and Simpson 1984, Miyamoto et al 2000, Osono and Takeda 2002b, Osono et al 2003). Laetiporus sulphureus, causing selective mass loss of carbohydrates in Abies and Betula, already has been reported as causing brown rot (Osono and Takeda 2003). Basidiomycete PI1027 also is regarded as cellulose decomposing fungi. Geniculosporium sp.2, D. atrocreas, T. augustata, P. neglecta, T. viride and P. glabrum in ascomycetes also are regarded as cellulose decomposers of Abies and Betula. Species in Geniculosporium, Discosia, Pestalotiopsis, Trichoderma and Penicillium are common litter inhabitants and have been shown to decompose carbohydrates in some litter types (Saito 1960, Hering 1967, Osono and Takeda 2002b, Osono et al 2003). These ascomycetes presumably caused soft-rot type decomposition in which carbohydrates were attacked preferentially (Nilsson et al 1989, Worrall et al 1997). On the other hand other basidiomycetes, ascomycetes and zygomycetes caused negligible mass loss in Abies needle and Betula leaf litter. Some of these fungi, such as A. pullulans, C. cladosporioides, U. ramanniana and M. alpina, might be regarded as ‘‘sugar fungi’’ sensu Hudson (1968). The growth of these fungi may depend on readily available energy sources such as soluble carbohydrates. Trichoderma polysporum and Paecilomyces farinosus are parasitic fungi that have limited ability to decompose litter (Harney and Widden 1991, Osono and Takeda 2002b). Other fungi might have a limited ability to attack Abies and Betula litter or it may be that the cultural conditions in this study might have been unsuitable for their growth. Lignin and carbohydrate utilization pattern.—Basidiomycetes attacked lignin and carbohydrates in Abies and Betula litter in various proportions, whereas ascomycetes preferentially decomposed carbohydrates. This result is consistent with Osono and Takeda (2002b), Osono et al (2003) and Fukasawa

OSONO AND TAKEDA: FUNGAL DECOMPOSITION OF SUBALPINE LITTER et al (2005), who compared lignin and cellulose decomposing ability among diverse fungi in other litter species or types. Collybia species (C. dryophila, C. butyracea, C. peronata) caused selective delignification in Abies and Betula. Lignin to carbohydrate loss ratio of Collybia in other litter types was determined as 2.2–8.2 (Lindeberg 1946, Osono and Takeda 2002b, Osono et al 2003). Collybia dryophila has been reported to produce laccase and manganese peroxidase (Hofrichter 2002, Tuomela et al 2005) and Collybia species has been known as white-rot decomposers in forest floor materials (Gourbie`re 1983, Miyamoto and Igarashi 2004). These indicated that Collybia spp. has an ability to cause selective delignification in various litter types. In these studies however the ligninolytic activity of Collybia spp. was evaluated as the loss of acid-insoluble ‘‘lignin’’ fractions during decomposition. Application of new analytical methodologies such as solid-state 13C nuclear magnetic resonance (NMR) to litter materials decomposed by Collybia spp. would provide further insight into their ligninolytic activity (Robert and Chen 1989, Almendros et al 1992). Values of L/C for the other basidiomycetes in the present study are within the range of previous reports. Those of Mycena polygramma have been reported as 0.2–0.7, T. versicolor as 0.2–1.0 and L. sulphureus as 0– 0.3 (Osono and Takeda 1999, 2002b, 2003; Osono et al 2003; Fukasawa et al 2005). Geniculosproium, Discosia and Trichoderma in ascomycetes have caused selective carbohydrate decomposition in beech litter with L/C of 0.1–0.3, according to Osono and Takeda (1999). Effect of litter type.—Mass loss of litter, lignin and carbohydrates was greater in Betula leaf litter than in Abies needle litter. This difference in decomposability between Abies and Betula also has been reported in the field by Tian et al (2000). Mikola (1956) and Osono and Takeda (2001a) also have reported the effect of litter types on the ability of fungi to decompose lignin and carbohydrates in pure-culture decomposition tests. One possible explanation for this is the difference in resource quality between litter types. For example the content of nitrogen, one of essential macronutrients for fungal growth, was lower in Abies than in Betula, which may impede fungal growth in Abies needle litter. On the other hand the difference in the arrangement of fibers within cell walls and the accessibility of enzymes, the higher content of guaiacyl unit in gymnospermous lignin than angiospermous lignin or host specificity of individual fungal species may account for the

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difference in mass loss between Abies and Betula litter. The difference in the decomposability between Abies and Betula, as well as the substratedependent pattern of lignin and carbohydrate use for diverse fungal species, suggest that the changes in species composition of not only trees but also fungi potentially influence the accumulation of soil organic matter in subalpine forests. Effect of temperature.— Mass loss of litter and carbohydrates was higher at 20 C than at 10 C but a similar difference was not detected in mass loss of lignin, suggesting lignin decomposition by the test fungi was less sensitive to temperature than carbohydrate decomposition within this temperature range. Such a difference in the response of lignin and carbohydrate decomposition to temperature resulted in the lower values of L/C at 20 C than at 10 C, which obviously was detected in C. dryophila (i.e. this fungus decomposed lignin in preference to carbohydrates, less so at 20 C than at 10 C). Donnelly et al (1990) measuring lignin and cellulose decomposition in soil incubated at 4 C, 12 C and 24 C found the lower ratio of lignin decomposition to cellulose decomposition at higher temperature. Therefore not only the rate at which fungi decompose litter but also the ability of fungi to use lignin and carbohydrate can be affected by temperature. Such a shift in fungal decomposition in lignin and cellulose in relation to temperature suggests the changing role of fungi in decomposition processes in subalpine forests in response to future increase of global temperature, leading to the increased accumulation of recalcitrant soil organic matter derived from lignin and lignin-like substances. It should be noted however that temperature increase also would be accompanied with the shift in species composition of basidiomycetes responsible for lignin and cellulose decomposition. Nevertheless the abundance and distribution of ligninolytic litter decomposing basidiomycetes on subalpine forest soils have been scarcely documented in published literature (Senn-Irlet and Bieri 1999). Further studies thus are required in this regard to discuss the role of ligninolytic fungi on the accumulation of soil organic matter in subalpine forests. ACKNOWLEDGMENTS

We thank Dr S. Iwamoto and Mr Y. Fukasawa for their kindness in providing fungal strains for the experiments; Dr S. Tokumasu for his helpful identification of fungi; Dr M. Hirobe for his collection of litter samples; Dr H. Barclay and

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MYCOLOGIA

A. Mori for their useful discussion and critical reading of the manuscript. LITERATURE CITED

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