Ecol Res (2007) 22: 955–974

DOI 10.1007/s11284-007-0390-z

M IY AD I A W AR D

Takashi Osono

Ecology of ligninolytic fungi associated with leaf litter decomposition

Received: 22 March 2007 / Accepted: 7 May 2007 / Published online: 15 June 2007

The Ecological Society of Japan 2007

Abstract Advances in our understanding of the decom-

position processes in forest ecosystems over the past
Introduction
three decades have demonstrated the importance of
Fungi are eukaryotic micro-organisms and constitute a
lignin as a regulating factor in the decomposition of leaf
major component of soil biota in forest ecosystems.
litter. Consequently, increasingly more attention is being
They are heterotrophic and produce extracellular en-
focused on the ecology of fungi associated with lignin
zymes to utilize the organic substrates present in litter as
decomposition. The aim of this review is to provide a
energy and nutrient sources. Fungi play an important
critical summary of the ecology of ligninolytic fungi
role in leaf litter decomposition as they contribute up to
inhabiting leaf litter and forest floor materials. The re-
90% of the total respiration of soil organisms (Kjøller
view focuses on the following aspects of ligninolytic
and Struwe 1982) and decompose the lignocellulose
fungi: the taxonomic and functional diversity of lignin-
matrix in the litter that other organisms are only rarely
olytic fungi, the outcomes of interactions between lig-
able to decompose (Cooke and Rayner 1984). Fila-
ninolytic fungi and other organisms, the activity and
mentous cells of fungi, which are called mycelia and
abundance of ligninolytic fungi measured by the pro-
have an average diameter of 2–10 lm, account for only a
duction of bleached leaves and humus, the activity of
very small portion – on a weight to weight basis – of the
ligninolytic enzymes in soil environments, the substra-
total organic material present on the forest floor, but
tum and seral succession, spatial and temporal patterns
they extend more than 10,000 m within 1 g of dry litter
in both mycelial abundance and species distribution, and
material. Hence, the activity of fungal mycelia are clo-
the effect of environmental factors such as nitrogen
sely associated with the functioning of the belowground
deposition and global environmental changes on lig-
part of forest ecosystems, such as the accumulation and
ninolytic fungi. This review integrates the ecology,
recycling of soil nutrients, the evolution of carbon
diversity, and activity of ligninolytic fungi into the
dioxide (CO2) from soil and the buildup of soil organic
context of an ecosystem in order to provide an under-
matter (Swift et al. 1979).
standing of the roles of ligninolytic fungi in decompo-
Lignin is an aromatic polymer made up of phenyl-
sition processes.
propane-based monomers linked via a variety of bonds
that bind cell-wall components together. It is one of the
Keywords Basidiomycetes Æ Bleach Æ Fungal
major structural components of the leaf litter of tree
community Æ Leaves Æ Lignin
species, accounting for 50–500 mg/g leaf material
(Fig. 1). Due to its complex structure, lignin is highly
refractory and persistent, being less readily available to
fungi than other components such as cellulose (Eriksson
et al. 1990). In addition, lignin forms a resistant shield
around cellulose to form lignocellulose in plant cell walls
Takashi Osono is the recipient of the 11th Denzaburo Miyadi
Award.
(Cooke and Whipps 1993). This makes most of the cel-
lulose in plant material less readily available to fungi
T. Osono because the lignified cellulose must be delignified before
Laboratory of Forest Ecology, Graduate School of Agriculture, the cellulose can be consumed.
Kyoto University, Kyoto 606-8502, Japan
E-mail: fujijun@kais.kyoto-u.ac.jp
Lignin is therefore considered to retard the fungal
Tel.: +81-75-7536079 decomposition of leaf litter (Berg and McClaugherty
Fax: +81-75-7536080 2003). Negative relationships between the lignin content
956

of leaf litter and the decomposition rate of leaf litter Hatakka 2001), and the ecology of wood-decomposing
have been reported from laboratory and field experi- fungi has been well established (Rayner and Todd 1979;
ments (reviewed in Osono and Takeda 2005a). In addi- Rayner and Boddy 1988; Boddy 1992). In contrast, the
tion, the relative amounts of lignin and other acid- ligninolytic metabolism and decomposition of lignin by
insoluble substances in the remaining litter increase litter-decomposing fungi have been the focus of only the
gradually as the decomposition proceeds (Berg et al. occasional investigation since the comprehensive work
1997; Osono et al. 2007), retarding yet further the mass of Lindeberg (1944). The diversity and ecology of litter-
loss rate of leaf litter in the later stages of decomposition decomposing fungi have been documented by Frankland
(McClaugherty and Berg 1987). Previous studies have et al. (1982), Cooke and Rayner (1984), and Dix and
also indicated that the accumulation and release of Webster (1995). However, few attempts have been made
nitrogen (N) in litter is associated with the decomposi- to relate the activity and ecology of ligninolytic fungi to
tion of lignin and the formation of acid-insoluble sub- the processes involved in the decomposition of leaf litter.
stances (reviewed in Osono and Takeda 2004; Osono This is partly due to the inherent difficulties involved in
et al. 2006a). The lignin-mediated accumulation of car- studying the function and ecology of minute fungal
bon (C) and N in soils has implications for the long-term mycelia that have an indeterminate growth form and
development of the ecosystem and the functioning of which lack useful morphological features for the iden-
ecosystem services (Amundson 2001; Berg and McC- tification of species. As illustrated in Fig. 2, it is usually
laugherty 2003; Lal 2005). Therefore, an in-depth difficult to study both functional and ecological aspects
understanding of the ecological roles of those fungi of fungal communities using the same methodology. It is
responsible for lignin decomposition will provide useful also difficult to examine both the abundance of micro-
insights into the mechanisms of decomposition and bial communities and the species composition of those
ecosystem processes in forests. communities concurrently with any single method.
Despite the importance of lignin as a regulatory Consequently, some studies (mostly soil microbiologi-
factor in decomposition and ecosystem processes, cal) focus on the metabolic and enzymatic activity of
information regarding the diversity, activity, and ecol- entire microbial communities, whereas others (mostly
ogy of fungi associated with lignin decomposition in leaf mycological) investigate the abundance of fungi or the
litter is still limited. Intensive studies have been per- species composition of fungal communities per se. Few
formed on ligninolytic systems of wood-decomposing studies, however, adopt these approaches simulta-
fungi (Kirk and Fenn 1982; Eriksson et al. 1990; neously. This has prevented studies of the ecology,
diversity, and activity of ligninolytic fungi from being
incorporated into an ecosystem context.
40 In the present review, I attempt to provide a critical
Number of tree species

summary of the ecology of fungi associated with lignin

30
decomposition in leaf litter and forest floor materials
within forest ecosystems. The review focuses on: (1) the
20
taxonomic and functional diversity of ligninolytic fungi;
10
(2) the outcomes of interactions between ligninolytic
fungi and other organisms; (3) the activity and abun-
0
dance of ligninolytic fungi determined by the production
of bleached leaves and humus; (4) the activity of lig-
[0,50)

[50,100)

[100,150)

[150,200)

[200,250)

[250,300)

[300,350)

[350,400)

[400,450)

[450,500)

ninolytic enzymes in soil environments; (5) the spatial

and temporal patterns in mycelial abundance and the
Lignin content (mg/g) distribution of ligninolytic fungal species, including
substratum and seral succession; (6) the effect of envi-
Fig. 1 A review of lignin content (as acid-insoluble residues) in leaf ronmental factors, such as N deposition and global
litter of tree species. Shaded bar Broadleaved species, open bar
coniferous species. The mean value for all data is 243 mg/g environmental changes, on the ligninolytic activity of
(n = 154); the mean value for broadleaved species is 235 mg/g fungi. Most of the data discussed in this review were
(n = 121) and for coniferous species is 271 mg/g (n = 33) derived from temperate forests, which have been inten-

Fig. 2 Methods for studying Fungal community

decomposer fungal
communities on leaf litter
Functional aspects Ecological aspects

Metabolic Enzymatic Species

Abundance
activity activity composition

CO2 Nutrient Organic C Organic Hyphal Specific

Colony Population Community
evolution mineralization compound N,P,S length compound
 957

sively researched, but reference is also made to other Table 1 Genera of fungi associated with lignin decomposition in
climatic regions, such as tropical forests. leaf litter and forest floor materials

Fungus Methoda Referencesb

Terminology of lignin Basidiomycetes

Agaricus E 14
The term ‘lignin’ is commonly used to denote that Agrocybe E, M 14, 18
Clavaria B, L 3, 6
fraction assayed as ‘acid-insoluble residues’ or ‘Klason Clitocybe B, E, L 3, 6, 10, 18, 20, 24
lignin’ based on proximate analyses, such as sulfuric acid Collybia B, E, L 2, 3, 4, 5, 6, 9, 14, 17, 22,
hydrolysis. This ‘lignin’ fraction contains not only true 24, 26, 28, 29
lignin but also cutin and tannin, as revealed by the Coprinus E 13, 15, 18
Cortinellus L 3
determination of hydroxyalkanoic acids (Kögel-Knab- Cudonia B 6
ner et al. 1989) and by solid-state 13C nuclear magnetic Cystoderma B 6
resonance (NMR) spectroscopy (Preston et al. 1997). Galerina E 18
This fraction is also believed to include humic sub- Hypholoma E 18
Lepiota B, E, L 3, 6, 14, 18
stances formed by the demethylation of lignin, by the Lepista E 15
incorporation of sugars and amino compounds into Lyophyllum E 13, 15, 18
humic substances, and by the binding of inorganic N to Macrolepiota E 14
phenolic compounds (Azhar et al. 1986a, b; Kögel 1986; Marasmius B, E, L 1, 6, 7, 14, 16, 17, 18, 29, 31
Kögel-Knabner et al. 1991; Steffen et al. 2002b). Fungal Micromphale L 24
Mycena B, E, L 3, 4, 5, 6, 17, 18, 21, 23,
melanins have structural similarities to soil humic acids 24, 26, 28
(Martin and Haider 1980; Schnitzer and Chan 1986; Phaelolepiota E 18
Paim et al. 1990; Coelho et al. 1997) and may be in- Psalliota B 6
cluded in the ‘lignin’ fraction. These humic substances Rhodocybe B 6
Spathularia B 6
can be depolymerized and mineralized by the ligninolytic Stropharia E, M 18, 26
enzymes of basidiomycetes, including the litter-decom-
posing ones (Blondeau 1989; Insam 1996; Steffen et al. Ascomycetesc
Alternaria E 27
2002b). Litter and soil microfungi, as well as actino- Aspergillus E, M 8, 27
mycetes, have been examined for their ability to Coccomyces B, L 25, 31
decompose tannins (Lewis and Starkey 1969; Grant Fusarium E, M 12
1976; Rai et al. 1988), melanins (Liu et al. 1995; Butler Geniculosporium B, L 19, 21, 28
Penicillium E, L, M 11, 12, 27
and Day 1998), humic acids (Mathur and Paul 1967; Pestalotiopsis E, M 12, 27, 30
Mishra and Srivastava 1986; Kontchou and Blondeau Xylaria B, L 19, 21, 25
1992), and ferulic acids (Black and Dix 1976; Tillett and a
Walker 1990). Plant pathogenic fungi have also been B, Bleaching activity in nature; E, enzyme (manganese peroxidases
and laccase) production in the laboratory; L, loss of lignin in leaves
shown to be capable of decomposing cutin (Baker and in the laboratory; M, mineralization of lignin and related com-
Bateman 1978; Lin and Kolattukudy 1980; Kolattukudy pounds in the laboratory
b
1981). Litter-decomposing ligninolytic fungi are able to 1, Lindeberg (1944); 2, Harris (1945); 3, Lindeberg (1946); 4, Saito
cause substantial loss of acid-insoluble residues that in- (1960, 1966); 5, Hering (1966); 6, Hintikka (1970); 7, Latter (1977);
clude not only lignin, but also tannins, melanins, humic 8, Kaplan and Hartenstein (1980); 9, Gourbière (1983); 10, Kuyper
and Bokeloh (1994); 11, Rodrı́guez et al. (1994); 12, Falcón et al.
substances, and cutin. However, few studies have (1995); 13, Yamanaka (1995); 14, Gramss et al. (1998); 15, So-
examined their potential ability to utilize the respective ponsathien (1998); 16, Tagger et al. (1998); 17, Miyamoto et al.
components. Although the terminology may be mis- (2000); 18, Steffen et al. (2000); 19, Osono and Takeda (2001a); 20,
leading, the present review refers to the acid-insoluble Osono (2002a); 21, Osono and Takeda (2002); 22, Steffen et al.
(2002b); 23, Ghosh et al. (2003); 24, Osono et al. (2003b); 25, Koide
residues as ‘lignin’ for the sake of simplicity. et al. (2005a); 26, Baldrian and Snajdr (2006); 27, Hao et al. (2006);
28, Osono and Takeda (2006); 29, Osono et al. (2006b); 30, Hao
et al. (2007); 31, T. Osono et al. unpublished data)
c
Diversity of ligninolytic fungi and their ligninolytic Including anamorphic states
capabilities
decompose lignin in leaves, and their mineralization of
Table 1 shows the taxonomic diversity of ligninolytic lignin and related compounds in the laboratory
fungi that decompose leaf litter and forest floor mate- (Table 1). Xylariaceous ascomycetes and their ana-
rials. The list includes a total of 31 genera (23 basidio- morphs, such as Xylaria and Geniculosporium, are
mycetes and eight ascomycetes) that have been reported commonly regarded as lignin decomposers (Whalley
to be able to decompose lignin in nature and/or in the 1996). Members of the genus Coccomyces of the family
laboratory. The major basidiomycete genera include Rhytismataceae have recently been reported to have
Clitocybe, Collybia, Marasmius, and Mycena, which are vigorous ligninolytic abilities (Table 1). These lignino-
most frequently studied for their bleaching activity in lytic fungi were successfully isolated from leaf tissues by
nature, their enzyme production, their ability to the surface disinfection method (Osono and Takeda
958

1999; Koide et al. 2005a). Species from other anamor-
phic genera of ascomycetes, such as Aspergillus spp. and
Penicillium spp., are litter and soil microfungi, and they
generally have much lower ligninolytic activities than
basidiomycetes (Kaplan and Hartenstein 1980; de Jong
et al. 1990; Hao et al. 2006). Bacteria and actinomycetes
also show some ligninolytic activity, but it is weaker
than that of fungi (Barder and Crawford 1981; Eriksson
et al. 1990).
Litter-decomposing fungi vary considerably in their
respective ability to decompose lignin in leaf litter (Ta-
ble 2). Care should be taken in interpreting the results
from the various studies on lignin-decomposing ability
of fungi listed in Table 2, however, as these are not
necessarily comparable with each other because of the
different methodologies of litter sterilization and incu-
bation among the studies. Despite this variability in the
experimental conditions, it is commonly accepted that
basidiomycetes have greater ligninolytic abilities than
ascomycetes, as demonstrated by Osono and Takeda
(2002, 2006) and Osono et al. (2003, 2006b) who inoc-
ulated both basidiomycetes and ascomycetes under the
same conditions. Fungi with greater ligninolytic abilities
often bring about a greater mass loss of litter. Selectivity
of lignin decomposition, expressed in Table 2 as the
lignin-to-weight loss ratio (L/W), is also highly variable
among fungal species (Table 2). Basidiomycetes
decompose lignin and other components, such as holo-
cellulose, in various proportions; for example, some
Clitocybe and Collybia spp. preferentially decompose
lignin (L/W of more than 2.0), whereas Mycena spp.
often cause the simultaneous decomposition of lignin
and other components (L/W of between 0.7 and 1.5).
Fungi from the ascomycetes, on the other hand, gener-
ally decompose cellulose selectively over lignin (L/W of
less than 0.6), whereas Coccomyces spp. are capable of
decomposing lignin selectively (L/W of more than 2.0).
Generally speaking, basidiomycetes have a larger L/W
than ascomycetes (Table 2).
The ratio between lignin and holocellulose decom-
position has an ecological implication. Lignin itself is
thought not to supply sufficient energy to maintain its
own decomposition, so nonlignified C energy sources
such as holocellulose are necessary as growth co-sub-
strates for fungi to decompose lignin (Kirk et al. 1976).
Even fungi that highly selectively delignify litter require
a small amount of carbohydrate co-substrate(s) to ini-
tiate the delignification process. Lignin decomposition is
thought to be a secondary metabolic function that serves
mainly to unmask cellulose and expose it to cellulases
from which it would otherwise have been protected
(Cooke and Whipps 1993). Therefore, the ratio between
lignin and holocellulose decomposition indicates the
efficiency with which ligninolytic fungi utilize energy
resources in litter. That is, fungi that selectively delignify
litter are able to decompose lignin more efficiently per
unit of holocellulose consumed than those that remove
lignin and holocellulose at the same rate and those that
decompose holocellulose in preference to lignin.
Fungi appear to be less efficient in decomposing the
lignin in coniferous needles than that in broadleaved leaf
litter (Table 2). Mikola (1956) and Osono and Takeda
(2006) demonstrated this difference by inoculating the
same fungal isolates onto both coniferous and broad-
leaved litter under the same conditions. The difference is
partly attributable to the presence of guaiacyl lignin in

Table 2 Mass loss (% original mass) of lignin in leaf litter and lignin-to-weight loss ratio (L/W) caused by basidiomycetes and asco-
mycetes tested in pure culture (nd not determined)

Litter species Taxona Method Mass loss of lignin L/Wb n Referencesc

Litter Incubation Mean Minimum, Mean Minimum,

sterilization maximum maximum

Broadleaved trees
Fagus sylvatica B Autoclaving 25C, 160–171 days 49.0 19.4, 76.5 1.9 1.1, 3.1 17 1
Fagus crenata B Autoclaving 20C, 56 days 29.8 6.5, 59.8 0.9 0.4, 1.1 6 3
A Autoclaving 20C, 56 days 5.5 2.0, 12.2 0.6 0.2, 1.5 8
Betula spp. B Gas sterilization 20C, 84 days 31.5 0.3, 72.8 1.1 0.0, 2.5 9 6
A Gas sterilization 20C, 84 days 1.5 1.9, 5.9 0.2 0.2, 0.8 6
Camellia japonica A Gas sterilization 20C, 56 days 9.7 10.3, 28.1 0.8 0.8, 2.3 9 5
Coniferous trees
Picea spp. B Gamma irradiation 23C, 56 days 21.8 9.0, 40.0 nd nd 10 2
Larix leptolepis B Gas sterilization 20C, 84 days 18.4 4.2, 39.6 1.9 0.5, 3.3 7 4
A Gas sterilization 20C, 84 days 1.7 3.7, 0.3 0.3 0.5, 0.0 5
Chamaecyparis obtusa B Gas sterilization 20C, 126 days 15.3 4.5, 36.7 0.6 0.4, 1.3 7 7
A Gas sterilization 20C, 126 days 0.6 5.1, 7.3 0.1 0.5, 0.5 5
Abies spp. B Gas sterilization 20C, 84 days 11.1 0.2, 36.0 1.3 0.1, 2.9 8 6
A Gas sterilization 20C, 84 days 1.1 4.2, 1.5 0.2 0.9, 0.5 3
a
B, Basidiomycetes; A, ascomycetes
b
L/W is an index of selective delignification caused by fungal species (Worrall et al. 1997). L/W = mass loss of lignin (% original mass)/
mass loss of litter (% original mass)
c
1, Lindeberg (1946); 2, Miyamoto et al. (2000); 3, Osono and Takeda (2002); 4, Osono et al. (2003b); 5, Koide et al. (2005a); 6, Osono and
Takeda (2006); 7, Osono et al. (2006b)

gymnosperms, which is more recalcitrant than the gua-
iacyl-syringyl lignin present in angiosperms (Eriksson
et al. 1990). The lower amount of lignin decomposition
that occurs on coniferous litter is more distinct for as-
comycetes than for basidiomycetes (Table 2). Fungal
decomposition of leaf litter is also affected by the lignin
content of the leaf litter, which not only differs among
litter species but also increases over successive stages of
decomposition (Fig. 3).
Fungi associated with the decomposition of leaf litter
and forest floor materials are functionally grouped as
litter-decomposing fungi. Fungi in other functional
groups, such as wood-decomposing and mycorrhizal
fungi, can also take part in lignin decomposition in leaf
litter. Examples of ligninolytic species in overlapping
groups between wood- and litter-decomposing fungi in-
clude Hypholoma spp. and Mycena crocata (Steffen
2003). There are a number of reports on the production
of ligninolytic enzymes in pure culture for ericoid and
ectomycorrhizal fungi (reviewed in Burke and Cairney
2002). The levels of peroxidase and polyphenol oxidase
increased when an ectomycorrhizal fungus, Suillus
granulatus, was in symbiosis with Pinus sylvestris under
laboratory conditions (Günther et al. 1998). However,
the enzymatic activities of mycorrhizal fungi are gener-
ally lower than those of saprobic fungi and they have not
yet been demonstrated in the field. Interestingly, Entry
et al. (1991) reported an enhanced decomposition of
lignin in mycelial mats of an ectomycorrhizal fungus,
Hysterangium setchellii, associated with Pseudotsuga
menziesii roots compared with adjacent non-mat soils.
The causal agents of lignin decomposition in the ecto-
mycorrhizal mat soils remained unknown, but this find-
ing suggests that the mycelial growth of ectomycorrhizal
fungi could enhance ligninolytic activity in soils.
Lignin decomposition involves numerous chemical
reactions, which indicates that a set of extracellular
a 40
Mass loss (%)
20
0 150 300
Initial lignin content (mg/g)
Fig. 3 Effects of lignin content on the decomposition of leaf litter
by ligninolytic fungi. a Mass loss (% original mass) of leaf litter of
15 tree species inoculated with Geniculosporium sp. as a function of
initial lignin content (T. Osono, unpublished data). R2 of the
regression line is 0.80. Bars indicate standard errors (n = 5).
b Mass loss (% original mass) of freshly fallen litter of Fagus
crenata compared with that of F layer materials (humic material)
caused by 19 isolates of litter-decomposing basidiomycetes (T. Osono,
959
enzymes is responsible for the fungal decomposition of
lignin (Eriksson et al. 1990). Phenol oxidase (e.g., lac-
case) and manganese peroxidase (MnP) are considered
to be the major enzymes involved in lignin decomposi-
tion by litter-decomposing basidiomycetes (Steffen
2003). To date, lignin peroxidase, another peroxidase
commonly found in ligninolytic wood-decomposing
fungi, has not been found in litter-decomposing fungi. A
few studies have purified and characterized ligninolytic
enzymes from litter-decomposing basidiomycetes
(Dedeyan et al. 2000; Steffen et al. 2002a; Farnet et al.
2004). Relatively little is known about the enzymatic
system of ligninolytic ascomycetes, despite the ability of
some species to cause selective delignification (Osono
and Takeda 2001a; Koide et al. 2005b).
Outcomes of interactions between ligninolytic fungi
and other organisms
The ligninolytic fungi present in natural environments
are rarely found under ‘pure culture’ conditions as in
nature they are in contact and interact with other
organisms, such as ligninolytic and nonligninolytic
fungi, bacteria, actinomycetes, and soil animals. How-
ever, most of the studies on the outcomes of interactions
between ligninolytic fungi and other organisms have
been performed under laboratory conditions and, con-
sequently, little is known of the importance of these
interactions in the field.
When one fungal mycelium is in contact with an-
other, mycelial interactions will occur. These include
synergic, neutral, and competitive and antagonistic
interactions, of which competitive and antagonistic
interactions are the most important for the development
of fungal communities (Rayner and Webber 1984).
Studies on wood-decomposing fungi have shown that
b 40
Mass loss of F layer material
CO
CO
20 MY
CO CO
CO
CL O MY
CL
MY MY MY
MR O O MY MY
O
0
450 0 20 40
Mass loss of freshly fallen litter
unpublished data). Content of acid-insoluble lignin was lower in
freshly fallen litter than in F-layer materials. CL Clitocybe spp., CO
Collybia spp., MR Marasmius spp., MY Mycena spp., O species in
other genera (Cyathus, Pseudoclitocybe, Gerronema, and
Psathyrella). The 1:1 line is indicated. Note that some Collybia
spp. caused greater mass loss on F-layer materials than on freshly
fallen litter, whereas Mycena spp. caused greater mass loss on
freshly fallen litter
960
mycelial interactions between ligninolytic fungi result in
the induction of laccase and peroxidase activities (White
and Boddy 1992; Savoie et al. 1998; Tsujiyama and
Minami 2005). It is uncertain, however, whether similar
results would be expected for mycelial interactions be-
tween ligninolytic litter-decomposing fungi. The rate of
leaf litter decomposition and laccase activity were found
to decrease when litter-decomposing basidiomycetes
were mixed with nonligninolytic fungi, bacteria, or
naturally occurring microbes owing to their antagonistic
interactions (Saito 1960; Kaplan and Hartenstein 1980;
Dix and Simpson 1984; Lang et al. 1997).
The addition of earthworms or millipedes enhanced
lignin decomposition by naturally occurring microbial
communities in Fagus sylvatica leaf litter (Scheu 1993).
The colonization of leaf litter by an unidentified saprobic
basidiomycete was enhanced by the presence of a
collembolan, Onychiurus subtenuis, which fed selectively
on a competing microfungus (Parkinson et al. 1979).
The decomposition rate of needle litter by Marasmius
androsaceus was also enhanced by grazing by Onychiurus
latus, whereas that of Mycena galopus was suppressed
(Newell 1984b). Some soil animals seem to have prefer-
ences for certain litter fungi (Mitchell and Parkinson
1976; Visser and Whittaker 1977; Kaneko et al. 1995),
but the effect of grazing depends on the animal density
(Hanlon and Anderson 1979). Thus, the presence of
collembola does not necessarily lead to the stimulation of
decomposition (e.g. Visser et al. 1981; Hassall et al. 1986).
The presence of some fungi can indirectly influence
the decomposition activity of other fungi through the
modification of litter quality. Pretreatment of leaf litter
with endophytic fungi and concomitant changes in litter
quality were found to affect the substrate utilization
patterns of Mycena spp., which shifted from simulta-
neous removal of lignin and carbohydrates to selective
delignification (Osono 2003). In turn, the removal of
lignin by ligninolytic fungi enhanced the decomposition
of leaf litter by succeeding fungi under both laboratory
and field conditions (e.g. Table 3) (Cox et al. 2001;
Koide et al. 2005a).
Bleaching: lignin decomposition by fungi
Contrary to laboratory experiments, the exact role of
individual fungal species in lignin decomposition is not
Table 3 Mass loss (% original mass) of bleached and nonbleached areas of Camellia japonica leaf litter (T. Osono, unpublished data)
Bleached areasa
Coccomyces sp. 10.3 ± 1.1
Dermateaceae sp. 7.4 ± 0.8
Xylaria sp. (anamorph) 23.6 ± 2.4
Values indicate means ± standard errors (n = 5)
a
Portions of C. japonica leaf litter were naturally colonized and delignified by Coccomyces sp. (Koide et al. 2005b). The bleached areas had
lower lignin content (272 mg/g dry material) than the nonbleached areas (351 mg/g). Leaf tissues from the bleached and nonbleached
areas were sterilized with ethylene oxide gas, inoculated with three fungal isolates on water agar, and incubated at 20C for 8 weeks to
determine the mass loss rates of litter
readily seen in nature because their mycelia, which are of
an indeterminate growth form, are too minute to be
delimited, quantified, and identified. However, the lig-
ninolytic activity of fungal species can be detected and
evaluated in nature by determinating the occurrence of
fungal colonies or the portions of the resource (i.e. leaves
or forest floor materials) occupied by fungal mycelia as
‘bleached portions’ on leaf surfaces and ‘bleached hu-
mus’ within the forest floor (Fig. 4). This approach has
two advantages. Individual colonies are easily delimited
by black zone lines or by sharp boundaries between
them and the nonbleached litter around the colony. This
enables researchers to quantify the number of colonies
and the area or amount of resource colonized by lig-
ninolytic fungi (e.g. Hirose and Osono 2006). Further-
more, fungi associated with the bleaching can be
identified based on the occurrence of fruiting bodies or
the isolation of fungi from the substrata.
According to Cooke and Rayner (1984), it is useful to
recognize that the ligninolytic activity of fungi in nature
operates at two levels of litter organization that are
associated with different modes of fungal colonization.
At one level, fungal colonies occur as bleached portions
on individual leaves (Fig. 4a). Litter in this case can be
regarded in terms of its component units – i.e., leaves –
each of which is considered to be an independent re-
source for fungal occupation. Many of the fungi are
‘component-restricted’ in that individual colonies are
limited in extent by the physical boundaries of the units
they occupy. At the second level, fungal colonies occur
as bleached humus within the forest floor (Fig. 4b). In
this case, the entire litter system – and not its individual
components – provides a habitat for fungi. Thus, sam-
pling methods should be scaled up accordingly. These
fungi are ‘component-unrestricted’ in that mycelia are
not restricted by the spatial limitations of individual
component units.
Osono (2006b) summarized data on the occurrence of
bleached areas on individual leaf litter of broadleaved
tree species in tropical and temperate forests. Bleaching
of this type is caused by both ascomycete and basidio-
mycete species that are component-restricted. Well-
studied examples include Xylaria spp. on Fagus crenata
leaf litter (Osono and Takeda 2001a) and Coccomyces
sp. on Camellia japonica leaf litter (Koide et al. 2005a,
b). Osono (2006b) found that the lignin content in the
bleached areas was consistently lower than that in the
Nonbleached areasa Probability
5.8 ± 1.0 P < 0.01
5.2 ± 1.2 0.10 > P > 0.05
17.9 ± 2.2 0.10 > P > 0.05

Fig. 4 Bleaching of leaf litter by component-restricted (a) and
component-unrestricted fungi (b). Bar 1 cm
nonbleached parts of the same leaves. Leaf mass per
area was also lower in the bleached than in the non-
bleached parts, indicating that colonization and lignin
decomposition by fungi led to a greater loss of leaf tissue
mass in the bleached portions.
Bleached humus, also called white-rot humus (Hint-
ikka 1970), is produced by component-unrestricted
basidiomycetes. The mycelia of these basidiomycetes
accounted for 1–13% of the length of the total fungal
mycelia in the forest floor of temperate forests (Ruscoe
1971; Bååth and Söderström 1977; Osono 2002a; Osono
and Takeda 2001b; Osono et al. 2002, 2006c), but the
ratio increased significantly in bleached humus (Frank-
land et al. 1981; Osono 2002a). Major fungal genera
known to produce bleached humus include Clitocybe,
Collybia, Marasmius, and Mycena (Table 1). In bleached
humus, the lignin content was lower and the soil respi-
ration rate greater than in the surrounding nonbleached
humus (Harris 1945; Saito 1957; Hintikka 1970; Osono
2002a). Thus, colonization and lignin decomposition by
fungi enhance the mineralization of organic matter in
the forest floor. Lignin decomposition in bleached hu-
mus also led to the mineralization of organic N (Hint-
ikka 1970; Osono 2002a). Kuyper and Bokeloh (1994)
demonstrated the relationship between fungal decom-
position of lignin and N mineralization in a laboratory
experiment.
961
The occurrence of bleached litter and humus in nat-
ure appears to depend on the ability of fungi to
decompose lignin selectively and effectively from sub-
strata. Xylaria spp. and Coccomyces spp., component-
restricted ascomycetes, have been shown to selectively
delignify litter to produce bleached areas on individual
leaves (Osono and Takeda 2001a; Koide et al. 2005a).
Clitocybe spp. and Collybia peronata, both component-
unrestricted basidiomycetes, are selective decomposers
of lignin that produced bleached humus in a cool tem-
perate forest (Osono 2002a). On the other hand, Mycena
filopes and M. polygramma were rarely associated with
bleached humus in the same forest, despite the frequent
occurrence of their fruiting bodies. These mycenas are
less effective in the decomposition of forest floor mate-
rials as they are simultaneous decomposers of lignin and
holocellulose (Fig. 3; Osono and Takeda 2002).
How frequently are bleached litter and humus
encountered on the forest floor? Bleached humus pro-
duced by component-unrestricted basidiomycetes cov-
ered 0.4–11.3% of the total area of the forest floor in
boreal forests (Hintikka 1970). Bleached humus
occurred around the base of fruiting bodies of Clitocybe
sp. in a cool temperate forest, but only two colonies
(each approximately 5 · 5 cm in size) were encountered
within a 0.1-ha area (Osono 2002a). These values are
lower than one would expect given that members of the
genera Clitocybe, Collybia, Marasmius, and Mycena are
well represented in assemblages of litter-inhabiting bas-
idiomycetes. Their fruiting bodies occur on the forest
floor much more frequently than bleached humus
(Table 4). This discrepancy suggests that only a portion
of these ligninolytic basidiomycetes are able to delignify
leaf litter and forest floor materials effectively under field
conditions – at least within temperate forests. The
bleached areas on leaf surfaces produced in a compo-
nent-restricted manner accounted for 6.3–14.5% of the
total leaf area (mean: 9.8%) in temperate forests and
7.9–29.7% (mean: 17.4%) in tropical forests (Osono
2006b).
Based on the available data on the occurrence of
bleached litter and humus, it is reasonable to assume for
temperate forests that ligninolytic fungi comprise as
much as 10% of the entire decomposer fungal commu-
nities or of the total resources available for fungal col-
onization. This is in good agreement with the estimate of
Gourbière (1983) that Collybia butyracea and C. macu-
lata bleached and decomposed 18 kg/ha/year of Abies
needles in the fermentation (F) layer. This decomposi-
tion rate was minor when compared with the total
amount of litter in the F layer (6.4 t/ha) or with the
annual rate of disappearance of the litter (1.0 t/ha/year).
Information on the occurrence of bleached litter and
humus in nature is still limited, despite its usefulness in
evaluating in situ ligninolytic activities of fungal species.
This is especially so in climatic regions other than tem-
perate forests, such as tropical forests. More studies are
necessary on the occurrence of bleached litter and hu-
mus in nature.
962

Table 4 Frequency of occurrence (%) of fruiting bodies of four genera of ligninolytic basidiomycetes on the forest floor

Forest type Location Observation plot Clitocybe Collybia Marasmius Mycena Referencea

Size (m2) Number

Broad-leaved forest
Fagus sylvatica Sweden 5 295 7 (3) 57 (4) 35 (3) 54 (13) 1
Quercus ilex France 100 64 27 (5) 27 (3) 3 (1) 41 (8) 8
Fagus crenata Japan 4 250 1 (1) 2 (2) 1 (2) 45 (8) 6
Alnus spp. USA 4 500 14 (10) 24 (4) <1 (1) 8 (5) 4
Mixed forest
Acer, Betula, Abies, Picea Canada 4 2000 8 (4) 16 (5) 11 (2) 24 (4) 3
Coniferous forest
Pinus sylvestris Finland 750 23 78 (2) 52 (5) 26 (1) 13 (4) 2
Picea abies Japan 1 100 0 (0) 42 (2) 7 (1) 46 (8) 5
Picea glehnii Japan 1 100 0 (0) 28 (2) 9 (3) 24 (5) 5
Thuja plicata Canada 9 96 <1 (2) <1 (2) 0 (0) 14 (19) 7
Picea sitchensis Canada 9 96 <1 (1) 0 (0) 0 (0) 11 (29) 7
Tsuga heterophylla Canada 9 96 2 (1) <1 (1) 1 (1) 8 (15) 7
Pseudotsuga menziesii Canada 9 96 2 (4) <1 (2) 1 (1) 7 (25) 7

Numbers indicate the frequency of the most frequent species within the genus. Numbers in parenthesis indicate species richness of the
genus. Note the great difference in size and number of the observation plots among studies
a
1, Tyler (1985); 2, Hintikka (1988); 3, Villeneuve et al. (1989); 4, Brunner et al. (1992); 5, Miyamoto et al. (2000); 6, Osono (2002a); 7,
Outerbridge (2002); 8, Richard et al. (2004)

stand (Gallo et al. 2004). The results from decomposi-

Activity of ligninolytic enzymes in soil environments
An alternative method for detecting and examining the
ligninolytic activity of fungal communities in nature is to
measure the activity of extracellular enzymes in soil
environments (Sinsabaugh et al. 1991; Sinsabaugh
1994). Enzyme assays are useful in that they directly
provide functional information on bulk microbial com-
munities that mediate leaf litter decomposition, although
the composition and activity of individual fungal species
are not taken into consideration (but see Waldrop et al.
2000 for the relationship between enzyme activities and
microbial community composition). Among the hun-
dreds of different enzymes released by microbes into the
environment, soil enzymes directly involved in the
decomposition of lignocellulose and the cycling of major
nutrients have been the focus of recent studies. These
soil enzymes include phenol oxidase (laccase), peroxi-
dase, glucosidases, cellulases, hemicellulases, proteases,
and phosphatases (Eriksson et al. 1990; Sinsabaugh and
Liptak 1997; Sinsabaugh 2005).
Of the major ligninolytic enzymes, laccase, followed
by MnP, have been found to be the predominant en-
zymes in the forest soils examined to date, while lignin
peroxidases have only rarely been detected (Criquet
et al. 2000; Fioretto et al. 2000; Baldrian et al. 2006).
The activities of laccase and MnP decreased with soil
depth (Baldrian et al. 2006), as did the diversity of lac-
case gene sequences (Luis et al. 2005). The activities of
laccase and MnP in decomposing leaf litter has also been
found to vary with litter species (Kourtev et al. 2002;
Sinsabaugh et al. 2002; Allison and Vitousek 2004; Hu
et al. 2006), with the type of ground cover, such as moss
and lichen (Sedia and Ehrenfeld 2006), and with forest
tion studies indicated that laccase activity was more
linearly associated with mass loss of litter and varied less
with seasonal changes in moisture content than MnP
activity (Fioretto et al. 2000; Kourtev et al. 2002; Allison
and Vitousek 2004; Di Nardo et al. 2004). The activities
of cellulases and glycosidases have also been found to be
subject to pronounced seasonal controls (Fioretto et al.
2000, 2001; Criquet et al. 2002). Di Nardo et al. (2004)
investigated the isoenzyme distribution of laccases and
peroxidases and found that some enzyme isoforms
contributed more than others to overall laccase and
peroxidase activity. This result suggests that some lig-
ninolytic fungi dominate over other species with similar
functional activities.
Spatial and temporal patterns in mycelial
abundance and distribution
Substratum succession of ligninolytic fungi
Succession is a directional change in the composition,
relative abundance, and spatial pattern of species com-
prising biological communities. Succession has been the
focus of research by mycologists working on litter-
decomposing fungi as it provides useful information on
resource utilization, interspecific interactions, and the
effects of physical and chemical environmental factors
on fungal populations. The succession of fungal com-
munities has been more precisely defined as ‘the
sequential occupation of the same site by thalli (nor-
mally mycelia) either of different fungi or of different
associations of fungi’ (Rayner and Todd 1979; Frank-
land 1992). Fungal successions are classified into sub-

stratum succession and seral succession (Frankland
1998). Substratum successions of saprobic fungi have
been described for a wide variety of litter types in
decomposition processes (Hudson 1968). Here, the
decomposition processes refer to the ‘initial’ processes of
transformation from freshly fallen leaves on the surface
of the litter (L) layer to near-humus materials in the F
layer. In contrast to substratum succession, less atten-
tion has been paid to the seral succession of saprobic
fungi in association with changes in the vegetation of
developing ecosystems.
Changes in the area of the bleached portions on leaf
surfaces indicate the succession of component-restricted
ligninolytic fungi during decomposition (Osono 2006b).
In a tropical forest, the bleached area on Shorea obtusa
leaf litter increased slowly to 1% of the total leaf area
during the first month and then increased sharply
thereafter to 30% after 9 months (Fig. 5). In a temper-
ate forest, on the other hand, the bleached area on
Camellia japonica leaf litter increased sharply to 17%
during the first 2 months and decreased gradually to 2%
after 18 months (Fig. 5). The bleaching agent for S.
obtusa litter has not been determined, but the pattern of
extension of the bleaching area suggests that lignin
decomposition was associated with colonization by
basidiomycetes in the later stages of decomposition
(Osono 2006b). Conversely, colonization by ligninolytic
ascomycete species was responsible for the bleaching of
C. japonica litter (Koide et al. 2005b). These were
endophytic on attached leaves and were capable of
removing lignin in freshly fallen leaves as prior colo-
nizers. They were isolated from the bleached portions
after no more than 4 months of decomposition. The
decrease (or darkening) of bleached areas after 4 months
30
Bleached area (%)
20 2
9
4
5 6
10
12
1 18
0 10 20 30 40
Accumulated mass loss of litter (%)
Fig. 5 Changes in the bleached area (% total leaf area) with respect
to accumulated mass loss of leaf litter of Shorea obtusa (filled
squares) in a tropical forest in Thailand and of Camellia japonica
(open circles) in a temperate forest in Japan. Numbers indicate the
months of decomposition. Bars indicate standard errors (n = 10).
Data are from Osono (2006b)
963
was due to the selective decomposition of holocellulose
by succeeding fungi (Koide et al. 2005a).
Changes in mycelial abundance in decomposing litter
have been investigated (e.g., Berg and Wessén 1984;
Berg 1991; Virzo de Santo et al. 2002; Osono et al.
2003a), but few data are available on the mycelial
growth of ligninolytic fungi during the decomposition
processes. It is clear that a measure of the abundance of
the total mycelial mass from the whole fungal commu-
nity is a poor guide to the colonization of the litter by
ligninolytic fungi. It is difficult, however, to identify the
mycelia of individual species based on the observation of
hyphae, except by means of the development and
application of antibodies, the direct extraction of DNA
from soils, or other molecular techniques (Frankland
et al. 1981; Hitchcock et al. 1997; Luis et al. 2004;
Cairney 2005). Alternatively, Osono and coworkers
followed changes in the mycelial abundance of basidio-
mycetes, some of which were expected to have lignino-
lytic ability (Fig. 6). Basidiomycetous mycelia increased
linearly with mass loss from Fagus crenata leaf litter,
with a few seasonal flushes, reaching approximately
20% of total hyphal length at the end of a 3-year period
of decomposition (Osono and Takeda 2001b). Osono
and Takeda (2001b) attributed this increase to the rel-
ative enrichment of the remaining litter with lignin. In
contrast, basidiomycetous mycelia remained at lower
levels during the decomposition of Swida controversa
and Camellia japonica leaf litter, accounting for an
average of 2% of the total hyphal length in both litter
types. It should be noted that not all basidiomycetes
colonizing litter are saprobic or ligninolytic, but the
difference among litter types suggests that the coloni-
zation of litter by basidiomycetes is possibly associated
1000
750
9
m/g dry litter
500
14 250
16
0 50 100
50 Accumulated mass loss of litter (%)
Fig. 6 Changes in the mycelial abundance of basidiomycetes with
respect to accumulated mass loss of leaf litter of Fagus crenata
(open squares), Swida controversa (open circles), and Camellia
japonica (open triangles). The length of basidiomycete mycelia was
determined under a microscope based on the presence of clamp
connections on their hyphae. Data are from Osono and Takeda
(2001b), Koide et al. (2005a), and Osono (2005)
964
with the lignin contents of the litters. Lignin content was
not only greater in F. crenata (437 mg/g) than in S.
controversa (196 mg/g) and C. japonica (212 mg/g), but
it also increased during the decomposition of F. crenata
leaf litter (Fig. 6).
Studies on the composition of fungal species using
isolation and/or direct observation methods have also
shown the frequent occurrence of basidiomycetes on leaf
litter in the later stages of decomposition (Saito 1956;
Kendrick and Burges 1962; Hudson 1968; Soma and
Saito 1979; Ponge 1991). A few basidiomycetes were
found in the early stages of needle litter decomposition
(Tokumasu 1996b, 1998; Virzo de Santo et al. 2002); at
this stage, they may take part in the removal of phenolic
compounds in the needles. In contrast, ligninolytic as-
comycetes appeared to take part in decomposition dur-
ing earlier stages than the basidiomycetes (Osono and
Takeda 2001b; Koide et al. 2005a), partly due to the
endophytic nature of some ligninolytic ascomycetes
(Osono 2002b; Koide et al. 2005b). This does not ex-
clude the possibility, however, that ligninolytic asco-
mycetes persist until later stages of decomposition. In
fact, xylariaceous ascomycetes were frequently isolated
from F. crenata and Pinus densiflora litter, even after
4 years of decomposition (T. Osono, unpublished data).
The colonization by xylariaceous fungi also varied with
litter types. In a cool temperate forest in Japan, for
example, the relative frequency of xylariaceous fungi
with respect to the entire fungal communities was
greater in freshly fallen (14% of total isolated fungi) and
decomposing leaves (54%) of lignin-richer F. crenata
(Osono 2002b) than in decomposing leaves of S. con-
troversa (9%) (Osono et al. 2004). In a study of mi-
crofungal assemblages on leaf litter from 29 tree species,
litter from which Xylaria spp. were isolated had a greater
lignin content (316 mg/g dry litter on average, n = 17)
than litter from which no Xylaria spp. were isolated
(242 mg/g, n = 12) (T. Osono, unpublished data).
Based on evidence currently available on temperate
forests, I propose an idealized diagram of the succession
of ligninolytic fungi in litter with varying lignin contents
during decomposition (Fig. 7). Overall, the relative
abundance of ligninolytic fungi increases not only
with the lignin content of the litter but also with the
relative enrichment of the litter with lignin during
decomposition. This is primarily due to competition
with nonligninolytic fungi such as cellulolytic and sugar
fungi whose hyphal growth is generally faster than that
of ligninolytic fungi. The lower the lignin content of the
litter, the greater the availability of nonlignified carbo-
hydrates that favor competitive colonization by nonlig-
ninolytic fungi and the concomitant exclusion of
ligninolytic fungi. Within the ligninolytic fungi, asco-
mycetes are more abundant in freshly fallen leaves than
basidiomycetes, but ascomycetes gradually decrease in
abundance during decomposition to be replaced by
basidiomycetes in the later stages. The extent and rate of
the decrease in the abundance of ascomycetes depend
upon such factors as life cycle, ability to utilize
Fig. 7 Idealized diagram of the succession of ligninolytic fungi of
the ascomycetes and the basidiomycetes in litter types with different
lignin contents. Axis a indicates litter type with greater lignin
content, axis b indicates decomposition stages with increasing
lignin content, axis c indicates the relative abundance of the fungi.
Relative abundance of ligninolytic fungi is represented as the
volume below the bold lines, which is further divided into
ascomycetes (darkly-shaded portion below the dotted lines) and
basidiomycetes (lightly-shaded portion above the dotted lines). The
decomposition stages in axis b represent the processes of
transformation from freshly fallen leaves on the surface of the L
layer to near-humus materials in the F layer
substrates, microenvironmental conditions, and com-
petitive and antagonistic mycelial interactions, which are
discussed in detail in Osono (2006a). Of these factors,
the efficiency with which fungi utilize resources is
important for controlling the effect of lignin on the
organization of the fungal community. A relative in-
crease in lignin content in decomposing litter will favor
competitive colonization and the replacement of asco-
mycetes with basidiomycetes, with the latter generally
decomposing lignin more efficiently than ascomycetes, as
discussed above. Some authors also ascribe the increase
in the abundance of basidiomycetes in the later stages of
decomposition to an increase in the moisture content of
the lower litter layers (Dix 1984, 1985; Dix and Frank-
land 1987). However, this is not always the case, as
demonstrated by Osono et al. (2006c) in a field experi-
ment in which the stage of decomposition was more
important than the moisture content for allowing the
colonization of the litter by basidiomycetes. The abun-
dance of basidiomycetes can be much greater than is
schematically described in Fig. 7 when the litter is
decomposed in exactly the same location as the colonies
of component-unrestricted basidiomycetes distributed
unevenly on the forest floor.
Seral succession of ligninolytic fungi
Successional changes in saprobic fungal communities in
litter and soils have been described in relation to primary
(Brown 1958a, b; Cooke and Lawrence 1959) and sec-

ondary vegetation development (Tresner et al. 1954;
Wicklow and Whittingham 1974; Countess et al. 1998).
Fruiting bodies of component-unrestricted basidiomy-
cetes have commonly been used as indicators of the
occurrence of ligninolytic fungi in successional series.
However, this method may underestimate the occur-
rence of basidiomycetes because the absence of a fruiting
body does not necessarily indicate the absence of myc-
elia in the soil. Thus, relatively little is known of the
changes in the abundance of the mycelia of ligninolytic
fungi or of the ligninolytic activity of fungal communi-
ties throughout vegetation development.
The establishment of host plants appears to be crucial
for the development of saprobic fungal communities in
early stages of primary succession – for example, in re-
cently deglaciated terrains (Bardgett and Walker 2004).
On deglaciated chronosequences in Alaska, the occur-
rence of fruiting bodies of Clitocybe, Collybia, Mycena,
and Marasmius spp. was associated with the presence of
host trees that provided the substrata for colonization
(Sprague and Lawrence 1959a, b, 1960). In fact, an
investigation of soil fungal assemblages inferred from
rDNA sequence analyses revealed the absence of sapr-
obic fungi, but the presence of mycorrhizal and parasitic
fungi, in nonvegetated areas of a glacier forefront
(Jumpponen 2003). Forest areas recently destroyed by
the thick deposition of volcanic debris were devoid of
fruiting bodies of Clitocybe and Collybia, which were
common components of macrofungal assemblages in
adjacent nondevastated forest areas (Obase et al. 2005).
Remarkable changes in ligninolytic basidiomycete
assemblages have been demonstrated during secondary
forest succession after harvest. Fujita (1989) and Iw-
abuchi et al. (1994), for example, reported a greater
number of species and more fruiting bodies of Collybia,
Mycena, and Marasmius spp. in forest stands after
20 years of stand development than in younger stands.
These authors suggested that this change was possibly
attributable to the accumulation of forest floor materials
as the stand aged. The opposite pattern was reported by
Hintikka (1988) who found that fruiting bodies of Col-
lybia and Clitocybe were concentrated in open stands 5–
15 years old and decreased in number in older stands.
Similar to Fujita (1989) and Iwabuchi et al. (1994),
Hintikka (1988) also considered that the greater amount
of litter residues left on the soil of the young stands after
felling had an effect on the ligninolytic basidiomycete
assemblages. Dighton et al. (1986) noted that both
Mycena and Marasmius spp. showed a pattern of greater
abundance of fruiting bodies in older stands of Picea
sitchensis than in younger stands, whereas the opposite
pattern was observed in the abundance of fruiting bodies
in younger and older stands of Pinus contorta. The dif-
ference in stand age-related patterns of fruiting between
the forest types has not yet been fully explained, but
Dighton et al. (1986) suggested the importance of litter
quality, which differed between the two tree species.
Bush fire affected the production of fruiting bodies of
basidiomycetes (Marı́n-Pinto et al. 2006), but little is
965
known of the post-fire succession of ligninolytic fungi
(Widden and Parkinson 1975; Bissett and Parkinson
1980; Visser 1995).
The occurrence of bleached areas on leaf surfaces was
examined in successional forest stands of regenerated
Pseudotsuga menziesii, using leaf litter of Gaultheria
shallon, a dominant understory shrub of the forests (T.
Osono et al., unpublished data). The bleaching was
caused by Marasmius sp. and Coccomyces sp., which was
verified by the ability of these fungi to cause selective
delignification in pure culture. Bleached areas on leaf
surfaces were smaller in young regeneration sites of 13–
14 years (2% of total leaf area) than in older sites of 50–
324 years (17–22%). The smaller bleached areas in the
regeneration sites may be due to changes in the micro-
environment and litter quality. The effect of clearcutting
on ligninolytic fungi will be discussed below.
Spatial and temporal distribution of ligninolytic
fungal populations
The spatial and temporal distributions of ligninolytic
fungi, other than in the substratum and in seral succes-
sion, have been studied under undisturbed conditions at
various scales. Spatial distribution has been examined
between forest types, between sites of various topo-
graphical position, within single forest stands, and be-
tween soil horizontals. Temporal variations in the
distribution of ligninolytic fungi have been studied sea-
sonally and annually. As in the case of seral succession,
the information currently available refers mostly to the
occurrence of fruiting bodies on component-unrestricted
basidiomycetes, and relatively little is known of the
distribution patterns of mycelia of ligninolytic fungi or
of the ligninolytic activity of fungal communities.
The occurrence of fruiting bodies of some ligninolytic
basidiomycetes is related to tree species and forest type.
Tyler (1992) and Hansen and Tyler (1992) found that in
southern Sweden species of Marasmius had a high
affinity for pure stands of F. sylvatica (M. alliaceus) or
Quercus robur (M. androsaceus and M. recubans),
whereas little or no relationship to tree species was re-
corded for species of Clitocybe and Collybia. The genus
Mycena was intermediate between these two sets of
species. Tyler (1992) suggested that fungal species
growing on leaf litter in the early stages of decomposi-
tion tended to have a higher affinity for one tree species
than those producing fruiting bodies from materials in
more advanced stages of decomposition. In a survey of
fruiting bodies over 104 plots within plantations con-
taining 12 tree species in Denmark, Lange (1993) noted
that some species in the genera Clitocybe, Mycena, and
Marasmius showed a preference for coniferous or
broadleaved trees, whereas Collybia spp. showed no
preference for any host.
The occurrence of fruiting bodies also varies with
topographical position. The biomass production of
fruiting bodies of Clitocybe, Collybia, Marasmius, and
966
Mycena spp. was greater on the lower slope than on the
upper slope of a Picea abies forest (Rastin et al. 1990a).
The number of plots in which fruiting bodies of Mycena
spp. occurred was greater on the lower slope than on the
upper slope of a Fagus crenata forest in Japan (Osono
2002a). However, this pattern of distribution of fruiting
bodies along forest slopes can vary depending on the
vegetation type and the genera of ligninolytic basidio-
mycetes (Okabe 1979). The amount of basidiomycete
mycelia in the litter layer also varied with slope position
and was greater on the upper slope than on the lower
slope in the F. crenata forest (Osono 2002a). This dif-
ference may reflect the predominance of mycorrhizal
fungi on the upper slope.
Mycelia of major ligninolytic basidiomycetes are
considered to be perennial. Consequently, they are dis-
tributed extensively and unevenly over the forest floor
because of their tendency to develop ‘fairy rings’ or
‘arcs’ (Shantz and Piemeisel 1917; Weaver 1975; Dow-
son et al. 1989; Frankland et al. 1995). Fruiting bodies of
these fungi have often been found to aggregate on the
forest floor in areas varying in size from 0.5 and 5 m
(Murakami 1989; Fukiharu and Kato 1997; Miyamoto
and Igarashi 2004; Yamashita and Hijii 2006). Analyses
of population structures revealed that the population
densities of Collybia subnuda and Marasmiellus prae-
acutus were 4–9 and 7–12 different individual genets per
100 m2, respectively (Murphy and Miller 1993, 1997).
Individuals of a rhizomorph-forming fungus, Marasmius
androsaceus, had high population densities of up to 18
individual genets within an area of 3 m2 (Holmer and
Stenlid 1991). Spatial variation in the number of fruiting
bodies and fruiting fungal species on the forest floor has
been correlated to the coverage and composition of trees
(Ferris et al. 2000), ground vegetation (Såstad 1995), or
the amount or thickness of the forest floor (Tyler 1991;
Yamashita and Hijii 2006). Conversely, Miyamoto and
Igarashi (2004) found that the number of fruiting bodies
of Collybia pinastris within each plot of 0.5 · 0.5 m was
not correlated with the thickness of the litter layer. In-
stead, plots in which the fruiting bodies of C. pinastris
occurred had a thinner litter layer than those in which
the fruiting bodies did not occur, probably due to the
decomposition of needle litter by the fungus.
Mycelia of basidiomycetes are often concentrated in
the interface between the L and F layers of temperate
forest soils (Saito 1956; Ruscoe 1971; Bååth and Sö-
derström 1977; Osono 2002a). In the forest floor of a
Picea sitchensis forest, the distribution of Marasmius
androsaceus was restricted to the L horizon, whereas
Mycena galopus occurred in the F1 horizon (Newell
1984a) despite the fact that, in a laboratory test, M.
androsaceus was able to colonize litter from both L and
F1 horizons more than twice as fast as M. galopus. Ne-
well (1984b) explained this result by attributing it to
grazing by collembola, demonstrating that mycelia of
M. androsaceus were grazed selectively by Onychiurus
latus, which was more abundant in the F1 horizon than
in the L horizon.
The occurrence of fruiting bodies of ligninolytic
basidiomycetes usually shows a seasonal pattern, with
two peak periods in the early summer and autumn, at
least in northern hemisphere temperate forests (Okabe
1983; Murakami 1989; Rastin et al. 1990b; Miyamoto
and Igarashi 1993; Osono 2002a; Kinoshita and Fuk-
uda 2004; Yamashita and Hijii 2004). Seasonal varia-
tion in the occurrence of fruiting bodies has been found
to differ among species. Individual species generally
have one peak period of fruiting, leading to changes in
the species composition with changes in season
(Murakami 1989; Miyamoto and Igarashi 1993;
Yamashita and Hijii 2004). It should be noted that the
peak period of fruiting does not necessarily correspond
to the peak period of ligninolytic activity of fungal
mycelia, but field evidence implies that there may be a
relationship between these two variables. For example,
Osono (2002a) found an increase in basidiomycetous
mycelia in November when the frequency of fruiting
bodies also reached its maximum. Criquet et al. (2000)
also reported increases in laccase and MnP activities
during the autumn, the period of favorable moisture
conditions. The fruiting of basidiomycetes varied be-
tween years (Eveling et al. 1990; Straatsma et al. 2001),
but the annual variation of ligninolytic fungi and the
factors affecting the variation have not been fully
evaluated.
Geographical locations
Geographical variations in litter decomposition rates
have been observed in temperate regions and have been
ascribed to climatic variables such as mean annual
temperature, summer and winter precipitation, and ac-
tual evapotranspiration, as determined by (Berg et al.
(1993) in Europe and Trofymow et al. (2002) in Canada.
Berg et al. (1997) examined the rates of increase of lignin
content in needle litter with respect to mass loss of litter
during decomposition in 30 sites across Europe. The
rates of increase of lignin concentration showed a posi-
tive correlation with actual evapotranspiration at the
sites, indicating that more lignin was decomposed in
cooler and drier climates than in warmer and wetter
climates. In other words, the efficiency at which fungal
communities decomposed lignin was higher at those sites
in cooler and drier climates and lower at those in warmer
and wetter climates. This pattern is consistent with the
results of incubation experiments that manipulated
temperature and moisture, as discussed below (Donnelly
et al. 1990; Osono and Takeda 2006). Berg et al. (1997)
interpreted the findings to mean that fast-growing
cellulolytic fungi would have an advantage over slow-
growing ligninolytic fungi under more favorable condi-
tions and that the opposite would be true under less
favorable conditions. Indeed, the relative abundance of
individual fungal species showed geographical patterns
that correlated with climatic variables (Tokumasu
1996a, 2001; Iwamoto and Tokumasu 2001).

The decomposition rate of leaf litter in general was
twofold higher in tropical forests than in temperate
forests (Takeda 1998; Takeda and Abe 2001). Lignin
decomposition also appeared to be faster in tropical
forests than in temperate forests (Takeda and Abe 2001;
Hirobe et al. 2004). The bleached area on the leaf sur-
faces was on average 1.8-fold greater in tropical forests
than in temperate forests, suggesting that the coloniza-
tion of leaf litter by component-restricted fungi that
cause selective delignification can be greater in tropical
forests (Osono 2006b). Consistent with this, Hirobe et al.
(2004) presented an interesting result that lignin was
removed more efficiently from decomposing leaves of 15
tree species in a lowland tropical rain forest than in
temperate forests (e.g., Berg et al. 1997; Osono and
Takeda 2005b). Our knowledge of the pattern of lignin
decomposition and the ecology of ligninolytic fungi in
tropical forests is still limited and should be studied
further.
Effects of changing environment
Excessive supply of nutrients
An excessive supply of N of anthropogenic origin, such
as atmospheric deposition and the addition of fertilizers,
affects lignin decomposition in leaf litter (Fog 1988; Berg
and Matzner 1997). Nitrogen amendment had a greater
effect on phenol oxidase activity than on peroxidase
activity, and the content of lignin and recalcitrant
materials in litter and soils controlled the effect of N
amendment (Carreiro et al. 2000; Hobbie 2000; Saiya-
Cork et al. 2002; Sinsabaugh et al. 2002, 2005; Waldrop
et al. 2004a). Thus, N amendment can stimulate phenol
oxidase activity and decomposition in low-lignin litter,
whereas it often suppresses phenol oxidase activity and
decomposition in high-lignin leaf litter (but see DeForest
et al. 2004a for decreased activity of phenol oxidase in
low-lignin litter). A probable explanation for the stim-
ulation of phenol oxidase in low-lignin litter is the
stimulation of cellulose decomposition that supplies co-
substrates for lignin decomposition. Phenol oxidase
activity and decomposition in mineral soils have been
found to be suppressed by N amendment irregardless of
forest type. Gallo et al. (2004) suggested that the inhi-
bition of oxidative activity in soils by N amendment
involved the inhibition of bacterial activity but that
changes in phenol oxidase activity were not always
attributable to specific groups of microbes (DeForest
et al. 2004a; Waldrop and Zak 2006). Nitrogen
amendment also stimulated the decomposition and
fungal assimilation of vanillin, a major product of lignin
depolymerization, in low-lignin litter, but inhibited it in
high-lignin litter (DeForest et al. 2004b; Waldrop et al.
2004b). Waldrop and Zak (2006) showed that phenol
oxidase activity responded directly and positively to the
amount of nitrate supplied in low-lignin litter but neg-
atively to that in high-lignin litter.
967
Sulfur dioxide, another major pollutant in atmo-
spheric deposition, strongly inhibited the respiration of
Mycena galopus, and this inhibitory effect was increased
by increasing concentrations of sulfur dioxide (Dursun
et al. 1996a, b). High concentrations of lead at shooting
ranges inhibited the growth of litter-decomposing
basidiomycetes and the activity of ligninolytic enzymes
(Tuomela et al. 2005).
Osono and coworkers (Osono et al. 2002, 2006a, b)
demonstrated the effect of the excessive supply of bird
excreta rich in N and phosphorus (P) on ligninolytic
fungi in a coniferous forest . The mycelial abundance of
ligninolytic Marasmius sp. decreased in forest stands
amended with a large amount of excreta (Osono et al.
2002). Consequently, the excreta deposition reduced
lignin decomposition in litter and led to the accumula-
tion of recalcitrant materials and excreta-derived nutri-
ents in the forest floor (Osono et al. 2006a). Osono et al.
(2006b) then explicitly demonstrated in laboratory
experiments that avian excreta reduced hyphal growth
rate and lignin decomposition in litter by ligninolytic
basidiomycetes. The decrease in net mass loss of lignin
was attributable not only to direct inhibition by the high
concentration of inorganic N and salts in the excreta,
but also to the formation, or net gain, of acid-insoluble
substances.
Global environmental changes
The atmospheric concentration of CO2 has increased in
recent years because of anthropogenic emissions, and
models predict that this rise in CO2 will increase global
temperature. Scientists are paying increasingly more
attention to the effect of these global environmental
changes on the structure and functioning of terrestrial
ecosystems and on terrestrial ecosystem processes,
including the decomposition of litter and soil organic
matter (Norby et al. 2001; Ito 2002; Berg and
McClaugherty 2003).
It is well known that decomposition rates of bulk leaf
litter increase with temperature (e.g. Carreiro and Koske
1992b). Lignin decomposition in leaf litter is also ex-
pected to increase with temperature, but relatively few
studies have examined the influence of temperature on
lignin decomposition. Laccase and peroxidase activities
in the upper horizons of temperate forest soils responded
linearly at temperatures between 2 and 30C in labora-
tory incubations (McClaugherty and Linkins 1990), as
did the mineralization of 14C-labeled lignin (Donnelly
et al. 1990). At the species level, mass loss rates of lignin
in Abies needles and Betula leaf litter caused by Collybia
dryophila were greater when the leaf litter incubated at
20C than at 10C (Osono and Takeda 2006). Donnelly
et al. (1990) and Osono and Takeda (2006) reported that
cellulose decomposition increased more rapidly than
lignin decomposition at higher temperatures, leading to
the decreased efficiency of lignin decomposition at
higher temperatures. Temperature affected the outcomes
968
of competitive interactions among fungal species
(Widden 1984; Widden and Hsu 1987; Widden and
Scattolin 1988; Carreiro and Koske 1992a), which
may also account for the shift in substrate utilization
efficiency at the community level.
The effect of CO2 concentration on lignin decompo-
sition can be indirect or direct. Indirectly, CO2 enrich-
ment is correlated with an increase in the lignin content
of leaf litter compared with ambient CO2 concentration
(Norby et al. 2001). The higher lignin content in leaf
litter produced at elevated CO2 concentrations will favor
competitive colonization by ligninolytic fungi but, in
turn, it will decrease the rate of decomposition of leaf
litter, as discussed above. In contrast, there are few
observations of the direct effect of elevated CO2 on the
activity of ligninolytic fungi. The development of fruit-
ing bodies of basidiomycetes may be inhibited by high
CO2 concentrations (Tabak and Cooke 1968), which
would affect the distribution of fungal propagules. The
growth of many litter-inhabiting fungi, including lig-
ninolytic species, is not significantly affected by high
CO2 levels according to Tabak and Cooke (1968) and
Hintikka and Korhonen (1970). Overall, the predicted
concentrations of CO2 in the near future will have a
negligible direct effect on the distribution and decom-
position activity of ligninolytic fungi.
Forest practices
Fungi can serve as indicators of stress and disturbance
resulting from forest management practices, such as
clearcutting, postharvest treatments, and transforma-
tion to agricultural fields (Durall et al. 2005). The
clearcutting of forests has been found to inhibit lignin
decomposition in leaf litter (Zhang and Liang 1995;
Ishikawa et al. 2007) and phenol oxidase activity in the
forest floor (Waldrop et al. 2003). The decrease in
ligninolytic fungi after clearcutting was partly attrib-
utable to the desiccation of the forest floor due to
canopy removal, and this may be responsible for the
slow decomposition rates of leaf litter in clearcut areas
(Edmonds 1978; Addison et al. 2003). Forest manage-
ment procedures other than clearcutting, such as the
removal and plowing of the forest floor, may also
influence the production of fruiting bodies by lignino-
lytic basidiomycetes (Ohenoja 1988; Kinoshita and
Fukuda 2004). On the other hand, activities of phenol
oxidase and peroxidase increased in plantations of
pineapple (Ananas comosus) originating from clearcut-
ting and burning compared with surrounding tropical
forests (Waldrop et al. 2000).
Concluding remarks
Mycologists are interested in the ecology of ligninolytic
fungi on leaf litter, with special emphasis on their suc-
cessional changes during decomposition, the species
richness of fruiting bodies that are visible on the forest
floor, and the ability of individual species to decompose
leaf litter in pure culture. The patterns of substratum
succession on various litter types were summarized in
Hudson (1968), and the origin, development, and suc-
cession of early colonizers were recently reviewed in
Osono (2006a). Data on the diversity and decomposing
ability of ligninolytic fungi have been published over the
last 60 years (see Tables 2, 4). However, the ecology,
diversity, and activity of specific ligninolytic fungi have
been explored individually, and they have been rarely
incorporated into an ecosystem context despite general
agreement among researchers that fungal communities
play irreplaceable roles in decomposition.
However, advances based on decomposition studies
carried out during the last three decades have demon-
strated the importance of lignin as a regulating factor in
the decomposition of leaf litter and the accumulation of
soil organic matter (e.g. Berg and McClaugherty 2003).
These have provided an opportunity for the integration
of ecology, diversity, and activity of ligninolytic fungi in
the present review. This integrative approach is useful
for understanding the ecological aspects of fungal
decomposition of lignin. More recently, progress in
molecular techniques has thrown light upon the enzy-
matic activity and genetic diversity of ligninolytic fungi
at a community level in the environment and at an
individual species level. Planning for future advances in
the studies of decomposition by ligninolytic fungi in
molecular, species, and community terms will allow us to
evaluate better the functioning of fungal communities in
ecological systems.
Acknowledgments I thank Dr. Hiroshi Takeda and Dr. Seiji
Tokumasu for encouragement and useful comments on the ecology
of fungi; Dr. Dai Hirose and Ms. Kanade Koide for useful dis-
cussions; Dr. Tony Trofymow for comments on decomposition;
Dr. Caroline M. Preston for helpful comments on chemical anal-
ysis; and Dr. Kari T. Steffen for comments on ligninolytic enzymes
of litter-decomposing basidiomycetes.
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