REVIEW / SYNTHÈSE
Role of phyllosphere fungi of forest trees in the
development of decomposer fungal communities
and decomposition processes of leaf litter
Abstract: The ecology of endophytic and epiphytic phyllosphere fungi of forest trees is reviewed with special emphasis
on the development of decomposer fungal communities and decomposition processes of leaf litter. A total of 41 genera
of phyllosphere fungi have been reported to occur on leaf litter of tree species in 19 genera. The relative proportion of
phyllosphere fungi in decomposer fungal communities ranges from 2% to 100%. Phyllosphere fungi generally disappear
in the early stages of decomposition, although a few species persist until the late stages. Phyllosphere fungi have the
ability to utilize various organic compounds as carbon sources, and the marked decomposing ability is associated with
ligninolytic activity. The role of phyllosphere fungi in the decomposition of soluble components during the early stages
is relatively small in spite of their frequent occurrence. Recently, the roles of phyllosphere fungi in the decomposition
of structural components have been documented with reference to lignin and cellulose decomposition, nutrient dynamics,
and accumulation and decomposition of soil organic matter. It is clear from this review that several of the common
phyllosphere fungi of forest trees are primarily saprobic, being specifically adapted to colonize and utilize dead host
tissue, and that some phyllosphere fungi with marked abilities to decompose litter components play important roles in
decomposition of structural components, nutrient dynamics, and soil organic matter accumulation.
Key words: carbon cycle, community, endophyte, epiphyte, succession.
Résumé : Nous faisons une revue de l’écologie des champignons endophytes et épiphytes de la phyllosphère d’arbres
forestiers en s’attardant sur le développement de communautés fongiques de décomposeurs et sur les processus de
décomposition de litières de feuilles. La présence d’un total de 41 genres de champignons de phyllosphère fut rapportée
sur la litière de feuilles d’espèces d’arbres distribuées au sein de 19 genres. La proportion relative des champignons
de phyllosphère chez les communautés fongiques de décomposeurs oscille entre 2 % et 100 %. Les champignons de
phyllosphère disparaissent généralement lors des stades précoces de la décomposition bien que quelques espèces persistent
jusqu’aux stades tardifs. Les champignons de phyllosphère ont la capacité d’utiliser divers composés organiques comme
sources de carbone et leur capacité notoire de décomposition est associée à une activité ligninolytique. Le rôle des
champignons de phyllosphère dans la décomposition de composantes solubles lors des stades précoces est relativement
petit malgré leur présence fréquente. Le rôle des champignons de phyllosphère dans la décomposition des composantes
structurelles fut récemment documenté en référence à la décomposition de la lignine et de la cellulose, des dynamiques
nutritionnelles et de l’accumulation et la décomposition de matières organiques du sol. Il est indéniable selon cette revue
que plusieurs des champignons de phyllosphère communs d’arbres forestiers sont principalement saprobes, étant spécifique-
ment adaptés pour la colonisation et l’utilisation de tissus morts de l’hôte, et que certains champignons de phyllosphère
ayant des capacités notoires pour la décomposition de composantes de la litière jouent des rôles importants dans
la décomposition de composantes structurales, les dynamiques nutritionnelles et l’accumulation de la matière organique
Mots clés : cycle du carbone, communauté, endophyte, épiphyte, succession.
[Traduit par la Rédaction]
Fungi in the phyllosphere are widespread and are encoun-
tered in a variety of host plants, such as forest trees, herbs,
graminoids, and mosses (Hudson 1968; Petrini 1986; Boddy
and Griffith 1989). Phyllosphere fungi have been studied
from various aspects, such as taxonomy, physiology, and
ecology (Preece and Dickinson 1971; Dickinson and Preece
Can. J. Microbiol. 52: 701–716 (2006) doi:10.1139/W06-023© 2006 NRC Canada
Received 28 November 2005. Revision received 27 February
2006. Accepted 13 March 2006. Published on the NRC
Research Press Web site at http://cjm.nrc.ca on 27 July 2006.
T. Osono. Laboratory of Forest Ecology, Division of
Environmental Science and Technology, Graduate School of
Agriculture, Kyoto University, Kyoto 606-8502, Japan (e-
1976; Blakeman 1981; Fokkema and van den Heuvel 1986;
Andrews and Hirano 1991; Morris et al. 1996; Redin and
Carris 1996; Lindow et al. 2002). The ecology of phyllo-
sphere fungi has been studied intensively in terms of their
interactions with plants, herbivores, and pathogens on living
leaves (Clay 1986, 1991; Petrini 1986, 1991; Kinkel 1991;
Carroll 1991, 1995; Dix and Webster 1995; Stone et al.
1996; Lindow and Brandl 2003). In contrast, the ecology of
phyllosphere fungi on leaf litter has received little attention
(Omacini et al. 2004; Lemons et al. 2005). Hudson (1968),
in his review of fungal succession on plant remains above
the soil, reported that a group of phylloplane fungi termed
common primary saprobes was the main unifying feature of
early stages of fungal succession on leaf litter. Since then,
several authors have confirmed the occurrence of these fungi
in early stages of decomposition on various leaf litters and
supported the general validity of the Hudson finding. To my
knowledge, however, there has been no review on the ecol-
ogy of phyllosphere fungi on leaf litter since Hudson (1968)
in spite of the accumulation of published data that enables
us to summarize the role of phyllosphere fungi in the devel-
opment of decomposer fungal communities.
Recent studies of leaf litter decomposition in forest eco-
systems have shown relatively rapid changes in remaining
mass and chemical composition during early stages of decom-
position (Berg and McClaugherty 2003; Osono and Takeda
2004b, 2005a). Phyllosphere fungi thus can play major roles
as early colonizers of leaf litter in decomposition, which is
closely associated with the production of carbon dioxide and
the accumulation of soil organic matter (SOM) in forest soils
and, hence, is associated with global carbon cycle (Berg and
McClaugherty 2003). Recent advances in decomposition stud-
ies will provide the basis to discuss the roles of phyllosphere
fungi in decomposition, but there has been little comprehen-
sive review of their roles in short-term and long-term pro-
cesses of decomposition and SOM accumulation.
The purpose of this review is to summarize the published
studies on phyllosphere fungi of forest trees, mainly temper-
ate trees, and describe their roles in the development of
decomposer fungal communities and decomposition processes
of leaf litter. Emphasis is placed on (i) the occurrence of
phyllosphere fungi on leaf litter and their relative proportion
in decomposer fungal communities, (ii) the origin and devel-
opment of early colonizers, (iii) their succession and persis-
tence until late stages of decomposition, (iv) the substrate
utilization and decomposing ability, (v) the roles in decom-
position processes, and (vi) their roles in the accumulation
and decomposition of SOM in forest soils.
In this review, the phyllosphere includes the living leaf as
a whole and consists of the surface (phylloplane) and inter-
nal tissue. Earlier studies, such as those of Last (1955) and
Ruinen (1956), used the term phyllosphere to indicate the
leaf surface only, but recent studies have defined the term
broadly to include not only the leaf surface but also the
internal tissues (Petrini 1991; Andrews 1996).
Phyllosphere fungi include epiphytes and endophytes that
frequently colonize the phylloplane and internal tissue, re-
spectively, of living leaves. The term epiphytes is a synonym
of phylloplane fungi according to Last and Deighton (1965).
Epiphytes in some studies referred to those fungi isolated
from washed leaves, but in other studies, such as Kinkel
(1991), they referred to those fungi isolated from leaf
washings. In the present study, I focus on those epiphytes
isolated frequently from washed leaves by means of washing
methods (Harley and Waid 1955; Tokumasu 1980).
Endophytes have been defined as those fungi that can col-
onize internal leaf tissues at some time in their life without
causing apparent harm to their host (Petrini 1991). This ac-
counts for latent pathogens that may live without causing
symptoms in the host for some time in their life and for
saprobic fungi present in the cuticle layer or epidermis
(Rodriguez and Redman 1997). Here, I define endophytes as
those fungi that can be isolated frequently from healthy-
looking live leaves by means of surface disinfection methods
(Kinkel and Andrews 1988; Hata 1997). Further discussion
of the definition of endophytes is found in Wennström (1994)
and Wilson (1995).
The distinction between endophytes and epiphytes is some-
times unclear and some fungi can occur as endophytes and
epiphytes at the same time. Examples include Ascochyta sp.
on Fagus crenata Bl. (Osono 2002; Osono and Mori 2003),
Colletotrichum gloeosporioides (Penz.) Penz. et Sacc., and
Phomopsis sp. on Swida controversa (Hemsl.) Sojak (Osono
et al. 2004; Osono and Mori 2004, 2005). Some endophytes
have a more or less lengthy epiphytic phase in their life
cycle, while some epiphytes colonize the internal tissues es-
pecially at leaf senescence (Petrini 1986, 1991).
Berg and McClaugherty (2003) defined three stages during
the decomposition of leaf litter: early, late, and limit-value
stages. The early stage is characterized by relatively rapid
loss of soluble components, such as sugars and extractable
polyphenols, and nonlignified polymer carbohydrates, such
as cellulose and hemicellulose. The late stage is character-
ized by the decomposition of lignin, lignified holocellulose,
cutin, and tannin. Mass loss rate of litter is slowed down in
the late stage as compared with the early stage due to the
rate-retardant effect of lignin. The duration of the early or
late stages can vary among litter types; litter types with rela-
tively higher lignin content tend to show longer duration of
the late stages than those with relatively lower lignin con-
tent. The limit-value stage is characterized by an imperceptible
mass loss of litter. The final values or maximum decomposi-
tion limits are estimated using an asymptotic model, assuming
that decomposition rates approach zero and that remaining
litter mass approaches a final value (Howard and Howard
1974). Such final values are denoted as limit values for litter
decomposition (Berg and McClaugherty 2003). This review
follows the three-stage model to describe the particular stage
Occurrence of phyllosphere fungi on leaf litter
Phyllosphere fungi are divided into two groups: those that
occur on not only live leaves but also leaf litter and those
that occur exclusively on live leaves and not on leaf litter.
The mean number of epiphytic phyllosphere species that oc-
curred on leaf litter is 4.4 (n = 14), which accounts for 64%
on average of the total number of epiphytic species on live
leaves (Table 1). The mean number of endophytic phyllo-
© 2006 NRC Canada
702Can. J. Microbiol. Vol. 52, 2006
sphere species that occurred on leaf litter is 2.5 (n = 15),
which accounts for 67% on average of the total number of
epiphytic species on live leaves (Table 1). Thus, two-thirds
of the phyllosphere fungi on live leaves can also occur on
leaf litter on average, but the species number of such phyllo-
sphere fungi are highly variable among tree species. Phyllo-
sphere fungi that occur on leaf litter can be regarded as
saprobes or nectotrophic parasites that have saprobic ability
to colonize and establish on leaf litter, whereas others that
did not can be regarded as biotrophic parasites with a lim-
ited saprobic ability to colonize leaf litter.
To my knowledge, a total of 41 genera of phyllosphere
fungi have been reported from leaf litter of tree species in 19
genera (Table 2). The review in Table 2 includes those studies
that examined fungal colonization of both live and dead
leaves at the same time. Certain genera of fungi have been
commonly found to be well represented in the phyllosphere
fungi that occur on leaf litter. Such genera belong to asco-
mycetes and their anamorphs, while zygomycetes and basidio-
mycetes are generally conspicuously absent from the
phyllosphere fungal assemblages that occur on leaf litter,
except for basidiomycetous yeasts, such as Sporobolomyces.
This pattern of taxonomical distribution is also consistent
with the phyllosphere fungal association on live leaves (Hudson
1968; Boddy and Griffith 1989).
Species in Phoma, Lophodermium, Phomopsis, Colletotri-
chum, Coccomyces, Ascochyta, and Rhabdocline (Table 2)
are primarily known as pathogenic fungi; however, recent
studies have indicated that some species of these fungi are
present in the phyllosphere without causing any apparent
harm to their hosts and that they persist in fallen leaves after
leaf death (e.g., Soma and Saito 1979; Stone 1987; Osorio
and Stephan 1991; Tokumasu 1996; Kaneko and Kakishima
2001; Osono 2002; Kaneko et al. 2003; Koide et al. 2005b).
Species in Cladosporium, Aureobasidium, Pestalotiopsis, and
Alternaria are well-known phylloplane fungi obtained repeat-
edly from a wide variety of tree species. Hence, they are
common primary saprobes (Hudson 1968). These fungi are
normally encountered as epiphytes, but some can also occur
as endophytes (Boddy and Griffith 1989; Petrini 1991).
Studies of fungal succession have shown that these fungi can
persist on senescent leaves and leaf litter in the early stages
of decomposition (Hudson 1968, 1971).
Xylariaceous fungi and their anamorphs, such as Xylaria
and Geniculosporium, are common endophytes of tree leaves
(Petrini and Petrini 1985; Petrini et al. 1995). Some authors
have suggested that xylariaceous endophytes occur also on
leaf litter (Carroll and Petrini 1983; Laessøe and Lodge 1994),
but few studies have demonstrated this to date (Osono 2002,
2005; Osono et al. 2004). These fungi generally have a marked
ability to decompose plant residues such as wood and leaf
litter (Rogers 1979; Whalley 1996; Osono and Takeda 2002b).
Relative proportion of phyllosphere fungi in decomposer
The relative proportion of phyllosphere fungi in decomposer
fungal communities has been described as follows: Relative
proportion (%) = (the sum of isolation frequency of
phyllosphere fungi / the sum of isolation frequency of all
fungi on leaf litter) × 100.
The relative proportion of phyllosphere fungi varies among
fungal communities from different tree species and ranges
from 2% to 100% (Table 3). The relative proportion gener-
ally decreases as decomposition progresses (Watson et al.
© 2006 NRC Canada
Pinus taeda L.
Nothofagus truncata (Col.) Ckn.
Quercus rotundifolia Lam.
Eucalyptus viminalis Labill.
Fagus crenata Bl.
Swida controversa (Hemsl.) Sojak
Populus tremuloides Michx.
Ilex aquifolium L.
Corylus avellana L.
Halimione portulacoides (L.) Aellen
Betula verrucosa Ehrh.
Abies alba Mill.
Abies firma Sieb. et Zucc.
Quercus petraea (Matt.) Liebl.
Liquidambar styraciflua L.
Rhododendron pulchrum var. speciosum Hara
Rhododendron macrosepalum Maxim.
Rhododendron reticulatum D.Don
Rhododendron obtusum Planch.
Pieris japonica D.Don
Quercus germana Cham. et Schlecht
Quercus sartorii Liemb.
Watson et al. 1974
Sadaka and Ponge 2003
Osono et al. 2004
Wildman and Parkinson 1979
Mishra and Dickinson 1981
Aoki et al. 1992
Aoki et al. 1990
Okane et al. 1998
Okane et al. 1998
Okane et al. 1998
Okane et al. 1998
Okane et al. 1998
Note: nd, no data.
*Numbers in parentheses indicate the proportion (%) of total number on live leaves.
Table 1. Species number of phyllosphere fungi that occurred on leaf litter as compared with the total species number of phyllosphere
fungi encountered on live leaves.
1974; Aoki et al. 1990, 1992; Heredia 1993; Osono et al.
2004), but Osono (2002) found an increase of endophytes in
the internal tissues of F. crenata leaves during decomposi-
tion. The relative proportion also varied seasonally. For ex-
ample, the relative proportion on dead leaves of Eucalyptus
viminalis Labill. was 33%–35% in summer and winter but
© 2006 NRC Canada
704Can. J. Microbiol. Vol. 52, 2006
Picea PinusPseudotsugaBetulaCamellia CorylusEucalyptus
N, PN, P
P N, P
Total no. of plant species examined
Note: N, endophyte; P, epiphyte.
*1, Kendrick and Burges 1962; 2, Dickinson 1965; 3, Hering 1965; 4, Hogg and Hudson 1966; 5, Ruscoe 1971; 6, Watson et al. 1974;
13, Sieber-Canavesi and Sieber 1987, 1993; 14, Stone 1987; 15, Aoki et al. 1990; 16, Osorio and Stephan 1991; 17, Aoki et al. 1992; 18, Heredia 1993;
25, Osono and Mori 2004; 26, Koide et al. 2005b.
Table 2. Genera of phyllosphere fungi that occur on leaf litter in various host trees.
decreased to 2% in autumn and spring (Cabral 1985). The
relative proportion on dead leaves of Nothofagus truncata
(Col.) Ckn. was 18%–56% in autumn, winter, and spring,
but decreased to 0%–3% in summer (Ruscoe 1971). In fun-
gal communities of the leaf interior, the relative proportion
of endophytes is higher than that of epiphytes in some litter
© 2006 NRC Canada
FagusHalimioneIlex LiquidambarNothofagus PierisPopulus Quercus RhododendronSwida
PPP N, P
7. Mitchell and Millar 1978; 8, Soma and Saito 1979; 9, Wildman and Parkinson 1979; 10, Mishra and Dickinson 1981; 11, Cabral 1985; 12, Kuter 1986;
19, Okane et al. 1998; 20, Kaneko and Kakishima 2001; 21, Kaneko et al. 2003; 22, Osono 2002; 23, Sadaka and Ponge 2003; 24, Osono et al. 2004;
Table 2 (concluded).