Current Research in Environmental & Applied Mycology
Swe A1, Li J2, Zhang KQ2, Pointing SB1, Jeewon R1 and Hyde KD3*
1School of Biological Science, University of Hong Kong, Pokfulam Hong Kong
2Laboratory for Conservation and Utilization of Bio-resources, and Key Laboratory for Microbial Resources of the
Ministry of Education, Yunnan University, Kunming, P. R. China
3School of Science, Mae Fah Luang University, Chiang Rai, Thailand
Swe A, Li J, Zhang KQ, Pointing SB, Jeewon R, Hyde KD. 2011 – Nematode-Trapping Fungi.
Current Research in Environmental & Applied Mycology 1(1), 1–26.
This manuscript provides an account of nematode-trapping fungi including their taxonomy,
phylogeny and evolution. There are four broad groups of nematophagous fungi categorized based
on their mechanisms of attacking nematodes. These include 1) nematode-trapping fungi using
adhesive or mechanical hyphal traps, 2) endoparasitic fungi using their spores, 3) egg parasitic fungi
invading nematode eggs or females with their hyphal tips, and 4) toxin-producing fungi
immobilizing nematodes before invasion The account briefly mentions fossil nematode-trapping
fungi and looks at biodiversity, ecology and geographical distribution including factors affecting
their distribution such as salinity. Nematode-trapping fungi occur in terrestrial, freshwater and
marine habitats, but rarely occur in extreme environments. Fungal-nematodes interactions are
discussed the potential role of nematode-trapping fungi in biological control is briefly reviewed.
Although the potential for use of nematode-trapping fungi is high there have been few successes
resulting in commercial products.
Key words – Ascomycetes – Biocontrol – Biodiversity – Fossil fungi – Fungi – Nematodes –
Received 4 June 2011
Accepted 6 June 2011
Published online 25 June 2011
*Corresponding author: Kevin D. Hyde – e-mail – firstname.lastname@example.org
Table of contents
Taxonomy, phylogeny and evolution of nematode-trapping fungi
Background of generic classification
Phylogenetic significance and evolution of trapping devices
Ancient nematode-trapping fungi
Biodiversity of nematode-trapping fungi
Ecology, occurrence and geographical distribution
Factors affecting the distribution of NTF
Effect of salinity
Host recognition, adhesion, host specificity and infection process
Extracellular enzymes involved in nematode infestation process
Biological control of nematodes
Use of NTF to control animal gut nematodes
Use of NTF in traditional or natural biocontrol of plant nematodes
Using advance techniques
Commercialization of products
There are four broad groups of nemato-
phagous fungi categorized based on their
mechanisms of attacking nematodes (Liu et al.
2009). These include (1) nematode-trapping
fungi using adhesive or mechanical hyphal
traps, (2) endoparasitic fungi using their spores,
(3) egg parasitic fungi invading nematode eggs
or females with their hyphal tips, and (4) toxin-
producing fungi immobilizing nematodes
before invasion (Kendrick et al. 2001, Liu et al.
The first nematode-trapping fungus to be
described was Arthrobotrys oligospora Fresen.
in 1852, but at that time its predatory habit was
unknown. The predatory habit was first obser-
ved 36 years later by Zopf (1888). Since nema-
tode-trapping fungi have considerable potential
for biological control of nematodes, there have
been extensive studies and reviews on their
taxonomy, phylogeny, biology, and ecology
(Cooke 1963, Kerry 1987, Sayre & Walter
1991, Sikora 1992, Kerry & Hominick 2002,
Morton et al. 2004, Dong & Zhang 2006,
Sikora et al. 2007). In this review, aspects such
as taxonomy, phylogeny, diversity, and eco-
logy of nematode-trapping fungi and their
potential in use in biocontrol of nematodes are
Taxonomy, phylogeny and evolution of
Background of the generic classification
Nematode-trapping fungi are a hetero-
geneous group of anamorphic ascomycetes
where species are defined primarily based on
conidial characteristics such as size, septation,
and type of conidiogenous cells (Oudemans,
1885, Subramanian, 1963). This has resulted in
considerable ambiguity and confusion in inter-
generic classification of these organisms. Since
the discovery of predacious activity in Arthro-
botrys oligospora (Zopf, 1888), nematode-
trapping fungi have attracted much interest
amongst mycologists. Many generic names
have been given to nematode-trapping fungi
but the basis on which species were circumscri-
bed to different genera was unclear and sub-
jective. Since 1930, nematode-trapping fungal
have been described and classified mostly in
Arthrobotrys Corda, Dactylaria Sacc, and Dac-
Corda (1839) established the genus Ar-
throbotrys with A. superba Corda as the type
species. Characteristics of this genus are hya-
line conidiophores which produce conidia
asynchronously on short denticles at swollen
conidiogenous heads or clusters of pronounced
denticles (De Hoog 1985). Conidia are subhya-
line, obovoidal or clavate and (0–)1(–6)-sep-
tate. Trapping devices are constricting rings,
adhesive nets, hyphae or adhesive knobs (De
Hoog 1985). Due to these broad morphological
criteria the delimitation from Arthrobotrys is
sometimes problematic, particularly in Dactyl-
ella species which form more than one or two
conidia on each conidiophore (Cooke &
Dickinson 1965). Based on this reason, Van
Oorschot (1985) restricted Dactylella to
species with fusiform, multi-septate conidia,
while Arthrobotrys species generally have
ovoidal to clavate, 0–3-septate conidia. Van
Oorschot (1985) recognized 28 species of Ar-
throbotrys. Schenck et al. (1977) expanded the
genus to 47 species. After Schenck et al. (1977)
transferring all predacious species formerly
described in Dactylaria to Arthrobotrys, Dacty-
laria was no longer tenable for nematode-
trapping species. Recent classification based
mostly on DNA sequence data has resulted in
the transfer of species characterized by adhe-
sive networks to Arthrobotrys (Scholler et al.
1999). Currently, there are 120 records of
Arthrobotrys species but this includes basio-
nyms and synonyms (Index Fungorum, 2011).
A more realistic estimate is 63 (Kirk et al.
Monacrosporium was introduced by
Oudemans (1885) with two species, Monacro-
Current Research in Environmental & Applied Mycology
sporium elegans Oudem. and M. subtile
Oudem. This generic name has been used by
many authors for several species following the
opinion of Oudemans (1885). Subramanian
(1964) later selected M. elegans as lectotype
species for this genus, highlighting the inflated
middle cell of the conidia as the distinguishing
generic criterion, and transferred a large num-
ber of nematode-trapping fungi from Dacty-
lella species to Monacrosporium. Rubner
(1996) revised most predacious hyphomycetes
in Dactylella and Monacrosporium to deli-
mitate between the two genera. Scholler et al.
(1999), however, proposed a new genus
concept for predatory anamorphic Orbiliaceae
and the genus Monacrosporium was discarded.
Many nematode-trapping fungal species are
homeless and Monacrosporium is used as their
current name. Currently, 74 taxa are listed in
Index Fungorum (Index Fungorum, 2011),
while Kirk et al. (2008) estimate there to be 68
Based on results obtained from morpho-
logical and molecular characters, Hagedorn &
Scholler (1999) and Scholler et al (1999)
proposed that nematode-trapping fungi should
be organized in four genera: Dactylellina M.
Morelet characterized by stalked adhesive
knobs including species characterized by non-
constricting rings and stalked adhesive knobs;
Gamsylella M. Scholler, Hagedorn & A.
Rubner characterized by adhesive branches and
unstalked knobs; Arthrobotrys characterized by
adhesive networks; and Drechslerella Subram.
characterized by constricting rings. Li et al.
(2005) emended genus Gamsylella and trans-
ferred species from Gamsylella to Arthrobotrys
and Dactylellina. Gamsylella was not treated
by them as a valid genus as proposed by
Scholler et al. (1999). Yang & Liu (2006) later
proposed to combine Dactylellina and Gam-
sylella into one genus based on molecular
phylogenetic analyses. However, there are still
debates concerning the generic concepts of
The genus Dactylellina was described by
Morelet (1968) with Dactylellina leptospora
(Drechsler) M. Morelet as type species.
Scholler et al. (1999) later transferred all preda-
cious species forming adhesive stalked knobs
and non-constricting trapping rings to this
genus. Thirty-two names are listed for this
genus in Index Fungorum (Index Fungorum,
2011). The current names for most species in
the genus are in Arthrobotrys (1) Dactylella (3)
Gamsylella (4) and Monacrosporium (8) and
only seven species are listed under Dactylellina
while the remaining are anamorphic Orbilia
(Index Fungorum 2011)
Subramanian (1964) based on the type species,
Drechslerella acrochaeta (Drechsler) Subram.
Scholler et al. (1999) later revised and trans-
fered all predacious species forming con-
stricting rings to this genus. Fourteen names
are listed in this genus in Index Fungorum
(Index Fungorum 2011), while Kirk et al.
(2008) estimated there are one species. Species
Fungorum (2011) currently lists seven names
as anamorphic Orbilia, while the other species
are organized in Arthrobotrys (3), Dactylella
(1), Geniculifera (1) and Monacrosporium (3).
Gamsylella was described by Scholler et
al. (1999) based on G. arcuata (Scheuer & J.
Webster) M. Scholler, Hagedorn & A. Rubner
Scholler et al. (1999) proposed Gamsylella as a
new genus combining all predacious species
that formed adhesive columns and unstalked
knob devices to this genus. Li et al. (2005) later
transferred those species to Arthrobotrys and
Yang & Liu (2006) combined this genus with
Dactylellina based on molecular phylogenetic
analyses. Six taxa belonging to Gamsylella
were reported by Index Fungorum (2008) and
Kirk et al. (2008). Nevertheless, a placement of
this genus based on phylogenetic analyses still
remains in questioning and therefore it should
Dactylella was proposed by Grove
(1884) based on the type species Dactylella
minuta Grove a nematode-trapping species.
The genus is characterized by erect, simple,
hyaline conidiophores with conidia produced
singly at the apex. Conidia are ellipsoidal,
fusoid or cylindrical, one-celled at first and
later having 2 to many septa. This genus has
been emended several times and both non-
predacious and predacious fungi have been
included (Subramanian, 1963), Schenck et al.
1977; de Hoog & Oorschot, 1985; Zhang et al.
1994). Rubner (1996) revised the generic
concept of Dactylella and excluded the
nematode-trapping species. However, several
nematode predacious species still remain in
Dactylella (Liu & Zhang 2003, Zhang et al.
2005). This genus was revisited by Liu &
Zhang (2003) and was separated into three
groups such as Dactylella, Vermispora and
Brachyphoris. One hundred and eight Dac-
tylella species are listed in Index Fungorum
(Index Fungorum, 2011) where there are 62
estimated species (Kirk et al. 2008).
Phylogenetic significance and evolution of
Morphology-based classification of fungi
has been demonstrated to be inadequate in
reflecting natural relationships among fungi.
Phylogenetic analyses using molecular data,
thus, have been used for more than a decade to
assess phylogenetic relationships and also to
revaluate the phylogenetic importance of
various morphological characters (Cai et al.
2009). The first notable phylogeny study on
nematode-trapping fungi was that of Rubner
(1996). He used trapping devices to rationalize
the classification of nematode-trapping fungi
using molecular data. Later phylogenetic
studies based rDNA sequence analysis also
found that trapping devices are more infor-
mative than other morphological characters in
delimiting genera (Liou & Tzean, 1997, Pfister
1997, Ahrén et al. 1998, Scholler et al. 1999,
Ahrén & Tunlid 2003, Kano et al. 2004, Li et
al. 2005, Yang & Liu 2006, Yang et al. 2007a,
Liu et al. 2009). For example, Ahrén et al.
(1998) revealed nematode-trapping fungi
grouping in three lineages based on different
types of trapping devices. Scholler et al. (2009)
classified nematode-trapping fungi into four
genera using 18S and ITS rDNA analysis. Li et
al. (2005) re-evaluated the placement of nema-
tode-trapping genera based 28S, 5.8S and β-
tubulin analysis and the establishment of
Gamsylella proposed by Scholler et al. (1999)
was criticized and not accepted. Yang & Liu
(2006) proposed to combine Dactylellina and
Gamsylella into one genus and Yang et al.
(2007b) traced the evolution of trapping
devices in predatory fungi based on analyses of
ITS, rpb2, ef-1, β-tubulin sequences. However,
the morphological affinity of Gamsylella to
genera Arthrobotrys and Dactylellina are still
unclear and intergeneric relationships of Gam-
sylella and its allies are still unresolved.
The evolution of nematode-trapping
devices has been discussed by Li et al. (2005)
and Yang et al. (2007a). Phylogenetic analysis
of nucleotide sequences demonstrated that
early trapping structures evolved along two
lines, yielding two distinct trapping mecha-
nisms. One lineage developed into constricting
rings and the other into adhesive traps. The
adhesive network separated early. The adhesive
knob evolved through stalk elongation, with a
final development of nonconstricting rings. Li
et al (2005) on the otherhand showed a
Orbiliales ITS and 28s rDNA-specific
PCR primers which directly detect nematode-
trapping fungi without culturing were deve-
loped by Smith & Jaffee (2009). The authors
believe the combined use of Orbiliales-specific
primers and culture-based techniques may
benefit future studies of nematophagous fungi
and can also be used to screen fungal isolates
for phylogenetic placement in the Orbiliales.
Ancient nematode-trapping fungi
An early record of a nematode-trapping
fungus is that of Palaeoanellus dimorphus
which lived approximately 100 million years
ago in a limnetic-terrestrial microhabitat
(Schmidt et al. 2008). The fossil probably
represents an anamorph of an ascomycete with
unicellular hyphal rings as trapping devices and
formed blastospores from which a yeast stage
developed. The authors speculated that because
predatory fungi with regular yeast stages are
not known from modern ecosystems, the
fungus is assumed to not be related to any
recent nematode-trapping fungi and is probably
an extinct lineage. Alternatively, it may be that
we may yet find this strange species in modern
Biodiversity of nematode-trapping fungi
Hawksworth (1991) estimated that there
are 1.5 million global species of fungi and this
has been accepted as a working figure by many
mycologists. There have been several other
publications debating estimates of fungal spe-
cies (Hammond 1992, Cannon 1997, Huhndorf
& Lodge 1997, Hyde et al. 2007). Neverthe-
less, however many fungi exist in nature, there
are few (ca 100,000) that have been described.
Hyde (2001) pointed out that most of the
undescribed fungi are microfungi and they may
occur in poorly investigated areas and less
explored niches, substrates, hosts abd habitats.
Current Research in Environmental & Applied Mycology
There has been a relatively large numbers
of studies on fungal diversity such as in
extreme environments (Connell et al. 2006,
2008, Fell et al. 2006, Porras-Alfaro et al.
2008), in marine habitats (Hyde 1996, Poon &
Hyde 1998, Barata 2006, Hyde & Sarma 2006,
Lai et al. 2007, Laurin et al. 2008, Nambiar et
al. 2008), in freshwater habitats (Tsui et al.
2000, Cai et al. 2003, Fryar et al. 2004, Tsui &
Hyde 2004, Duarte et al. 2006, Sole et al.
2008), in terrestrial habitats (Hyde & Alias
2000, Sun & Liu 2008, Wakelin et al. 2008a),
in areas of environmental pollution (Indra &
Meiyalagan 2005, Zafar & Ahmad 2005, Ellis
et al., 2007, Duarte et al. 2008, Stefanowicz et
al. 2008, Turnau et al. 2008), on decaying litter
(Tsui et al. 2000, Cai et al. 2003, Tsui & Hyde
2004, Gulis et al. 2008, Lonsdale et al. 2008).
However, there are relatively few diversity
studies of nematode-trapping fungi (Hao et al.
2005, Mo et al. 2006, 2008, Saxena 2008). Hao
et al. (2005) studied the diversity of nematode-
trapping from aquatic habitats; Mo et al. (2006,
2008) studied diversity of nematode-trapping
fungi from heavy metal polluted soils. Interes-
tingly, Mo et al. (2008) revealed that the
diversity index of nematode-trapping fungi was
positively correlated with concentration of
Diversity study on nematode-trapping
fungi using traditional methods has involved in
several processes, such as sample collection,
isolating with nematodes, preliminary morpho-
logical examination of fungal structures, single
spore isolations for examining trapping devices
and identifying species. These methods have
been commonly used because of their low cost
and the fact that they are easy to conduct
(Jeewon & Hyde, 2007). The traditional
methods used in nematode-trapping fungi
largely rely on the discovery of fungal spores
in natural environments. Hyde & Goh (1998)
pointed out that the incubation of substrates
effects the structure of fungal communities
recorded. Jeewon & Hyde (2007) suggested
that a large number of fungi existing as
mycelial propagules or dormant spores and can
be numerically dominant populations but in
their natural environment they may have little
Molecular techniques have been used to
investigate fungal diversity. The emergence of
these molecular methods overcomes the limita-
tions associated with traditional approaches
and isolation based methods. Jeewon & Hyde
(2007) recently reviewed advance molecular
techniques versus traditional techniques that
are used in the detection and diversity of fungi
from environmental samples. Molecular me-
thods used in assessing fungal diversity have
been employed such as Denaturing Gradient
Gel Electrophoresis (DGGE), Terminal Re-
striction Fragment Length Polymorphism (T-
RFLP), Amplified rDNA Restriction Analyses
(ARDRA), Amplified Random Intergeneric
Spacer Analysis (ARISA), and Temperature
Gradient Gel Electrophoresis (TGGE). Recen-
tly PCR-based fingerprinting techniques have
been applied to assess fungal diversity. Oligo-
nucleotide Fingerprinting of Ribosomal RNA
Gene (ORFG), a new method that sorts arrayed
rRNAgene clones into taxonomic clusters
through a series of hybridization experiments
(Kirk et al. 2004). Most frequently used
methods in assessing fungal diversity are Dena-
turing Gradient Gel Electrophoresis (DGGE)
and Terminal Restriction Fragment Length
Polymorphism (T-RFLP). Wakelin et al.
(2008b) used a semi-quantitative nested quan-
titative PCR approach and a DGGE approach
to detect soil total Fusarium communities on
maize root. Li et al. (2008) used a combination
of plate count, DGGE and clone library
analyses to investigate the effect of metha-
midophos on soil fungi community in micro-
cosms. Raberg et al. (2005) used T-RELP to
detect the early stages of wood decay and this
was compared with microscopic evaluation.
Yet, there is no study on diversity of nematode-
trapping fungi using molecular methods.
Although traditional methods and mole-
cular based methods both have disadvantages
and advantages, traditional methods presently
still have some advantages over molecular
based techniques in assessing fungal diversity.
Most of the molecular techniques involved do
not discriminate between active and inactive
stages of fungi (Jeewon & Hyde, 2007). Data
yielded from molecular techniques are difficult
to employ with respect to ecology and function
(e.g. correlation analysis between environ-
mental factors and fungal communities). More-
over, traditional methods often involve less
cost and no expensive specialized laboratory
equipment is needed, which are often not
available in developing world. In contrast, cur-
rent knowledge on the diversity and detection
and the community structure of the nematode-
trapping fungi in nature is still rudimentary.
Improvement in traditional approaches com-
bined with molecular techniques will provide a
better understanding of these fungal commu-
nity systems in nature.
There have been numerous surveys on
the occurrence of nematophagous fungi, which
have shown that the fungi are found throughout
the world and in all types of climate and
habitats (Duddington 1951, 1954, Gray 1987,
Sunder & Lysek 1988, Boag & Lopez-Llorca
1989, Saxena & Mukerji 1991, Dackman et al.
1992, Liu et al. 1992, Saxena & Lysek 1993,
Rubner 1994, Persmark & Nordbring-Hertz
1997, Persmark & Jansson 1997, Jaffee 2003,
Ahrén et al. 2004, Hao et al. 2005, Jaffee &
Strong 2005, Farrell et al. 2006, Su et al. 2007,
Mo et al. 2008, Saxena 2008). The teleomorph
state Orbilia of nematode-trapping fungi have
been recorded on decaying wood from terres-
trial and freshwater habitats (Pfister 1994,
Webster et al. 1998, Liu et al. 2005, 2006,
Zhang et al. 2006, 2007, Yu et al. 2007), and
the anamorphic states also commonly occur in
terrestrial, freshwater and marine habitats (Hao
et al. 2004, Li et al. 2006, Swe et al. 2008a, b,
2009), but rarely occur in extreme environ-
ments (Onofri & Tosi 1992). There have been
several studies on nematode-trapping fungi
because of their potential in biological control,
however most of these have concentrated on
agriculture and animal husbandry or forestry
(Kerry & Hominick 2002, Ahrén & Tunlid
2003, Jaffee & Strong 2005, Dong & Zhang
2006, Su et al. 2007) or freshwater
environments (Maslen 1982, Hao et al. 2005).
Numerous fungal-animal associa-tions have
been reported from aquatic habitats. The first
report of marine predacious fungi was three
zoophagous forms discovered in brackish water
(Jones 1958). Currently, more than 50 species
of predacious hyphomycetes have been
recorded from aquatic habitats (Ingold 1944,
Peach 1950, 1952, Johnson & Autery 1961,
Anastasiou 1964, Hao et al. 2004, 2005).
Arthrobotrys dactyloides Drechsler was the
first species of nematode-trapping fungi to be
reported from brackish water (Johnson &
Autery 1961) while Swe et al. (2008a, b, 2009)
recorded several species from mangroves.
Factors affecting the
The distribution and occurrence of nema-
tode-trapping species and groups of fungi is
associated with specific soil variables in parti-
cular pH, moisture, nutrients (N, P, K), heavy
metal and nematode density (Gray 1985,
Persson & Baath 1992, Jaffee 2004b, Sánchez-
Moreno et al. 2008, Mo et al. 2008). Gray
(1988) revealed that soil nutrients such as N, P
and K were all positively correlated with nema-
tode density. Species with stalked knobbed
trapping devices (Dactylellina) and those
species with constricting rings (Drechslerella)
were isolated more readily from richer soils
which contained a greater density of nema-
todes. However, net-forming species (Arthro-
botrys) are largely independent of soil fertility,
especially low K (Burges & Raw 1967).
Interestingly, Mo et al. (2008) found that
diversity of nematode-trapping was positively
correlated with lead concentration. These soil
variables are known to vary with depth, as are
the densities of soil bacteria, fungi and nema-
todes (Mankau & McKenny, 1976, McSorley
et al. 2006) and a high level of nematode-
trapping activity have been recorded from the
rhizosphere area (Peterson & Katznelson 1964,
Mitsui et al. 1976, Persmark & Jansson 1997,
Wang et al. 2003, McSorley et al. 2006).
However, there are large variations depending
on plant and soil types (Jansson & Lopez-
Llorca 2001). The species of nematode-
trapping fungi vary with depth (Gray & Bailey
1985). Peterson & Katznelson (1964) revealed
that the greatest diversity occurred in the upper
10–30 cm of soils, and this was a positive
correlation between the population density of
nematophagous fungi and root-knot nematodes
in peanut fields. Gray & Bailey (1985) have
examined the vertical distribution of nemato-
phagous fungi in soil cores collected from a
deciduous woodland, predators forming con-
stricting rings, adhesive branches and adhesive
knobs are restricted to the upper litter and
humus layer, while the net-forming predators
and endoparasites were isolated at all depths,
although they are significantly more abundant
Current Research in Environmental & Applied Mycology
in the lower mineral-rich soils. In contrast,
predators able to form traps spontaneously are
restricted to the organic soils of the hemi-
edaphic zone which are rich in nematodes.
Nematophagous fungi are small enough to be
affected by micro-climates within the soil
(Gray 1985). Hao et al. (2005) observed that
the nematode-trapping were not detected
deeper than four meter in a freshwater pond.
Several studies have also been carried out on
horizontal distribution (Persson et al. 2000,
Segers et al. 2000, Minglian et al. 2004). For
example, Persson et al. (2000) studied the
growth and dispersion of Arthrobotrys superba
Corda under natural conditions determined by a
radioactive tracing technique.
The effect of major biotic and abiotic
variables such as soil moisture, organic matter,
pH, nematode density, soil nutrients (Gray
1987) and submerged water condition on the
distribution of nematode-trapping fungi has
been extensively studied. The diversity was
highest at the depth of 20 cm and no nematode-
trapping fungi were found at the depth of 4 m
(Hao et al. 2005). Heavy metals concentrations
affected distribution of NTF and was not nega-
tively affected by Pb concentration (Mo et al.
2006, Mo et al. 2008). However, treatment
with ethylenediamine tetra-acetic acid (EDTA)
resulted in detecting various stages of fungi of
aggregates in the sediments from -5000 m deep
sea, gradually revealing the presence of fungal
hyphae within them (Damare & Raghukumar
2008). Gray (1987) pointed out that the endo-
parasitic nematophagous fungi are obligate
parasites, and unlike the predatory fungi, they
appear to be unable to live as saprotrophs in the
soil. He also suggested that non-specific me-
thod of attraction may rely on a greater density
of soil nematodes to ensure infection, as com-
pared with parasites which produce adhesive
conidia (Gray 1987).
Gray (1988) revealed that soil nutrients
N, P and K were all positively correlated with
nematode density. Based on his results, knob-
forming predators which rely on their ability to
produce traps spontaneously are isolated from
soils with low concentration of nutrients, while
those species with constricting rings are iso-
lated from richer soils which contain a greater
density of nematodes. Net-forming species are
largely independent of soil fertility, although
generally they are isolated from soils with
limited nutrients, especially low K (Burges &
Effect of salinity
The effect of salinity on fungal growth in
yeasts and moulds (Blomberg & Adler 1993,
Dan et al. 2002), marine fungi, mycorrhizal
fungi and some wood-rotting basidiomycetes
has been studied (Ritchie 1959, Davidson
1974, Byrne & Jones 1975, Jones & Byrne
1976, Kohlmeyer & Kohlmeyer 1979, Siegel &
Siegel 1980, Hyde et al. 1987, Lorenz &
Molitoris 1992, Clipson & Hooley 1995, Akira
& Tadayoshi 1996, Castillo & Demoulin 1997,
Juniper & Abbott 2006, Sharifi et al. 2007).
Some research has studied the effects of
salinity on the growth and the parasitic ability
of the parasitic fungi, with most having studied
the parasites of mosquitoes (Harrison & Jones
1971, Lord & Roberts 1985, Gardner & Pillai
1986, Lord et al. 1988, Kramer 1990, Teng et
al. 2005). The effect of abiotic factors, such as
temperature, pH, light, UV and nutrition on the
trapping efficacy of nematode-trapping fungi
has been intensively studied (Ciordia & Bizzell
1963, Gray 1985, 1988, Morgan et al. 1997,
Fernandez et al. 1999, Gronvold et al. 1999,
Zucconi et al. 2002, Jaffee 2006, Kumar &
Singh 2006a, 2006b, Paraud et al. 2006, Sun &
Liu 2006, Gao et al. 2007).
Speciation, the evolution of one species
into two, is one of the most fundamental
problems to appreciate in biology (Giraud et al.
2008). Numerous reviews on the modes of spe-
ciation in fungi have been published (Natvig &
May 1996, Burnett 2003, Kohn 2005, Giraud et
al. 2008). ‘Ecological speciation’, as defined
by Rundle & Nosil (2005) is ‘the process by
which barriers to gene flow evolve between
populations as a result of ecologically based
divergent selection’. Fungi are excellent
models for the study of eukaryotic speciation in
general (Burnett 2003, Kohn 2005). However,
they are still rarely included in general reviews
on this subject. Giraud et al. (2008) explained
why fungi is a excellent models for studying
speciation; (1) Many fungi can be cultured in
vitro and many experiments on mating types
among fungal species have been reported, (2)
Fungi display a huge variety of life cycle and
geographical and ecological distributions,
allowing the study of parameters most signi-
ficantly influencing the speciation processes,
(3) Numerous species complexes are known in
fungi, encompassing multiple recently diverged
sibling species which allows investigations on
the early stages of speciation.
It is important to define a species before
studying speciation. The traditional species
concept is the morphological species concept
(MSC) and in fungi is mainly based on mor-
phology and reproductive behavior (Taylor et
al. 2000). On the other hand, some mycologists
have debated that species concepts should also
be considered on an ecological basis as well as
on nucleotide divergence (ESC, ecological
species concept and phylogenetic species
concept, PSC) (Harrington & Rizzo 1999).
Nevertheless, the most commonly used species
criterion for the fungi has been the morpho-
logical species concept. However, many cryp-
tic species have been discovered within
morphological species, using the biological
species concept (e.g. Anderson & Ullrich 1979)
or the genealogical goncordance phylogenetic
species recognition, GCPSR (Taylor et al.
2000). Moreover, the phylogenetic species
concept uses the phylogenetic concordance of
multiple unlinked genes to indicate a lack of
genetic exchange and thus evolutionary inde-
pendence of lineages. Thus, species can be
identified which cannot be recognized using
other species criteria due to the lack of
morphological characters (Giraud et al. 2008).
Recently, the genealogical concordance phylo-
genetic species recognition criterion is also
useful tool or criterion in fungi and is most
widely used within the fungal kingdom
(Johnson et al. 2005, Pringle et al. 2005, Le
Gac et al. 2007).
Knowing which genes are involved in
reproductive isolation may help to get a better
understanding of speciation processes (Giraud
et al. 2008). There has been little research to
understand the genetics of speciation in fungi.
Four of five genes were involved in the inter-
sterility among Heterobasidion species (Chase
& Ullrich 1990). DNA multi-locus typing
showed that different clones of the fungus are
associated with different environments (Fisher
et al. 2005), which indicated that adaptation to
new environments constrains the organism’s
ability to successfully disperse in nature. The
population structure in asexual parasites may
reflect host or habitat adaptation at all loci,
because selection at one locus results in hitch-
hiking of the whole gene (Giraud et al. 2008)
‘The ecological species concept (ESC)’
and ‘ecological speciation’ have been proposed
as an important component of speciation
among widely spread and diverse living orga-
nisms such as fish (Hatfield &Schluter 1999),
lizards (Ogden & Thorpe 2002, Richmond &
Reeder 2002), and insects (Via 1999, Via et al.
2000, Rundle & Nosil 2005, Barat et al. 2008).
There have been some studies on host specia-
tion in fungi (Antonovics et al. 2002, Couch et
al. 2005, Lopez-Villavicencio et al. 2005).
However, ecological speciation in fungi has not
received much attention. One of the first
studies on ecological speciation was on the
insect pathogenic fungi, Metarhzium anisoplaie
by Bidochka et al. (2001) and in their study M.
anisoplaie clearly separated into two genetic
groups based on two habitats; agriculture and
forest. Another study was on a plant pathogen
of grasses, Claviceps purpurea and the result
shown that terrestrial isolates were signifi-
cantly divergent from other isolates of wet
/shady and salt marsh habitats (Douhan et al.
2008). There have however, been few related
studies on nematode-trapping fungi. Geogra-
phical speciation among 22 isolate of Dudding-
tonia flagrans (Dudd.) R.C. Cooke suggested
that there was no or little genetic variation
(Ahrén et al. 2004). However, using selective
fragment length amplification, Mukhopad
hyaya et al. (2004) found that D. flagrans
isolates are genetically diverse despite their
Host recognition, adhesion, host specificity
and infection process
Nematophagous fungi are an important
group of soil microorganisms that can suppress
the populations of plant and animal parasitic
nematodes. They can be grouped into three
categories according to their mode of infesta-
tion: nematode-trapping, endoparasitic, and
toxic compound producing (Nordbring Hertz &
Tunlid 2000). The pathogenic mechanisms
Current Research in Environmental & Applied Mycology
during the infestation process are diverse. They
can be mechanical through the production of
specialized capturing devices, or through
production of toxins that kill nematodes.
During infection, a variety of virulence factors
may be involved against nematodes by
nematophagous fungi. The infection processes
and host range of nematophagous fungi have
been studied using various techniques such as
light and low temperature electron microscopy
and bioassays and have been supported by
biochemical, physiological, immunological and
molecular techniques (Thorn & Barron 1984,
Murray & Wharton 1990, Jansson et al. 2000).
The ultrastructure of the nematode-trapping
devices has been extensively studied (Heintz &
Pramer 1972, Nordbring-Hertz & Stalhammar-
Carlemalm 1978, Dijksterhuis et al. 1994). The
mode of infection by nematophagous fungi has
been reviewed by Yang et al. (2007c).
Research on attraction of nematodes to
fungi has focused on the host-finding behavior
of fungal-feeding nematodes (Bordallo et al.
2002, Wang et al. 2010). Nematophagous fungi
are attracted to plant and animal parasitic
nematodes and microbivorous nematodes
(Balan & Gerber 1972, Jansson & Nordbring-
Hertz 1979, 1980). Zuckerman & Jansson
(1984) review nematode chemotaxis and
possible mechanisms of host/prey recognition.
The attracttion of nematodes to nematophagous
fungi has been studied using culture filtrates
and macerated mycelium
Nordbring-Hertz 1979) as well as living fungi
(Jansson & Nordbring-Hertz 1980). One of the
earliest observations described the attraction of
the plant parasitic nematode Meloidogyne
incognita to tomato roots grown in sterile Petri
plates (Zuckerman & Jansson 1984). Pena-
gellus redivivus was attracted to approximately
75% of the mycelium of nematophagous fungi
tested (Kuyama & Pramer 1962, Nordbring-
Hertz 1973, Barron 1977, Jansson 1982).
Fungal feeding and plant parasitic nematodes
seem to respond differently to fungal
chemotactic factors (Ward 1973, Field &
Webster 1977, Zuckerman & Jansson 1984,
Zhao et al. 2007), e.g. fungal feeding
nematodes were attracted to all fungi tested,
while some plant parasitic nematodes were
attracted to very few fungi (Field & Webster
1977); the volatiles produced by the host plants
could be the basis of a chemoecological
relationship between plant parasitic nematodes
and their vector insects (Zhao et al. 2007).
Jansson (1982) showed that the presence of
trapping devices on the hyphae increases the
ability of fungi to attract nematodes. Trapping
devices could be produced spontaneously, or
their formation can be induced by nematodes
or proteinaceous compounds (Jansson &
Nordbring-Hertz 1979). The connection be-
tween attraction ability and degree of para-
sitism was also confirmed when the parasitic
ability of the fungi was tested in soil micro-
cosms (Tunlid et al. 1992, Dijksterhuis et al.
More recently, Wang et al. (2009) invest-
tigated the attraction of Esteya vermicola J.Y.
Liou, J.Y. Shih & Tzean to the pinewood
nematode. The endoparasitic fungus was
attracted to living mycelia and exudative
substances of E. vermicola reflecting the
dependence of the fungi on nematodes for
nutrients. Attractive substances appeared to be
avolatile exudatives and volatile diffusing
Adhesion to host is an essential require-
ment for fungal parasites to be able to infect.
Most of pathogenic and parasitic fungi,
adhesion is mediated by an extracellular matrix
(ECM) or sheath on the fungus (O'Connell
1991, Åhman et al. 2002, Alston et al. 2005).
Tunlid et al. (1992) suggested that extracellular
adhesions are produced on the surfaces of
spores, appressoria and trapping devices and
are essential for infection. The adhesive layer
has a fibrillar structure with residues of neutral
sugars, uronic acid and proteins (Whipps &
Lumsden 2001). Jansson & Lopez-Llorca
(2001) suggested that the adhesion process is
much more complicated than a simple receptor-
ligand binding, and may involve the activity of
the fungal infection structure as well as the
surface of living nematodes. Initial contact
with the host cuticle may be followed by inter-
actions with specific receptors, reorganization
of surface polymers to strengthen the
adhesions, changes in morphology and the se-
cretion of specific enzymes (Jansson &
Nordbring-Hertz 1988, Kerry 2000, Abiko et
al. 2005). These processes and the structures
involved have been extensively reviewed
(Kerry et al. 1993).
Extracellular enzymes involved in nematode
During the infection process, the cuticle
must be penetrated, the nematode is immo-
bilized, and the prey is finally invaded and
digested. This sequence of infection seems to
be present in most nematophagous fungi, but
the molecular mechanisms are not well
understood (Lopez-Llorca & Duncan 1988,
Dackman et al. 1989). However, several nema-
tophagous fungi have been reported to produce
nematotoxins that immobilize or kill nema-
todes, and ultrastructural and histochemical
studies suggest that the penetration of the
nematode cuticle involves the activity of
hydrolytic enzymes (Schenck et al. 1980).
Enzymes involved in the infection processes of
nematophagous fungi are being cloned and
characterized. Also, many scientists have per-
formed screens of nematophagous fungi in
order to identify the structures of compounds
produced in vitro that may have nematicidal
action. There is a recent review on the modes
of infection and the biochemical properties of
the serine proteases enzyme (Yang et al.
Studies of insect and other parasitic fungi
have shown that the chemical composition of
the surface of the host is important for the
hydrolytic enzymes involved in infection
(Sahai & Manocha 1993). More detailed
studies on Metarhizium anisopliae (Metschn.)
Sorokīn has shown that proteases are produced
more rapidly and in higher concentrations than
other cuticle-degrading enzymes (Goettel et al.
1989, Veenhuis et al. 1985). There is much
evidence related to protease and chitinase
production by entomophagous fungi (Jansson
& Friman 2000, Tikhonov et al. 2002). Pro-
teases are the only enzymes produced in large
amounts (Maher 1993). Furthermore, the pro-
tein coating of chitin microfibrils in extracellu-
lar barriers of insects and nematodes would
render microibrils relatively non-amenable to
enzymolysis (Rong De et al. 2005). It can
therefore be assumed that the activity of
proteases is more important than chitinase in
host penetration. However, the importance and
function of extracellular proteases in the
infection process between nematodes and fungi
are still unknown.
The first study on proteases and their
involvement in the infection and immobili-
zation of nematodes by the nematode-trapping
fungi, Arthrobotrys oligospora was by Tunlid
& Jansson (1991). Subsequently, a first
pathogenic serine protease (P32) from the
nematode egg parasite Verticillium suchla-
sporium W. Gams & Dackman was purified
and characterized by
Robertson (1992). Recently more pathogenic
serine proteases were detected, characterized,
and cloned by several scientists, for examples
Aoz1 from Arthrobotrys oligospora (Zhao et
al. 2005), M1x from
microscaphoides Xing Z. Liu & B.S. Lu (Wang
et al. 2006a), and Ds1 from Dactylella
shizishanna X.F. Liu & K.Q. Zhang (Wang et
al. 2006b), Ac1 from Arthrobotrys conoides
Drechsler (Yang et al. 2007b), and Dv1 from
Dactylellina varietas Yan Li, K.D. Hyde &
K.Q. Zhang (Yang et al. 2007c). There have
been some research on chitinase and other
hydrolytic enzymes produced by nematode-
trapping fungi. Lipases,
pectinases have been detected in vitro in egg
parasites fungi (Lopez-Llorca & Duncan 1988,
Dackman et al. 1989). Collagenase was
isolated from Arthrobotrys amerospora S.
Schenck, W.B. Kendr. & Pramer (Tosi et al.
2002) and an extracellular chitinase CHI43
from Pochonia chlamydosporia (Goddard)
Zare & W. Gams and P. suchlasporium (W.
Gams & Dackman) Zare & W. Gams (Lysek &
Krajci 1987). Acid phosphatase has been
reported at the site of contact between
nematodes and A. oligospora using ultrastruc-
tural techniques (Veenhuis et al. 1985). Acid
and alkaline phosphatase activities have also
been found in the ECM of Drechmeria
coniospora (Drechsler) W. Gams & H.B.
Jansson conidia (Jansson & Friman 2000).
Maher (1993) suggested that phosphatase could
be involved in adhesion.
Biological control of nematodes
Nematode-trapping fungi have long been
considered promising biological agents for
control of plant-parasitic nematodes (Dupon
nois et al. 2001, Sorbo et al. 2003, Singh et al.
2007, Thakur & Devi 2007) and animal para-
sitic nematodes (Bogus et al. 2005, Mendoza-
De Gives et al. 2006, Paraud et al. 2007,
Carvalho et al. 2009, Santurio et al. 2011).
Current Research in Environmental & Applied Mycology
Use of NTF to control animal gut nematodes
Alternatives to using anthelmintic drugs
for the treatment of nematode infections of
various animals have been necessary because
development of drug resistance nematodes
(Carvalho et al. 2009, Santurio et al. 2011).
The nematode-trapping fungus Duddingtonia
flagrans (Dudd.) R.C. Cooke has become an
important organism in various integrated con-
trol strategies (Carvalho et al. 2009, Maciel et
al. 2010, Santurio et al. 2011). Several studies
have demonstrated that when chlamydospores
of this nematode-trapping fungus are admi-
nistered to sheep and other animals (e.g. dogs,
cattle) there is a dramatic reduction of eggs of
this nematode passed out in the faeces (Dias et
al. 2007, Carvalho et al. 2009, Maciel et al.
2010, Santurio et al. 2011). It is unlikely that
D. flagrans can be the cure-all for nematode
parasite control of livestock or other animals,
but it has potential for use in integrated control
strategies (Maciel et al. 2010, Santurio et al.
Horses are also hosts to a wide variety of
nematodes (Tavela et al. 2011). The viability of
the nematode-trapping fungus Monacrospo-
rium thaumasium (Drechsler) de Hoog &
Oorschot 1985 administered in a formulation
(pellets) against Cyathostomin nematodes was
assessed in biological control of horses (Tavela
et al. 2011). There was a significant reduction
in egg counts in faeces following treatment,
however, this did not significantly affect
weight gains in the horses. It was therefore
speculated that treatment of horses with pellets
containing M. thaumasium may be effective in
controlling cyathostomin (Braga et al. 2009,
Tavela et al. 2011).
Use of NTF in traditional or natural bio-
control of plant nematodes
There has been great promise and much
research in the use of nematode-trapping fungi
for the biocontrol of nematodes (Khan et al.
2006, Soares et al, 2006). In one example
Aboul-Eid et al. (2006) tested the commercial
bio-product Dbx 1003 20% containing the
nematode-trapping fungus Dactylaria brocho-
paga Drechsler against root-knot nematode
Meloidogyne incognita infesting grapevine.
There was a significant reduction of M. incog-
nita in soil and in the number of root galls
when comparing treated to untreated soils. The
topic has been reviewed extensively (Martin &
Zhang 2002, Khan et al. 2006, Mennan et al.
2006, Soares et al. 2006, Zhu et al. 2006) and is
not discussed further here.
Studies to create favorable conditions for
the NTF that naturally occur in the soil, to
control nematode populations, have also been
carried out (Duponnois et al. 2001, Jaffee
2004a, Sun & Liu 2006, Radwan et al. 2007).
However, Cooke (1968) has revealed that the
chance of establishing an ‘alien’ species of
nematophagous fungi in the soil is small. Based
on this Gray (1984) suggested that fungi are
generally poor saprobic competitors in soil
habitats, and are susceptible to antagonism
from other soil organisms. Moreover, one of
the major constraints to biological control is
the inconsistency in efficacy which is often
observed when useful antagonists reach the
stage of large-scale glasshouse or field testing
(Kerry & Hominick 2002). This can arise from
a variety of causes reflecting the biological
nature of the control microorganism (Hay et al.
1997, Bird et al. 1998). Therefore the use of
NTF as biological control agents has not been
hugely successful to date.
Using advance techniques
Nematophagous fungi are soil-living
fungi that are used as biological control agents
of plants and animal parasitic nematodes
(Jansson et al. 1997). Direct applications to the
soil using these agents may have little to no
effect on the target nematodes. Their potential
could be improved by genetic engineering, but
the lack of information about the molecular
background of the infection has precluded this
development. Åhman et al. (2002) suggested
that a way to improve the biocontrol potential
of nematophagous fungi could be to increase
the expression of the pathogenicity-related
proteases. With the development of molecular
techniques, increasing attention has been paid
to understanding the molecular aspect of the
infection process and identifying the potential
virulence factors. Relatively high numbers of
pathogenic serine proteases have been identi-
fied from nematophagous fungi and have been
characterized and cloned. Moreover, to achieve
successful control of parasitic nematodes using
nematode-trapping fungi, a detailed knowledge
on the infection process is needed, for example,
virulence factors have been identified and
factors controlling their activity have been
characterized (Åhman et al. 1996, Rosen et al.
1997). A transformation system also has to be
developed to examine the function of virulence
factors in detail, e.g., by constructing over ex-
pressing strains and knock-out mutants (Tunlid
et al. 1999). ΔPII mutant was constructed in
recombination (Åhman et al. 2002). However,
the pathogenicity of the mutant was reduced
only a little and it was suggested that there
might be a significant residual proteolysis
activity in the ΔPII mutant (Yang et al. 2007c).
Åhman et al. (2002) suggested that genetic
engineering can be used to improve the patho-
genicity of a nematode-trapping species. In
their study, the mutants containing additional
copies of the PII gene developed a higher num-
ber of infection structures and had an increased
speed of capturing and killing nematodes
compared to the wild type.
Recently some advance techniques were
developed such as the green fluorescent protein
(GFP) and suppression subtractive hybridiza-
tion (SSH), to study the interaction between the
NTF and the nematodes. Ahrén et al. (2005)
compared the gene expression patterns in traps
and in the mycelium of the nematode-trapping
fungus Monacrosporium haptotylum (Drechs
ler) Xing Z. Liu & K.Q. Zhang by microarray
analysis. The ability of a nematode-trapping
fungus to become established in field soil is an
important characteristic when considering its
use as a biological control agent. Persson et al.
(2000) determined the nematode-trapping fun-
gus, Arthrobotrys superba in the soil using a
radioactive tracing method. PCR is becoming
an important tool in fungi not only for its
original use (nucleic acid amplification), but
also for gene cloning, the specific study of
genes involved in pathogenesis (Goller et al.
Commercialization of products
The goal of biocontrol research using
nematophagous fungi is to provide additional
tools for nematode management and to deliver
these tools to growers, therefore products must
be commercialized. There have been relatively
few successes in developing commercially
acceptable formulations of nematophagous
fungi. In most cases, fungi have been mass
produced on solid substrates such as cereal
grain or bran and the colonized substrate has
been applied to the soil. Formulations based on
alginate (Kerry et al. 1993, Jaffee & Muldoon
1995) and other materials, have been produced
on a limited scale, but the submerged fermen-
tation and downstream processing technologies
currently used for production of biological
herbicides, have never been used. In two com-
panion paper, Stirling et al. (1998a, b) reported
attempts to mass produce both egg-parasitic
and nematode-trapping fungi in submerged
culture and convert the fungal biomass into a
granular product suitable for commercial use.
Biologically active kaolin based formulations
produced that parasitized eggs of the root-knot
nematode Meloidogyne javanica in glasshouse
tests (Stirling et al. 1998a). Similar formula-
tions of Arthrobotrys dactyloides Drechsler
reduced the number of juveniles in soil micro-
cosms and numbers of galls on roots of plants
grown in the glasshouse (Stirling et al. 1998b).
A number of the formulated products have
been tested in the field and green house (Jaffee
& Muldoon, 1995, Waller et al. 2001; Araujo
et al. 2004b) and the predatory activity of
nematode-trapping fungi has been screened for
use as biological control agents (Araujo et al.
1996, Araujo et al. 2004a). However, the deve-
lopment of fungal biological control agents for
commercial use may be limited by several
factors. e.g chemical, physical, and abiotic
factors in the soil would influence the growth
of fungi (Mo et al. 2005).
It is clear that the commercialization of
these microorganisms lags far behind the
resource investigation. One limiting factor is
their inconsistent performance in the field, due
to virulence loss and insufficient quality con-
trol in pre-application steps. With the help of
advance techniques (e.g. genomics, crystallo-
graphy, and the suppression subtractive hybri-
dization methods), we may obtain clear under-
standing on the encoding genes of traps, the
signaling pathways that control the switch from
saprotrophy to parasitism, and the molecular
mechanism of the infection process (Yang et al.
2007c). Such information will provide a novel
approach to improve the efficacy of nematode-
Current Research in Environmental & Applied Mycology
trapping fungi for biological control of
Aung Swe would like to thank the
University of Hong Kong for the award of a
postgraduate scholarship to study nematode-
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