Current Research in Environmental & Applied Mycology

Nematode-Trapping Fungi

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 – -Trapping Fungi. Current Research in Environmental & Applied Mycology 1(1), 1–26.

This manuscript provides an account of nematode-trapping fungi including their , phylogeny and evolution. There are four broad groups of nematophagous fungi categorized based on their mechanisms of attacking . 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 – Phylogeny

Article Received 4 June 2011 Accepted 6 June 2011 Published online 25 June 2011 *Corresponding author: Kevin D. Hyde – e-mail – [email protected]

Table of contents

Introduction 2 Taxonomy, phylogeny and evolution of nematode-trapping fungi 2 Background of generic classification 2 Phylogenetic significance and evolution of trapping devices 4 Ancient nematode-trapping fungi 4 Biodiversity of nematode-trapping fungi 4 Ecology, occurrence and geographical distribution 6 Factors affecting the distribution of NTF 6 Effect of salinity 7 Ecological speciation 7 Fungal-nematode interactions 8 Host recognition, adhesion, host specificity and infection process 8

1 Extracellular enzymes involved in nematode infestation process 10 Biological control of nematodes 10 Use of NTF to control gut nematodes 11 Use of NTF in traditional or natural biocontrol of plant nematodes 11 Using advance techniques 11 Commercialization of products 12

Introduction amongst mycologists. Many generic names There are four broad groups of nemato- have been given to nematode-trapping fungi phagous fungi categorized based on their but the basis on which were circumscri- mechanisms of attacking nematodes (Liu et al. bed to different genera was unclear and sub- 2009). These include (1) nematode-trapping jective. Since 1930, nematode-trapping fungal fungi using adhesive or mechanical hyphal have been described and classified mostly in traps, (2) endoparasitic fungi using their spores, Corda, Dactylaria Sacc, and Dac- (3) egg parasitic fungi invading nematode eggs tylella Grove. or females with their hyphal tips, and (4) toxin- Corda (1839) established the Ar- producing fungi immobilizing nematodes throbotrys with A. superba Corda as the type before invasion (Kendrick et al. 2001, Liu et al. species. Characteristics of this genus are hya- 2009). line conidiophores which produce conidia The first nematode-trapping to be asynchronously on short denticles at swollen described was Arthrobotrys oligospora Fresen. conidiogenous heads or clusters of pronounced in 1852, but at that time its predatory habit was denticles (De Hoog 1985). Conidia are subhya- unknown. The predatory habit was first obser- line, obovoidal or clavate and (0–)1(–6)-sep- ved 36 years later by Zopf (1888). Since nema- tate. Trapping devices are constricting rings, tode-trapping fungi have considerable potential adhesive nets, hyphae or adhesive knobs (De for biological control of nematodes, there have Hoog 1985). Due to these broad morphological been extensive studies and reviews on their criteria the delimitation from Arthrobotrys is taxonomy, phylogeny, biology, and ecology sometimes problematic, particularly in Dactyl- (Cooke 1963, Kerry 1987, Sayre & Walter ella species which form more than one or two 1991, Sikora 1992, Kerry & Hominick 2002, conidia on each conidiophore (Cooke & Morton et al. 2004, Dong & Zhang 2006, Dickinson 1965). Based on this reason, Van Sikora et al. 2007). In this review, aspects such Oorschot (1985) restricted Dactylella to as taxonomy, phylogeny, diversity, and eco- species with fusiform, multi-septate conidia, logy of nematode-trapping fungi and their while Arthrobotrys species generally have potential in use in biocontrol of nematodes are ovoidal to clavate, 0–3-septate conidia. Van reviewed. Oorschot (1985) recognized 28 species of Ar- throbotrys. Schenck et al. (1977) expanded the Taxonomy, phylogeny and evolution of genus to 47 species. After Schenck et al. (1977) nematode-trapping fungi transferring all predacious species formerly described in Dactylaria to Arthrobotrys, Dacty- Background of the generic classification laria was no longer tenable for nematode- Nematode-trapping fungi are a hetero- trapping species. Recent classification based geneous group of anamorphic ascomycetes mostly on DNA sequence data has resulted in where species are defined primarily based on the transfer of species characterized by adhe- conidial characteristics such as size, septation, sive networks to Arthrobotrys (Scholler et al. and type of conidiogenous cells (Oudemans, 1999). Currently, there are 120 records of 1885, Subramanian, 1963). This has resulted in Arthrobotrys species but this includes basio- considerable ambiguity and confusion in inter- nyms and synonyms (Index Fungorum, 2011). generic classification of these organisms. Since A more realistic estimate is 63 (Kirk et al. the discovery of predacious activity in Arthro- 2008). botrys oligospora (Zopf, 1888), nematode- Monacrosporium was introduced by trapping fungi have attracted much interest Oudemans (1885) with two species, Monacro-

2 Current Research in Environmental & Applied Mycology sporium elegans Oudem. and M. subtile genus in Index Fungorum (Index Fungorum, Oudem. This generic name has been used by 2011). The current names for most species in many authors for several species following the the genus are in Arthrobotrys (1) Dactylella (3) opinion of Oudemans (1885). Subramanian Gamsylella (4) and Monacrosporium (8) and (1964) later selected M. elegans as lectotype only seven species are listed under Dactylellina species for this genus, highlighting the inflated while the remaining are anamorphic Orbilia middle cell of the conidia as the distinguishing (Index Fungorum 2011) generic criterion, and transferred a large num- Drechslerella was described by ber of nematode-trapping fungi from Dacty- Subramanian (1964) based on the type species, lella species to Monacrosporium. Rubner Drechslerella acrochaeta (Drechsler) Subram. (1996) revised most predacious hyphomycetes Scholler et al. (1999) later revised and trans- in Dactylella and Monacrosporium to deli- fered all predacious species forming con- mitate between the two genera. Scholler et al. stricting rings to this genus. Fourteen names (1999), however, proposed a new genus are listed in this genus in Index Fungorum concept for predatory anamorphic (Index Fungorum 2011), while Kirk et al. and the genus Monacrosporium was discarded. (2008) estimated there are one species. Species Many nematode-trapping fungal species are Fungorum (2011) currently lists seven names homeless and Monacrosporium is used as their as anamorphic Orbilia, while the other species current name. Currently, 74 taxa are listed in are organized in Arthrobotrys (3), Dactylella Index Fungorum (Index Fungorum, 2011), (1), Geniculifera (1) and Monacrosporium (3). while Kirk et al. (2008) estimate there to be 68 Gamsylella was described by Scholler et species. al. (1999) based on G. arcuata (Scheuer & J. Based on results obtained from morpho- Webster) M. Scholler, Hagedorn & A. Rubner logical and molecular characters, Hagedorn & Scholler et al. (1999) proposed Gamsylella as a Scholler (1999) and Scholler et al (1999) new genus combining all predacious species proposed that nematode-trapping fungi should that formed adhesive columns and unstalked be organized in four genera: Dactylellina M. knob devices to this genus. Li et al. (2005) later Morelet characterized by stalked adhesive transferred those species to Arthrobotrys and knobs including species characterized by non- Yang & Liu (2006) combined this genus with constricting rings and stalked adhesive knobs; Dactylellina based on molecular phylogenetic Gamsylella M. Scholler, Hagedorn & A. analyses. Six taxa belonging to Gamsylella Rubner characterized by adhesive branches and were reported by Index Fungorum (2008) and unstalked knobs; Arthrobotrys characterized by Kirk et al. (2008). Nevertheless, a placement of adhesive networks; and Drechslerella Subram. this genus based on phylogenetic analyses still characterized by constricting rings. Li et al. remains in questioning and therefore it should (2005) emended genus Gamsylella and trans- be revaluated. ferred species from Gamsylella to Arthrobotrys Dactylella was proposed by Grove and Dactylellina. Gamsylella was not treated (1884) based on the type species Dactylella by them as a valid genus as proposed by minuta Grove a nematode-trapping species. Scholler et al. (1999). Yang & Liu (2006) later The genus is characterized by erect, simple, proposed to combine Dactylellina and Gam- hyaline conidiophores with conidia produced sylella into one genus based on molecular singly at the apex. Conidia are ellipsoidal, phylogenetic analyses. However, there are still fusoid or cylindrical, one-celled at first and debates concerning the generic concepts of later having 2 to many septa. This genus has Gamsylella. been emended several times and both non- The genus Dactylellina was described by predacious and predacious fungi have been Morelet (1968) with Dactylellina leptospora included (Subramanian, 1963), Schenck et al. (Drechsler) M. Morelet as type species. 1977; de Hoog & Oorschot, 1985; Zhang et al. Scholler et al. (1999) later transferred all preda- 1994). Rubner (1996) revised the generic cious species forming adhesive stalked knobs concept of Dactylella and excluded the and non-constricting trapping rings to this nematode-trapping species. However, several genus. Thirty-two names are listed for this nematode predacious species still remain in

3 Dactylella (Liu & Zhang 2003, Zhang et al. and Yang et al. (2007a). Phylogenetic analysis 2005). This genus was revisited by Liu & of nucleotide sequences demonstrated that Zhang (2003) and was separated into three early trapping structures evolved along two groups such as Dactylella, Vermispora and lines, yielding two distinct trapping mecha- Brachyphoris. One hundred and eight Dac- nisms. One lineage developed into constricting tylella species are listed in Index Fungorum rings and the other into adhesive traps. The (Index Fungorum, 2011) where there are 62 adhesive network separated early. The adhesive estimated species (Kirk et al. 2008). knob evolved through stalk elongation, with a final development of nonconstricting rings. Li Phylogenetic significance and evolution of et al (2005) on the otherhand showed a trapping devices conflicting result. Morphology-based classification of fungi Orbiliales ITS and 28s rDNA-specific has been demonstrated to be inadequate in PCR primers which directly detect nematode- reflecting natural relationships among fungi. trapping fungi without culturing were deve- Phylogenetic analyses using molecular data, loped by Smith & Jaffee (2009). The authors thus, have been used for more than a decade to believe the combined use of Orbiliales-specific assess phylogenetic relationships and also to primers and culture-based techniques may revaluate the phylogenetic importance of benefit future studies of nematophagous fungi various morphological characters (Cai et al. and can also be used to screen fungal isolates 2009). The first notable phylogeny study on for phylogenetic placement in the Orbiliales. nematode-trapping fungi was that of Rubner (1996). He used trapping devices to rationalize Ancient nematode-trapping fungi the classification of nematode-trapping fungi An early record of a nematode-trapping using molecular data. Later phylogenetic fungus is that of Palaeoanellus dimorphus studies based rDNA sequence analysis also which lived approximately 100 million years found that trapping devices are more infor- ago in a limnetic-terrestrial microhabitat mative than other morphological characters in (Schmidt et al. 2008). The fossil probably delimiting genera (Liou & Tzean, 1997, Pfister represents an anamorph of an ascomycete with 1997, Ahrén et al. 1998, Scholler et al. 1999, unicellular hyphal rings as trapping devices and Ahrén & Tunlid 2003, Kano et al. 2004, Li et formed blastospores from which a yeast stage al. 2005, Yang & Liu 2006, Yang et al. 2007a, developed. The authors speculated that because Liu et al. 2009). For example, Ahrén et al. predatory fungi with regular yeast stages are (1998) revealed nematode-trapping fungi not known from modern ecosystems, the grouping in three lineages based on different fungus is assumed to not be related to any types of trapping devices. Scholler et al. (2009) recent nematode-trapping fungi and is probably classified nematode-trapping fungi into four an extinct lineage. Alternatively, it may be that genera using 18S and ITS rDNA analysis. Li et we may yet find this strange species in modern al. (2005) re-evaluated the placement of nema- settings. tode-trapping genera based 28S, 5.8S and β- tubulin analysis and the establishment of Biodiversity of nematode-trapping fungi Gamsylella proposed by Scholler et al. (1999) Hawksworth (1991) estimated that there was criticized and not accepted. Yang & Liu are 1.5 million global species of fungi and this (2006) proposed to combine Dactylellina and has been accepted as a working figure by many Gamsylella into one genus and Yang et al. mycologists. There have been several other (2007b) traced the evolution of trapping publications debating estimates of fungal spe- devices in predatory fungi based on analyses of cies (Hammond 1992, Cannon 1997, Huhndorf ITS, rpb2, ef-1, β-tubulin sequences. However, & Lodge 1997, Hyde et al. 2007). Neverthe- the morphological affinity of Gamsylella to less, however many fungi exist in nature, there genera Arthrobotrys and Dactylellina are still are few (ca 100,000) that have been described. unclear and intergeneric relationships of Gam- Hyde (2001) pointed out that most of the sylella and its allies are still unresolved. undescribed fungi are microfungi and they may The evolution of nematode-trapping occur in poorly investigated areas and less devices has been discussed by Li et al. (2005) explored niches, substrates, hosts abd habitats. 4 Current Research in Environmental & Applied Mycology

There has been a relatively large numbers these molecular methods overcomes the limita- of studies on fungal diversity such as in tions associated with traditional approaches extreme environments (Connell et al. 2006, and isolation based methods. Jeewon & Hyde 2008, Fell et al. 2006, Porras-Alfaro et al. (2007) recently reviewed advance molecular 2008), in marine habitats (Hyde 1996, Poon & techniques versus traditional techniques that Hyde 1998, Barata 2006, Hyde & Sarma 2006, are used in the detection and diversity of fungi Lai et al. 2007, Laurin et al. 2008, Nambiar et from environmental samples. Molecular me- al. 2008), in freshwater habitats (Tsui et al. thods used in assessing fungal diversity have 2000, Cai et al. 2003, Fryar et al. 2004, Tsui & been employed such as Denaturing Gradient Hyde 2004, Duarte et al. 2006, Sole et al. Gel Electrophoresis (DGGE), Terminal Re- 2008), in terrestrial habitats (Hyde & Alias striction Fragment Length Polymorphism (T- 2000, Sun & Liu 2008, Wakelin et al. 2008a), RFLP), Amplified rDNA Restriction Analyses in areas of environmental pollution (Indra & (ARDRA), Amplified Random Intergeneric Meiyalagan 2005, Zafar & Ahmad 2005, Ellis Spacer Analysis (ARISA), and Temperature et al., 2007, Duarte et al. 2008, Stefanowicz et Gradient Gel Electrophoresis (TGGE). Recen- al. 2008, Turnau et al. 2008), on decaying litter tly PCR-based fingerprinting techniques have (Tsui et al. 2000, Cai et al. 2003, Tsui & Hyde been applied to assess fungal diversity. Oligo- 2004, Gulis et al. 2008, Lonsdale et al. 2008). nucleotide Fingerprinting of Ribosomal RNA However, there are relatively few diversity Gene (ORFG), a new method that sorts arrayed studies of nematode-trapping fungi (Hao et al. rRNAgene clones into taxonomic clusters 2005, Mo et al. 2006, 2008, Saxena 2008). Hao through a series of hybridization experiments et al. (2005) studied the diversity of nematode- (Kirk et al. 2004). Most frequently used trapping from aquatic habitats; Mo et al. (2006, methods in assessing fungal diversity are Dena- 2008) studied diversity of nematode-trapping turing Gradient Gel Electrophoresis (DGGE) fungi from heavy metal polluted soils. Interes- and Terminal Restriction Fragment Length tingly, Mo et al. (2008) revealed that the Polymorphism (T-RFLP). Wakelin et al. diversity index of nematode-trapping fungi was (2008b) used a semi-quantitative nested quan- positively correlated with concentration of titative PCR approach and a DGGE approach heavy metals. to detect soil total Fusarium communities on Diversity study on nematode-trapping maize root. Li et al. (2008) used a combination fungi using traditional methods has involved in of plate count, DGGE and clone library several processes, such as sample collection, analyses to investigate the effect of metha- isolating with nematodes, preliminary morpho- midophos on soil fungi community in micro- logical examination of fungal structures, single cosms. Raberg et al. (2005) used T-RELP to spore isolations for examining trapping devices detect the early stages of wood decay and this and identifying species. These methods have was compared with microscopic evaluation. been commonly used because of their low cost Yet, there is no study on diversity of nematode- and the fact that they are easy to conduct trapping fungi using molecular methods. (Jeewon & Hyde, 2007). The traditional Although traditional methods and mole- methods used in nematode-trapping fungi cular based methods both have disadvantages largely rely on the discovery of fungal spores and advantages, traditional methods presently in natural environments. Hyde & Goh (1998) still have some advantages over molecular pointed out that the incubation of substrates based techniques in assessing fungal diversity. effects the structure of fungal communities Most of the molecular techniques involved do recorded. Jeewon & Hyde (2007) suggested not discriminate between active and inactive that a large number of fungi existing as stages of fungi (Jeewon & Hyde, 2007). Data mycelial propagules or dormant spores and can yielded from molecular techniques are difficult be numerically dominant populations but in to employ with respect to ecology and function their natural environment they may have little (e.g. correlation analysis between environ- functionality. mental factors and fungal communities). More- Molecular techniques have been used to over, traditional methods often involve less investigate fungal diversity. The emergence of cost and no expensive specialized laboratory

5 equipment is needed, which are often not first species of nematode-trapping fungi to be available in developing world. In contrast, cur- reported from brackish water (Johnson & rent knowledge on the diversity and detection Autery 1961) while Swe et al. (2008a, b, 2009) and the community structure of the nematode- recorded several species from mangroves. trapping fungi in nature is still rudimentary. Improvement in traditional approaches com- Factors affecting the distribution of bined with molecular techniques will provide a nematode-trapping fungi better understanding of these fungal commu- The distribution and occurrence of nema- nity systems in nature. tode-trapping species and groups of fungi is associated with specific soil variables in parti- Ecology, occurrence and geographical cular pH, moisture, nutrients (N, P, K), heavy distribution metal and nematode density (Gray 1985, There have been numerous surveys on Persson & Baath 1992, Jaffee 2004b, Sánchez- the occurrence of nematophagous fungi, which Moreno et al. 2008, Mo et al. 2008). Gray have shown that the fungi are found throughout (1988) revealed that soil nutrients such as N, P the world and in all types of climate and and K were all positively correlated with nema- habitats (Duddington 1951, 1954, Gray 1987, tode density. Species with stalked knobbed Sunder & Lysek 1988, Boag & Lopez-Llorca trapping devices (Dactylellina) and those 1989, Saxena & Mukerji 1991, Dackman et al. species with constricting rings (Drechslerella) 1992, Liu et al. 1992, Saxena & Lysek 1993, were isolated more readily from richer soils Rubner 1994, Persmark & Nordbring-Hertz which contained a greater density of nema- 1997, Persmark & Jansson 1997, Jaffee 2003, todes. However, net-forming species (Arthro- Ahrén et al. 2004, Hao et al. 2005, Jaffee & botrys) are largely independent of soil fertility, Strong 2005, Farrell et al. 2006, Su et al. 2007, especially low K (Burges & Raw 1967). Mo et al. 2008, Saxena 2008). The teleomorph Interestingly, Mo et al. (2008) found that state Orbilia of nematode-trapping fungi have diversity of nematode-trapping was positively been recorded on decaying wood from terres- correlated with lead concentration. These soil trial and freshwater habitats (Pfister 1994, variables are known to vary with depth, as are Webster et al. 1998, Liu et al. 2005, 2006, the densities of soil bacteria, fungi and nema- Zhang et al. 2006, 2007, Yu et al. 2007), and todes (Mankau & McKenny, 1976, McSorley the anamorphic states also commonly occur in et al. 2006) and a high level of nematode- terrestrial, freshwater and marine habitats (Hao trapping activity have been recorded from the et al. 2004, Li et al. 2006, Swe et al. 2008a, b, rhizosphere area (Peterson & Katznelson 1964, 2009), but rarely occur in extreme environ- Mitsui et al. 1976, Persmark & Jansson 1997, ments (Onofri & Tosi 1992). There have been Wang et al. 2003, McSorley et al. 2006). several studies on nematode-trapping fungi However, there are large variations depending because of their potential in biological control, on plant and soil types (Jansson & Lopez- however most of these have concentrated on Llorca 2001). The species of nematode- agriculture and animal husbandry or forestry trapping fungi vary with depth (Gray & Bailey (Kerry & Hominick 2002, Ahrén & Tunlid 1985). Peterson & Katznelson (1964) revealed 2003, Jaffee & Strong 2005, Dong & Zhang that the greatest diversity occurred in the upper 2006, Su et al. 2007) or freshwater 10–30 cm of soils, and this was a positive environments (Maslen 1982, Hao et al. 2005). correlation between the population density of Numerous fungal-animal associa-tions have nematophagous fungi and root-knot nematodes been reported from aquatic habitats. The first in peanut fields. Gray & Bailey (1985) have report of marine predacious fungi was three examined the vertical distribution of nemato- zoophagous forms discovered in brackish water phagous fungi in soil cores collected from a (Jones 1958). Currently, more than 50 species deciduous woodland, predators forming con- of predacious hyphomycetes have been stricting rings, adhesive branches and adhesive recorded from aquatic habitats (Ingold 1944, knobs are restricted to the upper litter and Peach 1950, 1952, Johnson & Autery 1961, humus layer, while the net-forming predators Anastasiou 1964, Hao et al. 2004, 2005). and endoparasites were isolated at all depths, Arthrobotrys dactyloides Drechsler was the although they are significantly more abundant 6 Current Research in Environmental & Applied Mycology in the lower mineral-rich soils. In contrast, generally they are isolated from soils with predators able to form traps spontaneously are limited nutrients, especially low K (Burges & restricted to the organic soils of the hemi- Raw 1967). edaphic zone which are rich in nematodes. Nematophagous fungi are small enough to be Effect of salinity affected by micro-climates within the soil The effect of salinity on fungal growth in (Gray 1985). Hao et al. (2005) observed that yeasts and moulds (Blomberg & Adler 1993, the nematode-trapping were not detected Dan et al. 2002), marine fungi, mycorrhizal deeper than four meter in a freshwater pond. fungi and some wood-rotting basidiomycetes Several studies have also been carried out on has been studied (Ritchie 1959, Davidson horizontal distribution (Persson et al. 2000, 1974, Byrne & Jones 1975, Jones & Byrne Segers et al. 2000, Minglian et al. 2004). For 1976, Kohlmeyer & Kohlmeyer 1979, Siegel & example, Persson et al. (2000) studied the Siegel 1980, Hyde et al. 1987, Lorenz & growth and dispersion of Arthrobotrys superba Molitoris 1992, Clipson & Hooley 1995, Akira Corda under natural conditions determined by a & Tadayoshi 1996, Castillo & Demoulin 1997, radioactive tracing technique. Juniper & Abbott 2006, Sharifi et al. 2007). The effect of major biotic and abiotic Some research has studied the effects of variables such as soil moisture, organic matter, salinity on the growth and the parasitic ability pH, nematode density, soil nutrients (Gray of the parasitic fungi, with most having studied 1987) and submerged water condition on the the parasites of mosquitoes (Harrison & Jones distribution of nematode-trapping fungi has 1971, Lord & Roberts 1985, Gardner & Pillai been extensively studied. The diversity was 1986, Lord et al. 1988, Kramer 1990, Teng et highest at the depth of 20 cm and no nematode- al. 2005). The effect of abiotic factors, such as trapping fungi were found at the depth of 4 m temperature, pH, light, UV and nutrition on the (Hao et al. 2005). Heavy metals concentrations trapping efficacy of nematode-trapping fungi affected distribution of NTF and was not nega- has been intensively studied (Ciordia & Bizzell tively affected by Pb concentration (Mo et al. 1963, Gray 1985, 1988, Morgan et al. 1997, 2006, Mo et al. 2008). However, treatment Fernandez et al. 1999, Gronvold et al. 1999, with ethylenediamine tetra-acetic acid (EDTA) Zucconi et al. 2002, Jaffee 2006, Kumar & resulted in detecting various stages of fungi of Singh 2006a, 2006b, Paraud et al. 2006, Sun & aggregates in the sediments from -5000 m deep Liu 2006, Gao et al. 2007). sea, gradually revealing the presence of fungal hyphae within them (Damare & Raghukumar Ecological speciation 2008). Gray (1987) pointed out that the endo- Speciation, the evolution of one species parasitic nematophagous fungi are obligate into two, is one of the most fundamental parasites, and unlike the predatory fungi, they problems to appreciate in biology (Giraud et al. appear to be unable to live as saprotrophs in the 2008). Numerous reviews on the modes of spe- soil. He also suggested that non-specific me- ciation in fungi have been published (Natvig & thod of attraction may rely on a greater density May 1996, Burnett 2003, Kohn 2005, Giraud et of soil nematodes to ensure infection, as com- al. 2008). ‘Ecological speciation’, as defined pared with parasites which produce adhesive by Rundle & Nosil (2005) is ‘the process by conidia (Gray 1987). which barriers to gene flow evolve between Gray (1988) revealed that soil nutrients populations as a result of ecologically based N, P and K were all positively correlated with divergent selection’. Fungi are excellent nematode density. Based on his results, knob- models for the study of eukaryotic speciation in forming predators which rely on their ability to general (Burnett 2003, Kohn 2005). However, produce traps spontaneously are isolated from they are still rarely included in general reviews soils with low concentration of nutrients, while on this subject. Giraud et al. (2008) explained those species with constricting rings are iso- why fungi is a excellent models for studying lated from richer soils which contain a greater speciation; (1) Many fungi can be cultured in density of nematodes. Net-forming species are vitro and many experiments on mating types largely independent of soil fertility, although among fungal species have been reported, (2)

7 Fungi display a huge variety of life cycle and new environments constrains the organism’s geographical and ecological distributions, ability to successfully disperse in nature. The allowing the study of parameters most signi- population structure in asexual parasites may ficantly influencing the speciation processes, reflect host or habitat adaptation at all loci, (3) Numerous species complexes are known in because selection at one locus results in hitch- fungi, encompassing multiple recently diverged hiking of the whole gene (Giraud et al. 2008) sibling species which allows investigations on ‘The ecological species concept (ESC)’ the early stages of speciation. and ‘ecological speciation’ have been proposed It is important to define a species before as an important component of speciation studying speciation. The traditional species among widely spread and diverse living orga- concept is the morphological species concept nisms such as fish (Hatfield &Schluter 1999), (MSC) and in fungi is mainly based on mor- lizards (Ogden & Thorpe 2002, Richmond & phology and reproductive behavior (Taylor et Reeder 2002), and (Via 1999, Via et al. al. 2000). On the other hand, some mycologists 2000, Rundle & Nosil 2005, Barat et al. 2008). have debated that species concepts should also There have been some studies on host specia- be considered on an ecological basis as well as tion in fungi (Antonovics et al. 2002, Couch et on nucleotide divergence (ESC, ecological al. 2005, Lopez-Villavicencio et al. 2005). species concept and phylogenetic species However, ecological speciation in fungi has not concept, PSC) (Harrington & Rizzo 1999). received much attention. One of the first Nevertheless, the most commonly used species studies on ecological speciation was on the criterion for the fungi has been the morpho- pathogenic fungi, Metarhzium anisoplaie logical species concept. However, many cryp- by Bidochka et al. (2001) and in their study M. tic species have been discovered within anisoplaie clearly separated into two genetic morphological species, using the biological groups based on two habitats; agriculture and species concept (e.g. Anderson & Ullrich 1979) forest. Another study was on a plant pathogen or the genealogical goncordance phylogenetic of grasses, Claviceps purpurea and the result species recognition, GCPSR (Taylor et al. shown that terrestrial isolates were signifi- 2000). Moreover, the phylogenetic species cantly divergent from other isolates of wet concept uses the phylogenetic concordance of /shady and salt marsh habitats (Douhan et al. multiple unlinked genes to indicate a lack of 2008). There have however, been few related genetic exchange and thus evolutionary inde- studies on nematode-trapping fungi. Geogra- pendence of lineages. Thus, species can be phical speciation among 22 isolate of Dudding- identified which cannot be recognized using tonia flagrans (Dudd.) R.C. Cooke suggested other species criteria due to the lack of that there was no or little genetic variation morphological characters (Giraud et al. 2008). (Ahrén et al. 2004). However, using selective Recently, the genealogical concordance phylo- fragment length amplification, Mukhopad genetic species recognition criterion is also hyaya et al. (2004) found that D. flagrans useful tool or criterion in fungi and is most isolates are genetically diverse despite their widely used within the fungal kingdom morphological similarities. (Johnson et al. 2005, Pringle et al. 2005, Le Gac et al. 2007). Fungal-nematode interactions Knowing which genes are involved in reproductive isolation may help to get a better Host recognition, adhesion, host specificity understanding of speciation processes (Giraud and infection process et al. 2008). There has been little research to Nematophagous fungi are an important understand the genetics of speciation in fungi. group of soil microorganisms that can suppress Four of five genes were involved in the inter- the populations of plant and animal parasitic sterility among Heterobasidion species (Chase nematodes. They can be grouped into three & Ullrich 1990). DNA multi-locus typing categories according to their mode of infesta- showed that different clones of the fungus are tion: nematode-trapping, endoparasitic, and associated with different environments (Fisher toxic compound producing (Nordbring Hertz & et al. 2005), which indicated that adaptation to Tunlid 2000). The pathogenic mechanisms

8 Current Research in Environmental & Applied Mycology during the infestation process are diverse. They could be the basis of a chemoecological can be mechanical through the production of relationship between plant parasitic nematodes specialized capturing devices, or through and their vector insects (Zhao et al. 2007). production of toxins that kill nematodes. Jansson (1982) showed that the presence of During infection, a variety of virulence factors trapping devices on the hyphae increases the may be involved against nematodes by ability of fungi to attract nematodes. Trapping nematophagous fungi. The infection processes devices could be produced spontaneously, or and host range of nematophagous fungi have their formation can be induced by nematodes been studied using various techniques such as or proteinaceous compounds (Jansson & light and low temperature electron microscopy Nordbring-Hertz 1979). The connection be- and bioassays and have been supported by tween attraction ability and degree of para- biochemical, physiological, immunological and sitism was also confirmed when the parasitic molecular techniques (Thorn & Barron 1984, ability of the fungi was tested in soil micro- Murray & Wharton 1990, Jansson et al. 2000). cosms (Tunlid et al. 1992, Dijksterhuis et al. The ultrastructure of the nematode-trapping 1994). devices has been extensively studied (Heintz & More recently, Wang et al. (2009) invest- Pramer 1972, Nordbring-Hertz & Stalhammar- tigated the attraction of Esteya vermicola J.Y. Carlemalm 1978, Dijksterhuis et al. 1994). The Liou, J.Y. Shih & Tzean to the pinewood mode of infection by nematophagous fungi has nematode. The endoparasitic fungus was been reviewed by Yang et al. (2007c). attracted to living mycelia and exudative Research on attraction of nematodes to substances of E. vermicola reflecting the fungi has focused on the host-finding behavior dependence of the fungi on nematodes for of fungal-feeding nematodes (Bordallo et al. nutrients. Attractive substances appeared to be 2002, Wang et al. 2010). Nematophagous fungi avolatile exudatives and volatile diffusing are attracted to plant and animal parasitic compounds. nematodes and microbivorous nematodes Adhesion to host is an essential require- (Balan & Gerber 1972, Jansson & Nordbring- ment for fungal parasites to be able to infect. Hertz 1979, 1980). Zuckerman & Jansson Most of pathogenic and parasitic fungi, (1984) review nematode chemotaxis and adhesion is mediated by an extracellular matrix possible mechanisms of host/prey recognition. (ECM) or sheath on the fungus (O'Connell The attracttion of nematodes to nematophagous 1991, Åhman et al. 2002, Alston et al. 2005). fungi has been studied using culture filtrates Tunlid et al. (1992) suggested that extracellular and macerated mycelium (Jansson & adhesions are produced on the surfaces of Nordbring-Hertz 1979) as well as living fungi spores, appressoria and trapping devices and (Jansson & Nordbring-Hertz 1980). One of the are essential for infection. The adhesive layer earliest observations described the attraction of has a fibrillar structure with residues of neutral the plant parasitic nematode Meloidogyne sugars, uronic acid and proteins (Whipps & incognita to tomato roots grown in sterile Petri Lumsden 2001). Jansson & Lopez-Llorca plates (Zuckerman & Jansson 1984). Pena- (2001) suggested that the adhesion process is gellus redivivus was attracted to approximately much more complicated than a simple receptor- 75% of the mycelium of nematophagous fungi ligand binding, and may involve the activity of tested (Kuyama & Pramer 1962, Nordbring- the fungal infection structure as well as the Hertz 1973, Barron 1977, Jansson 1982). surface of living nematodes. Initial contact Fungal feeding and plant parasitic nematodes with the host cuticle may be followed by inter- seem to respond differently to fungal actions with specific receptors, reorganization chemotactic factors (Ward 1973, Field & of surface polymers to strengthen the Webster 1977, Zuckerman & Jansson 1984, adhesions, changes in morphology and the se- Zhao et al. 2007), e.g. fungal feeding cretion of specific enzymes (Jansson & nematodes were attracted to all fungi tested, Nordbring-Hertz 1988, Kerry 2000, Abiko et while some plant parasitic nematodes were al. 2005). These processes and the structures attracted to very few fungi (Field & Webster involved have been extensively reviewed 1977); the volatiles produced by the host plants (Kerry et al. 1993).

9 Extracellular enzymes involved in nematode involvement in the infection and immobili- infestation process zation of nematodes by the nematode-trapping During the infection process, the cuticle fungi, Arthrobotrys oligospora was by Tunlid must be penetrated, the nematode is immo- & Jansson (1991). Subsequently, a first bilized, and the prey is finally invaded and pathogenic serine protease (P32) from the digested. This sequence of infection seems to nematode egg parasite Verticillium suchla- be present in most nematophagous fungi, but sporium W. Gams & Dackman was purified the molecular mechanisms are not well and characterized by Lopez-Llorca & understood (Lopez-Llorca & Duncan 1988, Robertson (1992). Recently more pathogenic Dackman et al. 1989). However, several nema- serine proteases were detected, characterized, tophagous fungi have been reported to produce and cloned by several scientists, for examples nematotoxins that immobilize or kill nema- Aoz1 from Arthrobotrys oligospora (Zhao et todes, and ultrastructural and histochemical al. 2005), M1x from Monacrosporium studies suggest that the penetration of the microscaphoides Xing Z. Liu & B.S. Lu (Wang nematode cuticle involves the activity of et al. 2006a), and Ds1 from Dactylella hydrolytic enzymes (Schenck et al. 1980). shizishanna X.F. Liu & K.Q. Zhang (Wang et Enzymes involved in the infection processes of al. 2006b), Ac1 from Arthrobotrys conoides nematophagous fungi are being cloned and Drechsler (Yang et al. 2007b), and Dv1 from characterized. Also, many scientists have per- Dactylellina varietas Yan Li, K.D. Hyde & formed screens of nematophagous fungi in K.Q. Zhang (Yang et al. 2007c). There have order to identify the structures of compounds been some research on chitinase and other produced in vitro that may have nematicidal hydrolytic enzymes produced by nematode- action. There is a recent review on the modes trapping fungi. Lipases, amylases and of infection and the biochemical properties of pectinases have been detected in vitro in egg the serine proteases enzyme (Yang et al. parasites fungi (Lopez-Llorca & Duncan 1988, 2007c). Dackman et al. 1989). Collagenase was Studies of insect and other parasitic fungi isolated from Arthrobotrys amerospora S. have shown that the chemical composition of Schenck, W.B. Kendr. & Pramer (Tosi et al. the surface of the host is important for the 2002) and an extracellular chitinase CHI43 hydrolytic enzymes involved in infection from Pochonia chlamydosporia (Goddard) (Sahai & Manocha 1993). More detailed Zare & W. Gams and P. suchlasporium (W. studies on Metarhizium anisopliae (Metschn.) Gams & Dackman) Zare & W. Gams (Lysek & Sorokīn has shown that proteases are produced Krajci 1987). Acid phosphatase has been more rapidly and in higher concentrations than reported at the site of contact between other cuticle-degrading enzymes (Goettel et al. nematodes and A. oligospora using ultrastruc- 1989, Veenhuis et al. 1985). There is much tural techniques (Veenhuis et al. 1985). Acid evidence related to protease and chitinase and alkaline phosphatase activities have also production by entomophagous fungi (Jansson been found in the ECM of Drechmeria & Friman 2000, Tikhonov et al. 2002). Pro- coniospora (Drechsler) W. Gams & H.B. teases are the only enzymes produced in large Jansson conidia (Jansson & Friman 2000). amounts (Maher 1993). Furthermore, the pro- Maher (1993) suggested that phosphatase could tein coating of chitin microfibrils in extracellu- be involved in adhesion. lar barriers of insects and nematodes would render microibrils relatively non-amenable to Biological control of nematodes enzymolysis (Rong De et al. 2005). It can Nematode-trapping fungi have long been therefore be assumed that the activity of considered promising biological agents for proteases is more important than chitinase in control of plant-parasitic nematodes (Dupon host penetration. However, the importance and nois et al. 2001, Sorbo et al. 2003, Singh et al. function of extracellular proteases in the 2007, Thakur & Devi 2007) and animal para- infection process between nematodes and fungi sitic nematodes (Bogus et al. 2005, Mendoza- are still unknown. De Gives et al. 2006, Paraud et al. 2007, The first study on proteases and their Carvalho et al. 2009, Santurio et al. 2011).

10 Current Research in Environmental & Applied Mycology

Use of NTF to control animal gut nematodes when comparing treated to untreated soils. The Alternatives to using anthelmintic drugs topic has been reviewed extensively (Martin & for the treatment of nematode infections of Zhang 2002, Khan et al. 2006, Mennan et al. various have been necessary because 2006, Soares et al. 2006, Zhu et al. 2006) and is development of drug resistance nematodes not discussed further here. (Carvalho et al. 2009, Santurio et al. 2011). Studies to create favorable conditions for The nematode-trapping fungus Duddingtonia the NTF that naturally occur in the soil, to flagrans (Dudd.) R.C. Cooke has become an control nematode populations, have also been important organism in various integrated con- carried out (Duponnois et al. 2001, Jaffee trol strategies (Carvalho et al. 2009, Maciel et 2004a, Sun & Liu 2006, Radwan et al. 2007). al. 2010, Santurio et al. 2011). Several studies However, Cooke (1968) has revealed that the have demonstrated that when chlamydospores chance of establishing an ‘alien’ species of of this nematode-trapping fungus are admi- nematophagous fungi in the soil is small. Based nistered to sheep and other animals (e.g. dogs, on this Gray (1984) suggested that fungi are cattle) there is a dramatic reduction of eggs of generally poor saprobic competitors in soil this nematode passed out in the faeces (Dias et habitats, and are susceptible to antagonism al. 2007, Carvalho et al. 2009, Maciel et al. from other soil organisms. Moreover, one of 2010, Santurio et al. 2011). It is unlikely that the major constraints to biological control is D. flagrans can be the cure-all for nematode the inconsistency in efficacy which is often parasite control of livestock or other animals, observed when useful antagonists reach the but it has potential for use in integrated control stage of large-scale glasshouse or field testing strategies (Maciel et al. 2010, Santurio et al. (Kerry & Hominick 2002). This can arise from 2011). a variety of causes reflecting the biological Horses are also hosts to a wide variety of nature of the control microorganism (Hay et al. nematodes (Tavela et al. 2011). The viability of 1997, Bird et al. 1998). Therefore the use of the nematode-trapping fungus Monacrospo- NTF as biological control agents has not been rium thaumasium (Drechsler) de Hoog & hugely successful to date. Oorschot 1985 administered in a formulation (pellets) against Cyathostomin nematodes was Using advance techniques assessed in biological control of horses (Tavela Nematophagous fungi are soil-living et al. 2011). There was a significant reduction fungi that are used as biological control agents in egg counts in faeces following treatment, of plants and animal parasitic nematodes however, this did not significantly affect (Jansson et al. 1997). Direct applications to the weight gains in the horses. It was therefore soil using these agents may have little to no speculated that treatment of horses with pellets effect on the target nematodes. Their potential containing M. thaumasium may be effective in could be improved by genetic engineering, but controlling cyathostomin (Braga et al. 2009, the lack of information about the molecular Tavela et al. 2011). background of the infection has precluded this development. Åhman et al. (2002) suggested Use of NTF in traditional or natural bio- that a way to improve the biocontrol potential control of plant nematodes of nematophagous fungi could be to increase There has been great promise and much the expression of the pathogenicity-related research in the use of nematode-trapping fungi proteases. With the development of molecular for the biocontrol of nematodes (Khan et al. techniques, increasing attention has been paid 2006, Soares et al, 2006). In one example to understanding the molecular aspect of the Aboul-Eid et al. (2006) tested the commercial infection process and identifying the potential bio-product Dbx 1003 20% containing the virulence factors. Relatively high numbers of nematode-trapping fungus Dactylaria brocho- pathogenic serine proteases have been identi- paga Drechsler against root-knot nematode fied from nematophagous fungi and have been Meloidogyne incognita infesting grapevine. characterized and cloned. Moreover, to achieve There was a significant reduction of M. incog- successful control of parasitic nematodes using nita in soil and in the number of root galls nematode-trapping fungi, a detailed knowledge

11 on the infection process is needed, for example, acceptable formulations of nematophagous virulence factors have been identified and fungi. In most cases, fungi have been mass factors controlling their activity have been produced on solid substrates such as cereal characterized (Åhman et al. 1996, Rosen et al. grain or bran and the colonized substrate has 1997). A transformation system also has to be been applied to the soil. Formulations based on developed to examine the function of virulence alginate (Kerry et al. 1993, Jaffee & Muldoon factors in detail, e.g., by constructing over ex- 1995) and other materials, have been produced pressing strains and knock-out mutants (Tunlid on a limited scale, but the submerged fermen- et al. 1999). ΔPII mutant was constructed in tation and downstream processing technologies Arthrobotrys oligospora by homologous currently used for production of biological recombination (Åhman et al. 2002). However, herbicides, have never been used. In two com- the pathogenicity of the mutant was reduced panion paper, Stirling et al. (1998a, b) reported only a little and it was suggested that there attempts to mass produce both egg-parasitic might be a significant residual proteolysis and nematode-trapping fungi in submerged activity in the ΔPII mutant (Yang et al. 2007c). culture and convert the fungal biomass into a Åhman et al. (2002) suggested that genetic granular product suitable for commercial use. engineering can be used to improve the patho- Biologically active kaolin based formulations genicity of a nematode-trapping species. In of Verticillium chlamydosporium were their study, the mutants containing additional produced that parasitized eggs of the root-knot copies of the PII gene developed a higher num- nematode Meloidogyne javanica in glasshouse ber of infection structures and had an increased tests (Stirling et al. 1998a). Similar formula- speed of capturing and killing nematodes tions of Arthrobotrys dactyloides Drechsler compared to the wild type. reduced the number of juveniles in soil micro- Recently some advance techniques were cosms and numbers of galls on roots of plants developed such as the green fluorescent protein grown in the glasshouse (Stirling et al. 1998b). (GFP) and suppression subtractive hybridiza- A number of the formulated products have tion (SSH), to study the interaction between the been tested in the field and green house (Jaffee NTF and the nematodes. Ahrén et al. (2005) & Muldoon, 1995, Waller et al. 2001; Araujo compared the gene expression patterns in traps et al. 2004b) and the predatory activity of and in the mycelium of the nematode-trapping nematode-trapping fungi has been screened for fungus Monacrosporium haptotylum (Drechs use as biological control agents (Araujo et al. ler) Xing Z. Liu & K.Q. Zhang by microarray 1996, Araujo et al. 2004a). However, the deve- analysis. The ability of a nematode-trapping lopment of fungal biological control agents for fungus to become established in field soil is an commercial use may be limited by several important characteristic when considering its factors. e.g chemical, physical, and abiotic use as a biological control agent. Persson et al. factors in the soil would influence the growth (2000) determined the nematode-trapping fun- of fungi (Mo et al. 2005). gus, Arthrobotrys superba in the soil using a It is clear that the commercialization of radioactive tracing method. PCR is becoming these microorganisms lags far behind the an important tool in fungi not only for its resource investigation. One limiting factor is original use (nucleic acid amplification), but their inconsistent performance in the field, due also for gene cloning, the specific study of to virulence loss and insufficient quality con- genes involved in pathogenesis (Goller et al. trol in pre-application steps. With the help of 1998). advance techniques (e.g. genomics, crystallo- graphy, and the suppression subtractive hybri- Commercialization of products dization methods), we may obtain clear under- The goal of biocontrol research using standing on the encoding genes of traps, the nematophagous fungi is to provide additional signaling pathways that control the switch from tools for nematode management and to deliver saprotrophy to parasitism, and the molecular these tools to growers, therefore products must mechanism of the infection process (Yang et al. be commercialized. There have been relatively 2007c). Such information will provide a novel few successes in developing commercially approach to improve the efficacy of nematode-

12 Current Research in Environmental & Applied Mycology trapping fungi for biological control of nematophagous fungus Monacrosporium nematode pests. haptotylum. Microbiology 151, 789–803. Ahrén D, Ursing BM, Tunlid A. 1998 – Acknowledgements Phylogeny of nematode-trapping fungi Aung Swe would like to thank the based on 18S rDNA sequences. FEMS University of Hong Kong for the award of a Microbiology Letters 158, 179–184. postgraduate scholarship to study nematode- Akira N, Tadayoshi I. 1996 – Taxonomy and trapping fungi. ecology of Dactylella iridis: Its redes- cription as an entomogeneous and nema- References tode-capturing hyphomycete. Myco- science 37, 81–89. Abiko S, Saikawa M, Ratnawati. 2005 – Cap- Alston DG, Rangel DEN, Lacey LA, Golez ture of mites and rotifers by four strains HG, Jeong JK, Roberts DW. 2005 – of Dactylella gephyropaga known as a Evaluation of novel fungal and nematode nematophagous hyphomycete. Myco- isolates for control of Conotrachelus science 46, 22–26. nenuphar (Coleoptera: Curculionidae) Aboul-Eid HZ, Noweer EM, Ashour NE, larvae. Biological Control 35, 163–171. Ameen HH. 2006 – Evaluation of a Anastasiou CJ. 1964 – Some aquatic fungi nematode bio-product Dbx-20% against imperfecti from Hawaii. Pacific Science root-knot nematode Meloidogyne incog- 18, 202–206. nita affectting grapevine under field Anderson JB, Ullrich RC. 1979 – Biological conditions. Communications in Agri- species of Armillaria mellea in North cultural and Applied Biological Sciences America. Mycologia 71, 402–414. 71(3 Pt A), 659–668. Antonovics J, Hood M, Partain J. 2002 – The Åhman J, Ek B, Rask L, Tunlid A. 1996 – ecology and genetics of a host shift: Mi- Sequence analysis and regulation of a crobotryum as a model system. The gene encoding a cuticle-degrading serine American Naturalist 160, S40–S53. protease from the nematophagous fungus Araujo JV, Assis RCL, Campos AK, Mota Arthrobotrys oligospora. Microbiology MA. 2004a – In vitro predatory activity 142, 1605–1616. of nematophagous fungi Arthrobotrys, Åhman J, Johansson T, Olsson M, Punt PJ, Monacrosporium and Duddingtonia on Van den Hondel CAMJJ, Tunlid A. 2002 gastrointestinal parasites trichostrongy- – Improving the pathogenicity of a lids (Nematoda: Trichostrongyloidea) of nematode-trapping fungus by genetic bovines. Revista Brasileira de Parasito- engineering of a subtilisin with logia Veterinaria 13, 65–71. nematotoxic activity. Applied and Araujo JV, Guimares MP, Campos AK, S NC, Environmental Microbiology 68, 3408– Sarti P, Assis RCL. 2004b – Control of 3415. bovine gastrointestinal nematode para- Ahrén D, Tunlid A. 2003 – Evolution of sites using pellets of the nematode- parasitism in nematode-trapping fungi. trapping fungus Monacrosporium Journal of Nematology 35, 194–197. thaumasium. Cincia Rural 34, 457–463. Ahrén D, Faedo M, Rajashekar B, Tunlid A. Araujo JV, Neto AP, Azevedo MHF. 1996 – 2004 – Low genetic diversity among Screening parasitic nematode-trapping isolates of the nematode-trapping fungus fungi Arthrobotrys for passage through Duddingtonia flagrans: evidence for the gastrointestinal of calves. Arquivo recent worldwide dispersion from a Brasileiro de Medicina Veterinaria e single common ancestor. Mycological Zootecnia 48, 543–552. Research 108, 1205–1214. Balan J, Gerber NN. 1972 – Attraction and Ahrén D, Tholander M, Fekete C, Rajashekar killing of the nematode Panagrellus redi- B, Friman E, Johansson T, Tunlid A. vivus by the predacious fungus Arthro- 2005 – Comparison of gene expression in botrys dactyloides. Nematologica 18, trap cells and vegetative hyphae of the 163–173.

13 Barat M, Tarayre M, Atlan A. 2008 – Genetic fungus Duddingtonia flagrans in tropical divergence and ecological specialisation southeastern Brazil. Veterinary Parasito- of seed weevils (Exapion spp.) on gorses logy 163, 335–340. (Ulex spp.). Ecological Entomology 33, Burges A, Raw F. 1967 – Soil Biology. edn. 328–336. Academic Press, London. Barata M. 2006 – Marine fungi from Mira river Burnett JH. 2003 – Fungal Populations and salt marsh in Portugal. Revista Ibero- Species. Oxford University Press, americana de Micologia 23, 179–184. Oxford. Barron GL. 1977 – The nematode-destroying Byrne PJ, Jones EBG. 1975 – Effect of salinity fungi. topics in Mycobiology, Canadian on the reproduction of terrestrial and Biological Publications Ltd., Guelph, marine fungi. Transactions of the British Ontario N1H 6J9, Canada. Mycological Society 65: 185–200. Bidochka MJ, Kamp AM, Lavender TM. 2001 Cai L, Zhang KQ, McKenzie EHC, Hyde KD. – Habitat association in two genetic 2003 – Freshwater fungi from bamboo groups of the insect-pathologenic fungus and wood submerged in the Liput River Metarhzium anisoplaie, Uncovering cry- in the Philippines. Fungal Diversity 13, ptic species. Applied and Environmental 1–12. Microbiology 67, 1335–1342. Cai L, Hyde KD, Taylor PWJ, Weir BS, Waller Bird J, Larsen M, Nansen P, Kragelund HO, JM, Abang MM, Zhang JZ, Yang YL, Grønvold J, Henriksen SA, Wolstrup J. Phoulivong S, Liu ZY, Prihastuti H, 1998 – Dung-derived biological agents Shivas RG, McKenzie EHC, Johnston associated with reduced numbers of PR. 2009 – A polyphasic approach for infective larvae of equine strongyles in studying Colletotrichum. Fungal Diver- faecal cultures. Journal of Helminthology sity 39, 183–204. 72, 21–26. Cannon PF. 1997 – Diversity of the Phylla- Blomberg A, Adler L. 1993 – Tolerance of choraceae with special reference to the fungi to NaCl. In Stress Tolerance of tropics. In biodiversity of tropical micro- fungi. (ed. DH Jennings). Marcel Dekker fungi (ed. KD Hyde). Hong Kong Inc, New York, 209–232. University Press, Hong Kong, 255–278. Boag B, Lopez-Llorca LV. 1989 – Nematodes Carvalho RO, Araújo JV, Braga FR, Ferreira and nematophagous fungi associated with SR, Araujo JM, Silva AR, Frassy LN, cereal fields and permanent pasture in Alves CDF. 2009 – Biological control of Eastern Scotland. Crop Research 29, 1– Ancylostomosis in dogs using the nema- 10. tode-trapping fungus Monacrosporium Bogus MI, Czygier M, Kedra E, Samborski J. thaumasium in southeastern Brazil. 2005 – In vitro assessment of the in- Veterinary Parasitology 165, 179–183 fluence of nutrition and temperature on Castillo G, Demoulin V. 1997 – NaCl salinity growing rates of five Duddingtonia and temperature effects on growth of flagrans isolates, their insecticidal pro- three wood-rotting basidiomycetes from perties and ability to impair Heligmoso- a Papua New Guinea coastal forest. moides polygyrus motility. Experimental Mycological Research 101, 341–344. Parasitology 109, 115–123. Chase TE, Ullrich RC. 1990 – Five Genes Bordallo JJ, Lopez-Llorca LV, Jansson HB, Determining Intersterility in Heterobasi- Salinas J, Persmark L, Asensio L. 2002 – dion annosum. Mycologia 82, 73–81. Colonization of plant roots by egg- Ciordia H, Bizzell WE. 1963 – The effects of parasitic and nematode-trapping fungi. various constant temperatures on the New Phytologist 154, 491–499. development of the free living-stages of Braga FR, Araújo JV, Silva AR, Araujo JM, some nematode parasites of cattle. Carvalho RO, Tavela AO, Campos AK, Journal of Parasitology 49, 60–63. Carvalho GR. 2009 – Biological control Clipson N, Hooley P. 1995 – Salt tolerance of horse cyathostomin (Nematoda: Cya- strategies in marine fungi. Mycologist 9, thostominae) using the nematophagous 3–5.

14 Current Research in Environmental & Applied Mycology

Connell L, Redman R, Craig S, Rodriguez R. Davidson DE. 1974 – Salinity tolerance and 2006 – Distribution and abundance of ecological aspects of some microfungi fungi in the soils of Taylor Valley, from saline and non-saline soils in Antarctica. Soil Biology and Bioche- Wyoming. Mycopatholgia et Mycologia mistry 38, 3083–3094. Applicata 54, 181–188. Connell L, Redman R, Craig S, Scorzetti G, De Hoog G. 1985 – Taxonomy of the Iszard M, Rodriguez R. 2008 – Diversity Dactylaria Complex, IV. Dactylaria, of soil yeasts isolated from South Neta, Subulispora and Scolecobasidium. Victoria Land, Antarctica. Microbial Studies in Mycology 26, 1–6 Ecology, 1–12. De Hoog GS, Van Oorschot CAN. 1985 – Cooke RC. 1963 – Ecological characteristics of Taxonomy of the Dactylaria complex. nematode-trapping hyphomycetes I. Studies in Mycology 26, 1–122. Preliminary studies. Annals of Applied Dias AS, Araújo JV, Campos AK, Braga FR, Biology 52, 431–437. Fonseca TA. 2007 – Application of a Cooke RC. 1968 – Relationships between formulation of the nematophagous fun- nematode-destroying fungi and soil- gus Duddingtonia flagrans in the control borne phytonematodes. Phytopathology of cattle gastrointestinal 58, 909–913. nematodiosis. World Journal of Cooke R, Dickinson C. 1965 – Nematode- Microbiology and Biotechnology 23(9), trapping species of Dactylella and 1245–1252. Monacrosporium. Transactions of the Dijksterhuis J, Veenhuis M, Harder W, British Mycological Society 48(4), 621– Nordbring-Hertz B. 1994 – Nemato- 629. phagous fungi: Physiological aspects and Corda ACI. 1839 – Pracht-Flora Europaïscher structure-function relationships. In Schimmelbildungen. I-VIII, 55 pp, 25 Advance in Microbial Physiology. Vol. tabs. Germany, Leipzig & Dresden. 36 Academic Press, 111–143. Couch BC, Fudal I, Lebrun MH, Tharreau D, Dong LQ, Zhang KQ. 2006 – Microbial control Valent B, van Kim P, Notteghem JL, of plant-parasitic nematodes: a five-party Kohn LM. 2005 – Origins of host- interaction. Plant and Soil 288, 31–45. specific populations of the blast pathogen Douhan GW, Smith ME, Huyrn KL, Magnaporthe oryzae in crop domes- Westbrook A, Beerli P, Fisher AJ. 2008 – tication with subsequent expansion of Multigene analysis suggests ecological pandemic clones on rice and weeds of speciation in the fungal pathogen rice. Genetics 170, 613–630. Claviceps purpurea. Molecular Ecology Dackman C, Chet I, Nordbring-Hertz B. 1989 – 17, 2276–2286. Fungal parasitism of the cyst nematode Duarte S, Pascoal C, Cássio F. 2008 – High Heterodera schachtii: infection and diversity of fungi may mitigate the enzymatic activity. FEMS Microbiology impact of pollution on plant litter decom- Letters 62, 201–208. position in streams. Microbial Ecology Dackman HB, Jansson and Nordbring–Hertz B. 56, 688–695. 1992 – Nematophagous fungi and their Duarte S, Pascoal C, Cássio F, Bärlocher F. activities in soil. In Soil biochemistry. 2006 – Aquatic hyphomycete diversity (eds G Stotzky, JM Bollag). Marcel and identity affect leaf litter decomposi- Dekker, New York, 95–103. tion in microcosms. 147, 658–666. Damare S, Raghukumar C. 2008 – Fungi and Duddington CL. 1951 – The ecology of macroaggregation in deep-sea sediments. predaceous fungi. I. Preliminary survey. Microbial Ecology 56, 168–177. Transactions of the British Mycological Dan NP, Visvanathan C, Polprasert C, Ben Society 34, 322–331. Aim R. 2002 – High salinity wastewater Duddington CL. 1954 – Nematode-destroying treatment using yeast and bacterial mem- fungi in agricultural soils. Nature 173, brane bioreactors. Water Science and 500–501. Technology 46, 201–209.

15 Duponnois R, Chotte JL, Sall S, Cadet P. 2001 australis. I. Influence of – The effects of organic amendments on temperature, pH and salinity on the the interactions between a nemato- growth and sporulation of the fungus in phagous fungus Arthrobotrys oligospora the laboratory. Mycopathologia 96, 87– and the root-knot nematode Meloidogyne 90. mayaguensis parasitizing tomato plants. Giraud T, Refrégier G, Le Gac M, de Vienne Biology and Fertility of Soils 34, 1–6. DM, Hood ME. 2008 – Speciation in Ellis CJ, Coppins BJ, Dawson TP. 2007 – fungi. Fungal Genetics and Biology 45, Predicted response of the lichen epiphyte 791–802. Lecanora populicola to climate change Goettel MS, St Leger RJ, Rizzo NW, Staples scenarios in a clean-air region of RC, Roberts DW. 1989 – Ultrastructural Northern Britain. Biological Conser- localization of a cuticle-degrading pro- vation 135, 396–404. tease produced by the entomopathogenic Farrell FC, Jaffee BA, Strong DR. 2006 – The fungus Metarhizium anisopliae during nematode-trapping fungus Arthrobotrys penetration of host (Manduca sexta) oligospora in soil of the Bodega marine cuticle. Microbiology 135, 2233–2239. reserve: distribution and dependence on Goller SP, Gorfer M, Mach RL, Kubicek CP. nematode-parasitized moth larvae. Soil 1998 – Gene cloning using PCR. In Biology & Biochemistry 38, 1422–1429. Applications of PCR in Mycology (eds. Fell JW, Scorzetti G, Connell L, Craig S. 2006 PD Bridge, DK Arora, CA Reddy, RP – Biodiversity of micro-eukaryotes in Elander). CAB international, Walling Antarctic Dry Valley soils with <5% soil ford, 21–45. moisture. Soil Biology and Biochemistry Gray NF. 1984 – Ecology of nematophagous 38, 3107–3119. fungi: Methods of collection, isolation Fernandez AS, Larsen M, Wolstrup J, and maintenance of predatory and endo- Gronvold J, Nansen P, Bjorn H. 1999 – parasitic fungi. Mycopathologia 86, 143– Growth rate and trapping efficacy of 153. nematode-trapping fungi under constant Gray NF. 1985 – Ecology of nematophagous and fluctuating temperatures. Parasito- fungi: effect of soil moisture, organic logy Research 85, 661–668. matter, pH, and nematode density in dis- Field JI, Webster J. 1977 – Traps of predacious tribution. Soil Biology and Biochemistry fungi attract nematodes. Transactions of 17, 499–507. the British Mycological Society 68, 467– Gray NF. 1987 – Nematophagous fungi with 469. particular reference to their ecology. Fisher MC, Hanage WP, de Hoog S, Johnson Biological Reviews 62, 245–304. E, Smith MD, White NJ, Vanittanakom Gray NF. 1988 – Ecology of nematophagous N. 2005 – Low effective dispersal of fungi: Effect of the soil nutrients N, P asexual genotypes in heterogeneous land- and K, and seven major metals on scapes by the endemic pathogen Peni- distribution. Plant and Soil 108, 286–290. cillium marneffei. PLoS Pathogens 1, 20. Gray NF, Bailey F. 1985 – Ecology of Fryar SC, Booth W, Davies J, Hodgkiss IJ, nematophagous fungi: vertical distri- Hyde KD. 2004 – Distribution of fungi bution in a deciduous woodland. Plant on wood in the Tutong River, Brunei. and Soil 86, 217–223. Fungal Diversity 17, 17–38. Gronvold J, Wolstrup J, Nansen P, Larsen M, Gao L, Sun MH, Liu XZ, Che YS. 2007 – Henriksen SA, Bjorn H, Kirchheiner K, Effects of carbon concentration and car- Lassen K, Raw H, Kristiansen, HL. 1999 bon to nitrogen ratio on the growth and – Biotic and abiotic factors influencing sporulation of several biocontrol fungi. growth rate and production of traps by Mycological Research 111, 87–92. the nematode-trapping fungus Dudding- Gardner JM, Pillai JS. 1986 – Tolypocladium tonia flagrans when induced by Cooperia cylindrosporum (Deuteromycotina: Mo- oncophora larvae. Journal of Helmin- niliales), a fungal pathogen of the thology 73, 129–136.

16 Current Research in Environmental & Applied Mycology

Grove WB. 1884 – New or noteworthy fungi. tropical forest in Puerto Rico. Tropical Journal of Botany 22, 195–201. Ecology 38, 307–315. Gulis V, Suberkropp K, Rosemond AD. 2008 – Hyde KD. 1996 – Biodiversity of microfungi in Comparison of fungal activities on wood north Queensland. Australian Systematic and leaf litter in unaltered and nutrient- Botany 9, 261–271. enriched headwater streams. Applied and Hyde KD. 2001 – Where are the missing Environmental Microbiology 74, 1094– fungi? Does Hong Kong have any 1101. answers? Mycological Research 105, Hagedorn G, Scholler M. 1999 – A revaluation 1514–1518. of predatory orbiliaceous fungi I. Phylo- Hyde KD, Alias SA. 2000 – Biodiversity and genetic analysis using rDNA sequence distribution of fungi associated with data. Sydowia 51, 27–48. decomposing Nypa fruticans. Biodiver- Hammond PM. 1992 – Species inventory. In sity and Conservation 9, 393–402. Global biodiversity – Status of the Hyde KD, Goh TK. 1998 – Fungi on sub- Earth’s living resources (ed. B Groom merged wood in Lake Barrine, north bridge). Chapman & Hall, London, UK, Queensland, Australia. Mycological 17–39. Research 102, 739–749. Hao Y, Luo J, Zhang KQ. 2004 – A new Hyde KD, Sarma VV. 2006 – Biodiversity and aquatic nematode-trapping hyphomycete. ecological observations on filamentous Mycotaxon 89, 235–239. fungi of mangrove palm Nypa fruticans Hao Y, Mo M, Su H, Zhang KQ. 2005 – Wurumb (Liliopsida-Arecales) along the Ecology of aquatic nematode-trapping Tutong River, Brunei. Indian Journal of hyphomycetes in southwestern China. Marine Sciences 35, 297–307. Aquatic Microbial Ecology 40, 175–181. Hyde KD, Farrant CA, Jones EBG. 1987 – Harrington TC, Rizzo DM. 1999 – Defining Isolation and culture of marine fungi. species in the fungi. In Structure and Botanica Marina 30, 291–303. Dynamics of Fungal Populations. (ed. JJ Hyde KD, Bussaban B, Paulus B, Crous PW, Worrall). Kluwer Academic, 43–70. Lee S, Mckenzie EHC, Photita W, Harrison JL, Jones EBG. 1971 – Salinity tole- Lumyong S. 2007 – Diversity of saprobic rance of Saprolegnia parasitica Coker. microfungi. Biodiversity and Conserva- Mycopatholgia et Mycologia Applicata tion 16, 7–35. 43, 297–307. Index Fungorum. (2011). http://www.Index Hatfield T, Schluter D. 1999 – Ecological fungorum.org/names/Names.asp speciation in sticklebacks: Environment- Indra V, Meiyalagan V. 2005 – Diversity and dependent hybrid fitness. Evolution 53, distribution of microfungi in polluted and 866–873. nonpolluted water bodies from an Indus- Hawksworth DL. 1991 – The fungal dimension trial areas of River Palar, Vellore-India. of biodiversity: magnitude, significance, Asian Journal of Microbiology, Biotech- and conservation. Mycological Research nology and Environmental Sciences 7, 95, 641–655. 723–725. Hay FS, Niezen JH, Miller C, Bateson L, Ingold CT. 1944 – Some new aquatic hypho- Robertson H. 1997 – Infestation of sheep mycetes. Transactions of the British dung by nematophagous fungi and Mycological Society 27, 45–46. implications for the control of free-living Jaffee BA. 2003 – Correlations between most stages of gastro-intestinal nematodes. Vet probable number and activity of nema- Parasitol 70, 247–254. tode-trapping fungi. Phytopathology 93, Heintz CE, Pramer D. 1972 – Ultrastructure of 1599–1605. nematode-trapping fungi. Journal of Jaffee BA. 2004a – Do organic amendments Bacteriology 110, 1163. enhance the nematode-trapping fungi Huhndorf SM, Lodge DJ. 1997 – Host speci- Dactylellina haptotyla and Arthrobotrys ficity among wood-inhabiting pyreno- oligospora? Journal of Nematology 36, mycetes (Fungi, Ascomycetes) in a wet 267–275.

17 Jaffee BA. 2004b – Wood, nematodes, and the temperature scanning electron micro- nematode-trapping fungus Arthrobotrys scopy. Mycologia 92, 10–15. oligospora. Soil Biology and Bioche- Jansson HB, Tunlid A, Nordbring-Hertz B. mistry 36, 1171–1178. 1997 – Biological control: nematodes. In Jaffee BA. 2006 – Interactions among a soil Fungal Biotechnology. (ed. T Anke). organic amendment nematodes and the Chapman and Hall, Weinheim, 38–50. nematode-trapping fungus Dactylellina Jeewon R, Hyde KD. 2007 – Detection and candidum. Phytopathology 96, 1388– diversity of fungi from envrionmental 1396. samples: Traditional versus molecular Jaffee BA, Muldoon AE. 1995 – Susceptibility approaches. In Advanced techniques in of root-knot and cyst nematodes to the soil microbiology, Soil biology Vol. 11 nematode-trapping fungi Monacrospo- (eds A Varma, R Oelmuller). Springer, rium ellipsosporum and M. cionopagum. Berlin, 1–15. Soil Biology and Biochemistry 27, 1083– Johnson JA, Harrington TC, Engelbrecht CJB. 1090. 2005 – Phylogeny and taxonomy of the Jaffee BA, Strong DR. 2005 – Strong bottom- north American clade of the Ceratocystis up and weak top-down effects in soil: fimbriata complex. Mycologia 97, 1067– nematode-parasitized insects and nema- 1092. tode-trapping fungi. Soil Biology and Johnson TW, Autery CL. 1961 – An Arthro- Biochemistry 37, 1011–1021. botrys from brackish water. Mycologia Jansson HB. 1982 – Predacity of nemato- 53, 432–433. phagous fungi and its relation to the Jones EBG, Byrne PJ. 1976 – Physiology of attraction of nematodes. Microbial the higher marine fungi. Recent Ecology 8, 233–240. Advances in Aquatic Mycology, 135– Jansson HB, Friman EVA. 2000 – Infection- 175. related surface proteins on conidia of the Jones FR. 1958 – Three zoopagales from nematophagous fungus Drechmeria brackish water. Nature 181, 575–576. coniospora. Mycological Research 103, Juniper S, Abbott LK 2006 – Soil salinity 249–256. delays germination and limits growth of Jansson HB, Lopez-Llorca LV. 2001 – Biology hyphae from propagules of arbuscular of Nematophagous Fungi. In Tricho- mycorrhizal fungi. Mycorrhiza 16, 371– mycetes and other fungal groups. (eds. 379. JK Misra, BW Horn). Science Publishers, Kano S, Aimi T, Masumoto S, Kitamoto Y, Plymouth, UK. 145–172. Morinaga T. 2004 – Physiology and Jansson HB, Nordbring-Hertz B. 1979 – molecular characteristics of a pine wilt Attraction of nematodes to living myce- nematode-trapping fungus, Monacrospo- lium of nematophagous fungi. Journal of rium megalosporum. Current Microbio- General Microbiology 112, 89–93. logy 49, 158–164. Jansson HB, Nordbring-Hertz B. 1980 – Inter- Kendrick B. 2001 – The Fifth Kingdom 3rd Ed. actions between nematophagous fungi Mycologue Publications, Canada. and plant-parasitic nematodes: attraction, Kerry BR. 1987 – Biological control. In Prin- induction of trap formation and capture. ciples and practice of nematode control Nematologica 26, 383–389. in crops (eds. RH Brown, BR Kerry). Jansson HB, Nordbring-Hertz B. 1988 – Infec- Academic Press, New York, 233–263. tion mechanisms in the fungus-nematode Kerry BR. 2000 – Rhizosphere interactions and system. In Diseases of nematodes, Vol. 2 the exploitation of microbial agents for (eds. GO Poinar, HB Jansson). CRC the biological control of plant-parasitic Press, Boca Raton, 58–72. nematodes. Annual Review of Phyto- Jansson HB, Persson C, Odeslius R. 2000 – pathology 38, 423–441. Growth and capture activities of nemato- Kerry BR, Hominick WB. 2002 – Biological phagous fungi in soil visualized by low control. In The biology of nematode. (ed.

18 Current Research in Environmental & Applied Mycology

DL Lee). Taylor&Francis, London, New Laurin V, Labbe N, Parent S, Juteau P, York, 483–510. Villemur R. 2008 – Microeukaryote Kerry BR, Kirkwood IA, de Leij FAAM, Barba diversity in a marine methanol-fed J, Leijdens MB, Brookes PC. 1993 – fluidized denitrification system. Micro- Growth and survival of Verticillium bial Ecology 56, 637–648. chlamydosporium Goddard, a parasite of Le Gac M, Hood ME, Fournier E, Giraud T. nematodes, in soil. Biocontrol Science 2007 – Phylogenetic evidence of host- and Technology 3, 355–365. specific cryptic species in the anther smut Khan A, Williams KL, Nevalainen HKM. 2006 fungus. Evolution 61, 15–26. – Infection of plant-parasitic nematodes Li X, Zhang H, Wu M, Zhang Y, Zhang C. by Paecilomyces lilacinus and Mona- 2008 – Effect of methamidophos on soil crosporium lysipagum. BioControl 51, fungi community in microcosms by plate 659–678. count, DGGE and clone library analysis. Kirk JL, Beaudette LA, Hart M, Moutoglis P, Journal of Environmental Sciences 20, Klironomos JN, Lee H, Trevors JT. 2004 619–625. – Methods of studying soil microbial Li Y, Hyde KD, Jeewon R, Lei C, Vijaykrishna diversity. Journal of Microbiological D, Zhang KQ. 2005 – Phylogenetics and Methods 58, 169–188. evolution of nematode-trapping fungi Kirk PM, Cannon PF, Minter DW, Stalpers JA. (Orbiliales) estimated from nuclear and 2008 – Dictionary of the fungi, 10th edn. protein coding genes. Mycologia 97, CABI publishing, Wallingford, UK. 1034–1046. Kohlmeyer J, Kohlmeyer E. 1979 – Marine Li Y, Jeewon R, Hyde KD, Mo MH, Zhang Mycology: The higher fungi. 1st edn. KQ. 2006 – Two new species of nema- Academic Press, London. tode-trapping fungi: relationships infered Kohn LM. 2005 – Mechanisms of fungal from morphology, rDNA and protein speciation. Annual Review of Phyto- gene sequence analyses. Mycological pathology 43, 279–308. Research 110(7), 790–800. Kramer VI. 1990 – Laboratory evaluation of Liou GY, Tzean SS. 1997 – Phylogeny of the Lagenidium giganteum (Oomycetes: genus Arthrobotrys and allied nematode- Lagenidiales) in water from Contra Costa trapping fungi based on rDNA County, California, mosquito sources. sequences. Mycologia 89, 876–884. Journal of American Mosqueto Control Liu B, Liu XZ, Zhuang WY. 2005 – Orbilia Association 6, 79–83. querci sp. nov. and its knob-forming Kumar D, Singh KP. 2006a – Assessment of nematophagous anamorph. FEMS Micro- Predacity and Efficacy of Arthrobotrys biology Letters 245, 99–105. dactyloides for Biological Control of Liu B, Liu XZ, Zhuang WY, Baral HO. 2006 – Root Knot Disease of Tomato. Journal of Orbiliaceous fungi from Tibet, China. Phytopathology 154, 1–5. Fungal Diversity 22, 107–120. Kumar D, Singh KP. 2006b – Variability in In- Liu X, Ding L, Wu X, Shen C. 1992 – Nemo- dian isolates of Arthrobotrys dactylloides tophagous fungi in China. Mycosystema Drechsler a nematode-trapping fungus. 5, 117–126. Current Microbiology 52, 293–299. Liu X, Xiang M, Che Y. 2009 – The living Kuyama S, Pramer D. 1962 – Pruification and strategy of nematophagous fungi. Myco- properties of a protein having nemin science 50(1), 20–25. activity. Biochim Biophys Acta 56, 631– Liu XF, Zhang KQ. 2003 – Dactylella shizi- 632. shanna sp. Nov., from Shizi Mountain, Lai X, Cao L, Tan H, Fang S, Huang Y, Zhou China. Fungal Diversity 14, 103–107. S. 2007 – Fungal communities from me- Lonsdale D, Pautasso M, Holdenrieder O. 2008 thane hydrate-bearing deep-sea marine – Wood-decaying fungi in the forest: sediments in South China Sea. ISME conservation needs and management Journal 1, 756–762. options. European journal of forest research 127, 1–22.

19 Lopez-Llorca LV, Duncan GH. 1988 – A study Mankau R, McKenny MV. 1976 – Spatial of fungal endoparasitism of the cereal distribution of nematophagous fungi cyst nematode (Heterodera avenae) by associated with Meloidogyne incognita scaning electron microscopy. Canadian on peach. Journal of Nematology 8, 294– Journal of Microbiology 34, 613–619. 295. Lopez-Llorca LV, Robertson WM. 1992 – Martin DL, Zhang H. 2002 – Evaluating the Immunocytochemical localization of a efficacy of Arthrobotrys oligospora to re- 32-kDa protease from the nemato- duce plant parasitic nematodes in putting phagous fungus Verticillium suchlaspo- greens. Phytopathology 92, S88. rium in infected nematode eggs. Fungal Maslen NR. 1982 – An unidentified nematode- Genetics and Biology 16, 261–267. trapping fungus from a pond on Lopez-Villavicencio M, Enjalbert J, Hood ME, Alexander Island. British Antarctic Shykoff JA, Raquin C, Giraud T. 2005 – Survey Bulletin 51, 285–287. The anther smut disease on Gypsophila McSorley R, Wang KH, Kokalis-Burelle N, repens: a case of parasite sub-optimal Church G. 2006 – Effects of soil type and performance following a recent host steam on nematode biological control shift? Journal of Evolutionary Biology potential of the rhizosphere community. 18, 1293–1303. Nematropica 36, 197–214. Lord JC, Roberts DW. 1985 – Effects of Mendoza-De GP, Zapata NC, Liebano HE, salinity, pH, organic solutes, anaerobic Lopez AME, Rodriguez DH, Garduno conditions, and the presence of other RG. 2006 – Biological control of gastro- microbes on production and survival of intestinal parasitic nematodes using Dud- Lagenidium giganteum (Oomycetes: dingtonia flagrans in sheep under natural Lagenidiales) zoospores. Journal of conditions in Mexico. Annals of the New Invertebrate Pathology 45, 331–338. York Academy of Sciences 1081, 355– Lord JC, Fukuda T, Daniels E. 1988 – Salinity 359. tolerance of Leptolegnia chapmanii Mennan S, Chen S, Melakeberhan H. 2006 – (Oomycetes: Saprolgeniales), a fungal Suppression of Meloidogyne hapla pathogen of mosquito larvae. Journal of populations by Hirsutella minnesotensis. the American Mosquito Control Asso- Biocontrol Science and Technology 16, ciation 4, 370–371. 181–193. Lorenz R, Molitoris HP. 1992 – Combined Minglian Z, Minghe M, Keqin Z. 2004 – influence of salinity and temperature Characterization of a neutral serine (Phoma-pattern) on growth of marine protease and its full-length cDNA from fungi. Canadian Journal of Botany 70, the nematode-trapping fungus Arthro- 2111–2115. botrys oligospora. Mycologia 96, 16–22. Lysek H, Krajci D. 1987 – Penetration of Mitsui Y, Yoshida T, Okamoto K, Ishii R. ovicidal fungus Verticillium chlamydo- 1976 – Relationship between nematode- sporium through the Ascaris lumbri- trapping fungi and Meloidogyne hapla in coides egg-shells. Folia Parasitol (Praha) the peanut field. Japanese journal of 34, 57–60. Nematology 6, 47–55 Maciel AS, Freitas LG, Campos AK, Lopes EA, Mo MH, Chen WM, Su HY, Zhang KQ, Duan Araújo JV. 2010 – The biological control CQ, He DM. 2006 – Heavy metal tole- of Ancylostoma spp. dog infective larvae rance of nematode-trapping fungi in lead- by Duddingtonia flagrans in a soil micro- polluted soils. Applied Soil Ecology 31, cosm. Veterinary Parasitology 173(3–4), 11–19. 262–270. Mo MH, Chen WM, Yang HR, Zhang KQ. Maher PA. 1993 – Activation of phosphorty- 2008 – Diversity and metal tolerance of rosine phosphatase activity by reduction nematode-trapping fungi in Pb-polluted of cell-substrate adhesion. Proceedings of soils. Journal of Microbiology (Seoul, the National Academy of Sciences, USA Korea) 46, 16–22. 90, 11177–11181.

20 Current Research in Environmental & Applied Mycology

Mo MH, Xu C, Zhang KQ. 2005 – Effects of fungus Arthrobotrys oligospora. Physiol. carbon and nitrogen sources, carbon to Plant 29, 223–233. nitrogen ratio, and initial pH on the Nordbring-Hertz B, Stalhammar-Carlemalm growth of nematophagous fungus Pocho- M. 1978 – Capture of nematodes by nia chlamydosporia in liquid culture. Arthrobotrys oligospora, an electron Mycopathologia 159, 381–387. microscopic study. Canadian Journal of Morelet M. 1968 – De aliquibus in mycologia Botany 56, 1297–1307. novitatibus (5e note). Bulletin de la O'Connell RJ. 1991 – Cytochemical analysis of Société des Sciences Naturelles et infection structures of Colletotrichum d'Archéologie de Toulon et du Var 178, 6. lindemuthianum using fluorochrome- Morgan M, Behnke JM, Lucas JA, Peberdy JF. labelled lectins. Physiological and Mole- 1997 – In vitro assessment of the cular Plant Pathology 39, 189–200. influence of nutrition, temperature and Ogden R, Thorpe RS. 2002 – Molecular evi- larval density on trapping of the infective dence for ecological speciation in tropical larvae of Heligmosomoides polygyrus by habitats. Proceedings of the National Arthrobotrys oligospora, Duddingtonia Academy of Sciences 99, 13612. flagrans and Monacrosporium megalo- Onofri S, Tosi S. 1992 – Arthrobotrys ferox sp. sporum. Parasitology 115, 303–310. nov. a springtailcapturing hyphomycete Morton CO, Hirsch PR, Kerry BR. 2004 – from Continental Antarctica. Mycotaxon Infection of plant-parasitic nematodes by 44, 445–451. nematophagous fungi. A review of the Oudemans CAJA. 1885 – Aanwinsten voor de application of molecular biology to flora mycologica van Nederland. Neder- understand infection processes and to landsch Kruidkundig Archief 4, 236–257. improve biological control. Nematology Paraud C, Pors I, Chartier C. 2007 – Effi- 6, 161–170. ciency of feeding Duddingtonia flagrans Mukhopadhyaya PN, Nagee A, Sanyal PK. chlamydospores to control nematode 2004 – Dense molecular marking reveals parasites of first-season grazing goats in genetic diversity in morphologically France. Veterinary Research Communi- similar isolates of the nematophagous cations 31, 305–315. fungus Duddingtonia flagrans. Paraud C, Pors I, Chicard C, Chartier C. 2006 – Roumanian archives of microbiology and Comparative efficacy of the nematode- immunology 63, 253–270. trapping fungus Duddingtonia flagrans Murray DS, Wharton DA. 1990 – Capture and against Haemonchus contortus, Telador- penetration processes of the free-living sagia circumcincta and Trichostrongylus juveniles of Trichostrongylus colubrifor- colubriformis in goat faeces: Influence of mis (Nematoda) by the nematophagous the duration and of the temperature of fungus, Arthrobotrys oligospora. Parasi- coproculture. Parasitology Research 98, tology 101, 93–100. 207–213. Nambiar GR, Jaleel CA, Raveendran K. 2008 – Peach M. 1950 – Aquatic predacious fungi I. A comparative account of backwater and Transactions of the British Mycological brackish water marine mycoflora of north Society 33, 148–153. Malabar (Kerala) India. Comptes Peach M. 1952 – Aquatic predacious fungi. II. Rendus, Biologies 331, 294–297. Transactions of the British Mycological Natvig DO, May G. 1996 – Fungal evolution Society 35, 19–23. and speciation. Journal of Genetic 75, Persmark L, Jansson HB. 1997 – Nema- 441–452. tophagous fungi in the rhizosphere of Nordbring-Hertz B, Tunlid A. 2000 – agricultural crops. FEMS Microbiology Nematophagous fungi. In Encyclopedia Ecology 22, 303–312. of life science. Macmillan Publishers, Persmark L, Nordbring-Hertz B. 1997 – Basingstoke. Conidial trap formation of nematode- Nordbring-Hertz B. 1973 – Peptide induced trapping fungi in soil and soil extracts. morphogenesis in the nematode-trapping

21 FEMS Microbiology Ecology 22, 313– species group (Squamata:Scincidae). 323. Evolution 56, 1498–1513. Persson C, Olsson S, Jansson HB. 2000 – Ritchie D. 1959 – The effect of salinity and Growth of Arthrobotrys superba from a temperature on marine and other fungi birch wood resource base into soil from various climates. Bulletin of the determined by radioactive tracing. FEMS Torrey Botanical Club 86, 367–373. Microbiology Ecology 31, 47–51. Rong De J, Joo WS, Ro DP, Yong WK, Hari Persson Y, Baath E. 1992 – Quantification of BK, Kil YK. 2005 – Effect of chitin mycoparasitism by the nematode- compost and broth on biological control trapping fungus Arthrobotrys oligospora of Meloidogyne incognita on tomato on Rhizoctonia solani and the influence (Lycopersicon esculentum Mill.). Nema- of nutrient levels. FEMS Microbiology tology V7, 125–132. Letters 101, 11–16. Rosen S, Sjollema K, Veenhuis M, Tunlid A. Peterson EA, Katznelson H. 1964 – Occurrence 1997 – A cytoplasmic lectin produced by of nematode-trapping fungi in the the fungus Arthrobotrys oligospora rhizosphere. Nature 204, 1111–1112. functions as a storage protein during Pfister DH. 1994 – Orbilia fimicola, a nemato- saprophytic and parasitic growth. Micro- phagous discomycete and its Arthro- biology 143, 2593–2604. botrys anamorph. Mycologia 86, 451– Rubner A. 1994 – Predaceous fungi from 453. Ecuador. Mycotaxon 51, 143–151. Pfister DH. 1997 – Castor, Pollux and life Rubner A. 1996 – Revision of predacious histories of fungi. Mycologia 89, 1–23. hyphomycetes in the Dactylella-Mona- Poon MOK, Hyde KD. 1998 – Biodiversity of crosporium complex. Studies in Myco- intertidal estuarine fungi on Phragmites logy 39, 1–134. at Mai Po marshes, Hong Kong. Botanica Rundle HD, Nosil P. 2005 – Ecological specia- Marina 41, 141–155. tion. Ecology Letters 8, 336–352. Porras-Alfaro A, Herrera J, Sinsabaugh RL, Sahai AS, Manocha MS. 1993 – Chitinases of Odenbach KJ, Lowrey T, Natvig DO. fungi and plants: their involvement in 2008 – A novel root fungal consortium morphogenesis and host-parasite inter- associated with a dominant desert grass. action. FEMS Microbiology Reviews 11, Applied and Environmental Micro- 317–338. biology 74, 2805–2813. Sánchez-Moreno S, Smukler S, Ferris H, Pringle A, Baker DM, Platt JL, Wares JP, O’Geen AT, Jackson LE. 2008 – Nema- Latge JP, Taylor JW. 2005 – Cryptic tode diversity, food web condition, and speciation in the cosmopolitan and clonal chemical and physical properties in human pathogenic fungus Aspergillus different soil habitats of an organic farm. fumigatus. Evolution 59, 1886–1899. Biology and Fertility of Soils 44(5), 727– Raberg U, Hogberg NOS, Land CJ 2005 – 744. Detection and species discrimination Santurio JM, Zanette RA, Da Silva AS, Fanfa using rDNA T-RFLP for identification of VR, Farret MH, Ragagnin L, Hecktheuer wood decay fungi. Holzforschung 59, PA, Monteiro SG. 2011 – A suitable 696–702. model for the utilization of Duddingtonia Radwan MA, Ibrahim HS, Kassem SI, Abu- flagrans fungus in small-flock-size sheep Elamayem MM. 2007 – Integrated farms. Experimental Parasitology, Article management of root-knot nematode, in Press. Meloidogyne incognita infecting tomato. Saxena G. 2008 – Observations on the occur- Pakistan Journal of Nematology 25, 295– rence of nematophagous fungi in Scot 303. land. Applied Soil Ecology 39, 352–357. Richmond JQ, Reeder TW. 2002 – Evidence Saxena G, Lysek G. 1993 – Observation of for parallel ecological speciation in Scin- nematophagous fungi in natural soils by cid lizards of the eumeces Skiltonianus fluorescence microscopy and their

22 Current Research in Environmental & Applied Mycology

correlation with isolation. Mycological plant-parasitic nematodes. Australasian Research 97, 1005–1011. Plant Pathology 36, 124–134. Saxena G, Mukerji KG. 1991 – Distribution of Singh KP, Jaiswal RK, Kumar N, Kumar D. nematophagous fungi in Varanasi, India. 2007 – Nematophagous fungi associated Nova Hedwigia 52, 487–495. with root galls of rice caused by Meloido- Sayre RM, Walter DE. 1991 – Factors gyne graminicola and its control by affecting the efficacy of natural enemies Arthrobotrys dactyloides and Dactylaria of nematodes. Annual Review of Phyto- brochopaga. Journal of Phytopathology pathology 29, 149–166. 155, 193–197. Schenck S, Chase T, Rosenzweig WD, Pramer Smith ME, Jaffee BA. 2009 – PCR primers D. 1980 – Collagenase Production by with enhanced specificity for Nematode- Nematode-Trapping Fungi. Applied and trapping fungi (Orbiliales). Microbial Environmental Microbiology 40, 567– Ecology 58(1), 117–128. 570. Soares ACF, Sousa CDS, Coimbra JL, Schenck S, Kendrick WB, Pramer D. 1977 – A Machado GDS, Garrido MDS, Almeida new nematode-trapping hyphomycetes NDS. 2006 – Predatory ability of Arthro- and a revaluation of Dactylaria and botrys musiformis and Monacrosporium Arthrobotrys. Canadian Journal of thaumasium on Scutellonema bradys. Botany 55, 977–985. Scientia Agricola 63, 396–398. Schmidt AR, Dörfelt H, Perrichot V. 2008 – Sole M, Fetzer I, Wennrich R, Sridhar KR, Palaeoanellus dimorphus gen. et sp. nov. Harms H, Krauss G. 2008 – Aquatic (Deuteromycotina): A cretaceous preda- hyphomycete communities as potential tory fungus. American Journal of Botany bioindicators for assessing anthropogenic 95, 1328–1334. stress. Science of the Total Environment Scholler M, Hagedorn G, Rubner A. 1999 – A 389, 557–565. revaluation of predatory orbiliaceous Sorbo DG, Marziano F, D'Errico FP. 2003 – fungi. II. A new generic concept. Diffusion and effectiveness of the ne- Sydowia 51, 89–113. matophagous fungus Hirsutella rhossi- Segers R, Butt TM, Carder JH, Keen JN, Kerry liensis in control of the cyst nematode BR, Peberdy JF. 2000 – The subtilisins of Heterodera daverti under field conditions. fungal pathogens of insects, nematodes Journal of Plant Pathology 85, 219–221. and plants: distribution and variation. Species Fungorum. 2011 – http://www.species Mycological Research 103, 395–402. fungorum.org/Names/SynSpecies.asp?Re Sharifi M, Ghorbanli M, Ebrahimzadeh H. cordID=296413 2007 – Improved growth of salinity- Stefanowicz AM, Niklinska M, Laskowski R. stressed soybean after inoculation with 2008 – Metals affect soil bacterial and salt pre-treated mycorrhizal fungi. Jour- fungal functional diversity differently. nal of Plant Physiology 164, 1144–1151. Environmental Toxicology and Chemis- Siegel BZ, Siegel SM. 1980 – Further studies try 27, 591–598. on the environmental capabilities of Stirling GR, Licastro KA, West LM, Smith LJ. fungi: interactions of salinity, ultraviolet 1998a – Development of comercially irradiation, and temperature in Peni- acceptable formulations of the nemato- cillium. Life Science Space Research 18, phagous fungus Verticillium chlamydo- 59–64. sporium. Biological Control 11, 217–223. Sikora RA. 1992 – Management of the Stirling GR, Smith LJ, Licastro KA, Eden LM. antagonistic potential in agricultural eco- 1998b – Control of root-knot nematode systems for the biological control of plant with formulations of the nematode- parasitic nematodes. Annual Review of trapping fungus Arthrobotrys dactyl- Phytopathology 30, 245–270. loides. Biological Control 11, 224–230. Sikora RA, Schaefer K, Dababat AA. 2007 – Su H, Hao YE, Mo MH, Zhang KQ. 2007 – Modes of action associated with micro- The ecology of nematode-trapping bially induced in planta suppression of hyphomycetes in cattle dung from three

23 plateau pastures. Veterinary Parasitology oligospora and Paecilomyces lilacinus. 144, 293–298. Agricultural Science Digest 27, 50–52. Subramanian CV. 1963 – Dactylella, Monacro- Thorn RG, Barron GL. 1984 – Carnivorous sporium and Dactylina. Journal of Indian mushrooms. Science 224, 76–78. Botany Societies 42, 291–300. Tikhonov VE, Lopez-Llorca LV, Salinas J, Subramanian CV. 1964 – Prefatory obser- Jansson HB. 2002 – Purification and vations on host-parasitic relationships on Characterization of Chitinases from the plant diseases. Indian Phytopathology Nematophagous Fungi Verticillium chla- Society Bulletin 2, 5–17. mydosporium and V. suchlasporium. Sun BD, Liu XZ. 2008 – Occurrence and Fungal Genetics and Biology 35, 67–78. diversity of insect-associated fungi in Tosi S, Annovazzi L, Tosi I, Iadarola P, Caretta natural soils in China. Applied Soil G. 2002 – Collagenase production in an Ecology 39, 100–108. antarctic strain of Arthrobotrys tortor Sun M, Liu X. 2006 – Carbon requirements of Jarowaja. Mycopathologia 153, 157–162. some nematophagous, entomopathogenic Tavela ADO, Araújo JV, Braga FR, Silva AR, and mycoparasitic hyphomycetes as fun- Carvalho RO, Araujo JM, Ferreira SR, gal biocontrol agents. Mycopathologia Carvalho GR. 2011 – Biological control 161, 295–305. of cyathostomin (Nematoda: Cyatho- Sunder A, Lysek G. 1988 – Quantitative inves- stominae) with nematophagous fungus tigations on nematode-trapping hypho- Monacrosporium thaumasium in tropical mycetes from woodland soils. FEMS southeastern Brazil. Veterinary Parasi- Microbiology Letters 53, 285–290. tology 175(1-2), 92–96. Swe A, Jeewon R, Hyde KD. 2008a – Nema- Tsui CKM, Hyde KD. 2004 – Biodiversity of tode-trapping fungi from mangrove habi- fungi on submerged wood in a stream tats. Cryptogamie Mycologie 29(4), 333– and its estuary in the Tai Ho Bay, Hong 354. Kong. Fungal Diversity 15, 205–220. Swe A, Jeewon R, Pointing SB, Hyde KD. Tsui CKM, Hyde KD, Hodgkiss IJ. 2000 – 2008b – Taxonomy and molecular phylo- Biodiversity of fungi on submerged wood geny of Arthrobotrys mangrovispora sp. in Hong Kong streams. Aquatic Micro- nov. a new marine nematode-trapping bial Ecology 21, 289–298. fungal species. Botanica Marina 51(4), Tunlid A, Jansson S. 1991 – Proteases and their 331–338. involvement in the infection and immo- Swe A, Jeewon R, Pointing SB, Hyde KD. bilization of nematodes by the nemato- 2009 – Diversity and abundance of phagous fungus Arthrobotrys oligospora. nematode-trapping fungi from decaying Applied and Environmental Microbio- litter in terrestrial, freshwater and man- logy 57, 2868–2872. grove habitats. Biodiversity & Conser- Tunlid A, Åhman J, Oliver RP. 1999 – Trans- vation 18(6), 1695–1714. formation of the nematode-trapping Taylor JW, Jacobson DJ, Kroken S, Kasuga T, fungus Arthrobotrys oligospora. FEMS Geiser DM, Hibbett DS, Fisher MC. Microbiology Letters 173, 111–116. 2000 – Phylogenetic species recognition Tunlid A, Jansson HB, Nordbring-Hertz B. and species concepts in fungi. Fungal 1992 – Fungal attachment to nematodes. Genetics and Biology 31, 21–32. Mycological Research 96, 401–412. Teng HJ, Lu LC, Wu YL, Fang JG. 2005 – Turnau K, Anielska T, Ryszka P, Gawronski S, Evaluation of various control agents Ostachowicz B, Jurkiewicz A. 2008 – against mosquito larvae in rice paddies in Establishment of arbuscular mycorrhizal Taiwan. Journal of vector ecology 30, plants originating from xerothermic 126. grasslands on heavy metal rich industrial Thakur NSA, Devi G. 2007 – Management of wastes, New solution for waste revege- Meloidogyne incognita attacking okra by tation. Plant and Soil 305, 267–280. nematophagous fungi, Arthrobotrys Van Oorschot CAN. 1985 – Taxonomy of the Dactylaria complex, V. A review of

24 Current Research in Environmental & Applied Mycology

Arthrobotrys and allied genera. Studies in Nematophagous Fungus Esteya ver- Mycology 26, 61–96. mincola. Current Microbiology 60, 387– Veenhuis M, Nordbring-Hertz B, Harder W. 392. 1985 – An electron-microscopical analy- Wang RB, Yang JK, Lin C, Zhang Y, Zhang sis of capture and initial stages of pene- KQ. 2006b – Purification and characte- tration of nematodes by Arthrobotrys rization of an extracellular serine pro- oligospora. Antonie Van Leeuwenhoek tease from the nematode-trapping fungus 51, 385–398. Dactylella shizishanna. Letters in Via S. 1999 – Reproductive isolation between Applied Microbiology 42, 589–594. sympatric races of pea aphids. I. gene Ward S. 1973 – Chemotaxis by the nematode flow restriction and habitat choice. Caenorhabditis elegans: Identification of Evolution 53, 1446–1457. attractants and analysis of the response Via S, Bouck AC, Skillman S. 2000 – Repro- by use of mutants. Proceedings of the ductive isolation between divergent races National Academy of Sciences, USA 70, of pea aphids on two hosts. II. Selection 817–821. against migrants and hyprids in the Webster J, Henrici A, Spooner B. 1998 – Orbi- parental environments. Evolution 54, lia fimicoloides sp. nov., the teleomorph 1626–1637. of Dactylella cf. oxyspora. Mycological Wakelin SA, Macdonald LM, Rogers SL, Research 102, 99–102. Gregg AL, Bolger TP, Baldock JA. Whipps JM, Lumsden RD. 2001 – Comercial 2008a – Habitat selective factors influen- use of fungi as plant disease biological cing the structural composition and func- control agents: status and prospects. In tional capacity of microbial communities Fungi as biocontrol agents progress, in agricultural soils. Soil Biology and problems and potential (eds TM Butt, Biochemistry 40, 803–813. CW Jackson, N Magan). CAB inter- Wakelin SA, Warren RA, Kong L, Harvey PR. national, New York, 9–22. 2008b – Management factors affecting Yang J, Li J, Liang L, Tian B, Zhang Y, Cheng size and structure of soil Fusarium C, Zhang KQ. 2007a – Cloning and communities under irrigated maize in characterization of an extracellular serine Australia. Applied Soil Ecology 39, 201– protease from the nematode-trapping 209. fungus Arthrobotrys conoides. Archives Waller PJ, Knox MR, Faedo M. 2001 – The of Microbiology 188, 167–174. potential of nematophagous fungi to con- Yang J, Liang L, Zhang Y, Li J, Zhang L, Ye trol the free-living stages of nematode F, Gan Z, Zhang KQ. 2007b – Purifi- parasites of sheep: Feeding and block cation and cloning of a novel serine studies with Duddingtonia flagrans. protease from the nematode-trapping Veterinary Parasitology 102, 321–330. fungus Dactylellina varietas and its Wang KH, Sipes BS, Schmitt DP. 2003 – potential roles in infection against nema- Enhancem ent of Rotylenchulus reni- todes. Applied Microbiology and Bio- formis suppressiveness by Crotalaria technology: 75, 557–565. juncea amendment in pineapple soils. Yang J, Tian B, Liang L, Zhang KQ. 2007c – Agriculture, Ecosystems & Environment Extracellular enzymes and the patho- 94, 197–203. genesis of nematophagous fungi. Applied Wang M, Yang J, Zhang KQ. 2006a – Charac- Microbiology and Biotechnology 75, 21– terization of an extracellular protease and 31. its cDNA from the nematode-trapping Yang Y, Liu XZ. 2006 – A new generic fungus Monacrosporium microsca- approach to the taxonomy of predatory phoides. Canadian Journal of Micro- anamorphic Orbiliaceae (Ascomycotina). biology 52, 130–139. Mycotaxon 97, 153–161. Wang CY, Wang Z, Fang ZM, Zhang DL, Gu Yu Z, Qiao M, Zhang Y, Baral HO, Zhang KQ. LJ, Liu L, Sung CK. 2010 – Attraction of 2007 – Orbilia vermiformis sp. nov. and Pinewood Nematode to Endoparasitic its anamorph. Mycotaxon 99, 271–278.

25 Zafar S, Ahmad I. 2005 – Fungal diversity of Zhao ML, H u ang JS, Mo MH, Zhang KQ. metal contaminated agricultural soils and 2005 – A potential virulence factor in vitro fungi-toxicity of heavy metals. involved in fungal pathogenicity: serine- Polution Research 24, 793–799. like protease activity of nematophagous Zhang J, Mo M, Deng J, Liu X, Bi T, Zhang fungus Clonostachys rosea. Fungal KQ. 2005 – Dactylella zhongdianensis Diversity 19, 217–234. sp. nov, a new predacious antagonist of Zhu ML, Mo MH, Xia ZY, Li YH, Yang SJ, Li nematodes. Mycotaxon 92, 289–294. TF, Zhang KQ. 2006 – Detection of two Zhang Y, Yu ZF, Baral HO, Qiao M, Zhang fungal biocontrol agents against root- KQ. 2007 – Pseudorbilia gen. nov. knot nematodes by RAPD markers. (Orbiliaceae) from Yunnan, China. Mycopathologia 161, 307–316. Fungal Diversity 26 I, 305–312. Zopf W. 1888 – Zur Kenntnis der Infektion- Zhang Y, Yu ZF, Qiao M, Zhang KQ. 2006 – skrankheiten niederer Thiere und A new species of Orbilia from China. Pflanzen. Nova Acadamy of Caes. Leop. Cryptogamie Mycologie 27, 289–294. German. Nat. Cur. 52, 314–376. Zhao LL, Wei W, Kang L, Sun JH. 2007 – Zucconi L, Ripa C, Selbmann L, Onofri S. Chemotaxis of the pinewood nematode, 2002 – Effects of UV on the spores of the Bursaphelenchus xylophilus, to volatiles fungal species Arthrobotrys oligospora associated with host pine, Pinus masso- and A. ferox. Polar Biology 25, 500–505. niana, and its vector Monochamus alter- Zuckerman BM, Jansson HB. 1984 – Nema- natus. Journal of Chemical Ecology 33, tode chemotaxis and possible mecha- 1207–1216. nisms of host/prey recognition. Annual Review of Phytopathology 22, 95–113.

26