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[edit] 'Predatory' fungi

Fungi can act as parasites and pathogens in a host of species from plants to animals however their relationship with soil nematodes and other 'prey' is unique. Over 200 species have been identified that have mechanisms facilitating identification, luring and ambush of prey [1]. These mechanisms are what characterize some fungal species as 'predatory' fungi. Typical fungal parasites and pathogens have endoparasitic mechanisms in which pathogenesis results from the germination of fungal spores dispersed upon host tissue [2]. In essence luring and ambush of food sources is not involved in endoparasitism. Trapping and digestion of prey is made possible by many different traps that differentiate from fungal hypha. Research on 'predatory' fungi dates back to 1888 and is ongoing today with research that may reveal further beneficial applications of 'predatory' fungi in agriculture, medicine, and pest-control.

[edit] Definitions

Long strands of fungal tissue that branch to promote growth of the fungus.
Collection of hyphae.
Conidia (conidium pl)
non-motile spore of a fungus in which are fromed from the process of mitosis
A specialized fungal hypha in which produce conidia
Are ectoparasites of rotifers and nematodes. The vegetative hyphae produce short lateral braches form knobs which trap their prey and fill them with parasite hyphae. [3]
18s rDNA (18s rRNA)
The S is for Svedberg units. One of the basic components of all eukaryotic organism and 18s rRNA is one of the genes most commonly used for phylogenetic experiments. 18S rDNA is the coding genes for 18S r RNA.
The level of toxic effect a substance has on a living cell.
Is a particle that is less than 100nm in size.
Nitrogen Cycle
A series of reactions where nitrogen travels from the atmosphere in the form of rain to the soil where it is metabolized by plants and bacteria. Nitrogen then returns to the atmosphere when organic material decays.
The growth or production of cells by multiplication of parts.
Attached directly by its base without a stalk or peduncle.

[edit] History

Arthrobotrys trapping a nematode as described by Dr. Wilhelm Zopf in 1888.
Arthrobotrys trapping a nematode as described by Dr. Wilhelm Zopf in 1888.[4]

The earliest known record of predatory fungi occurs in classical reports describing the observation of the capture and digestion of nematodes by the fungi Arthrobotrys oligospora, one of the most common predacious fungi. The A. oligospora was originally classified as a saprophyte in 1852, however, 20 years after its discovery, germinating spores were observed producing mycelium with curving hyphae forming a system of loops, the significance of which remained unknown at the time.[5] It was not until research preformed in 1888 by Dr. Wilhelm Zopf was the purpose of these loops discovered. Zopf grew cultures of A. oligospora, in the presence of nematodes and demonstrated that the nematode eelworms were caught by the loops, where the nematode remained until its death. He then observed how the fungi introduced absorptive hyphae into the body of the nematode and consume its carcass.

The discovery of predatory A. oligospora occurred at a time similar to that of another fungi of intrest, Dactylella ellipsospora. This fungi was first described in 1851 under the genus Menispora; it was later given the title Dactylella upon being discovered on decaying wood. The predatory effect of D. ellipsospora wasn't discovered until 1937 by Dr. Charles Drechsler. Publications by Drechsler describe D. ellipsospora and the formation of adhesive knobs along its hyphae used in the capture and digestion of nematodes.[5]

The next great discovery in predacious fungi did not occur until 1933, when Drechsler, over the course of several publications, described the discovery of never before seen predatory activity associated with nematode and amoeboid digestion. These articles were of the first to describe the capture of amoebae with the use of adhesive protuberances along the hyphae and the use of a single germ tube directly invading the host for digestion.[6] It was also at this time that it was noted how the organs of capture were generally absent in any predacious fungi grown on pure agar, in the absence of living nemas. However, upon addition of this food source, trapping loop growth was observed.[7] Thus giving the first recorded case of environmental stimuli giving rise to predatory function. Further publications describe Zoopagaceae, a family of predatory fungi, feeding mainly on amoebae and decaying organic matter. In 1937, Drechsler's research resulted in the detailed activity of A. oligospora, A. superba, D. candida and D. ellipsospora.[5]

[edit] Habitats

Environmental conditions which favour the ecological niche and successful growth of predatory fungi are typically areas where amoebae and nematode worms are most abundant as this is the most common host of this type of fungi. However, high host count in an area does not necessarily guarantee the presence of predatory fungi species. [8]

A few principal terrestrial habitats have been identified through literature. These environments include leaf mould, decaying wood, partly decayed plant remains, dung, and living bryophytes- all of which are found in soil.

  • Leaf Mold

Many fungi thrive in this environment, however it not the most prevalent condition for predatory fungi specifically, though some may still be found in such areas. [8]

  • Decaying wood

Decaying wood is one of the most dominant habitats for predatory fungi. Wood in advanced stages of the decaying process, is often rich in nematode species, thus substantially resonating with the life of predatory fungi and providing ideal host trapping conditions. [8]

  • Plant remains

Decaying plant remains, especially those leaves and stems significantly softened by the early stages of decay, are often rich in predatory fungi. [8]

  • Dung

Dung is also a typical environment in which predatory fungi thrive. It is important to note that as the dung ages, the organisms colonized within it change, and the oldest material usually contains the most variance in predatory fungi species. [8]

  • Living Bryophytes

Bryophytes appear to be the most prevalent and successful predatory fungi habitat. Mosses, especially when moist, are an optimal environment for large nematode worms and thus provide extremely favourable host trapping environments. [8]

Interestingly, some predatory fungi species can be found in aquatic habitats, although they are regarded as terrestrial. True aquatic forms such as Zoophagus insidians do exist however. [8]

[edit] Common Mechanisms of Predation

Types of traps:

[edit] Adhesive Traps

These multicellular traps contain electron dense bodies and adhesive surface polymers. This means the tight binding of fungus and the nematode is caused by interaction between sugars and other charged molecules on the cell surfaces. Trapping occurs when the nematode makes contact with the trap’s surface. [1]

Subtypes: [1]

  1. Adhesive network- Amongst the most common fungal traps. Hyphal branches form loops and these loops form a three-dimensional web which attract and entangle approaching nematodes. These loops typically have a diameter of 20um.
  2. Adhesive knob- It is hypothesized that ring and network traps evolved from adhesive knobs in orbiliaceous fungi (those belonging to the order Orbiliales). These traps are composed of a bulbous cell attached at the terminal end of a hyphal stalk. They are usually closely spaced along the hypha to maximize the chances of successfully trapping the nematode.
  3. Non-constricting ring- Always accompany adhesive knobs. These form from lateral branches which loop around forming three-celled rings that attach to a stalk.
  4. Adhesive column- A hyphal branch composed of a few inflated cells.

[edit] Constricting Rings

Similar to the non-constricting ring, this is a three-celled trap attracts nematodes searching for food through the ring. The unique feature of the constricting ring is that it actively captures the prey. When the nematode is sensed chemically or physically, the ring cells will inflate within seconds thus trapping the nematode along its length. This is the most sophisticated trapping mechanism. [1]

[edit] Nematode Trapping

Nematode trapping fungi are a common and clear demonstrations of fungal predation in action. Nematophagous or nematode-killing fungi have evolved traps along their hyphae which can secrete nematode-attracting chemicals and can be set-off when prey is detected. Specific species like Arthrobotrys oligospora can even increase or decrease the number of traps expressed on their hyphae when nematodes or chemicals secreted by them are detected. [14]

[edit] Post-trapping Digestion

When the nematode has become sufficiently bound to the adhesive layer or crushed by the constrictive ring, hypha produce a penetration peg which punctures the outer layer of the nematode. Infection bulbs full of digestive enzymes inflate within the nematode and erupt initiating absorptive nutrition. Absorptive nutrition involves the digestion of nutrients outside of the fungal cell followed by absorption of the products. These products fuel further hyphal growth and hypha can even begin to grow out of the dead nematode. [14]

[edit] Common Predatory Species

Listed below are some Nematophagus fungi and their methods of entrapment. Some fungi are capable of using multiple methods in order to ensnare their prey, while others are fairly specific in their approach. In almost all instances, the fungi will utilize an attraction mechanism in order to lure in their prey.

[edit] Arthrobotrys oligospora

One of the most common Predatory fungi, Arthrobotrys utilizies a three dimensional web in order to capture its prey[15] (See Illustration).
Three Dimesnional Web of Arthrobotrys.
Three Dimesnional Web of Arthrobotrys[16].
This three dimensional web will trap a nematode, while the fungi will proceed to lyse the cuticle of the nematode and penetrate with hyphae [15]. Interactions along the fungi’s web surface allows for the entrapment of the nematode. It has been shown that this part of the fungi contains lectin for which the nematode will bind.

[edit] Dactylaria candida

This species of fungi utilizes adhesive knobs paired with non constricting rings. The formation of this dual structure for entrapment involves the formation of an inflated cell along the route of the hyphae (Knob)[14] and the production of a three membered ring which has no inflation upon nematode presence. This type of trapping device is paired with an attraction molecule for the fungi along with lectins on the adhesive cell surface.
Adhesive Knob Method of Entrapment.
Adhesive Knob Method of Entrapment[17].

[edit] Arthrobotyrys dactyloides[18]

The contractile ring is formed via a three cell protrusion from the mycelium which loops around in order to form the termed ring. Arthroboytrys dactyloides will produce nematode attraction compounds, one of which have been identified as carbon dioxide[19]. Once the nematode has been lured to the constricting ring, A. dactyloides mechanically traps the Nematode by expansion of the cells in the ring, and is digested by release of ammonia [19](See Animation).
Contractile Ring Method of Entrapment Animation.
Contractile Ring Method of Entrapment Animation[16].

[edit] Carnivorous Mushrooms

25 species of carnivorous mushrooms have been discovered, and is hypothesized that probably all mushroom species from Hohenbuehelia capture nematodes with the use of adhesive knobs. Hohenbuehelia are nematode specific and consist of sticky knobs. They are strictly restricted to capturing nematodes as a form of their nitrogen source [20].

[edit] Notes on Predacity

It has been shown that the most effective fungi are the ones with the most motility in their environment, as predator prey interaction depends on frequency of interaction[21]. With that being said, density of the fungi and density of the prey are very important factors in affecting the effectiveness as highly dense redatores can limit the population in an area of the prey, and large populations of prey, limit substrate for fungi to grow[22].

[edit] Phylogenetics & Evolution

The majority of nematode trapping fungi is hyphomycetes, which belong within the Orbiliales group.

[edit] 18s rDNA

Phylogeny of nematode-trapping fungi used to be classified based on morphological characters of the conidia and conidiophores. They were divided into three genres: Arthrobotrys, Dactylella and Monacrosporium Subramanian.[23] Recently, based on 18s rDNA sequences indicated that, trapping devices offer more information than any other morphological structure in determining genera.

The idea of predatory nematode-trapping fungi evolved from non predatory fungi was first brought forward by Rubner (1996), and was concluded by Scholler et al (1999) through 18S data that predatory species did in fact originate from non predatory species within the genus Orbilia[23].

A study (Aheren et al, 1998) further analyzed 18s rDNA finding that species with constricting rings are monophyletic and are unique from species with other trapping devices and non predatory species in which suggested that the capability for fungi to catch nematodes have arisen twice, one being a lineage in which already contained constrictive rings and another in a lineage in which evolved into other trapping structures[23].

Adhesive knobs are considered to be a sister group of trapping rings and trapping networks because they were most closely related to the non predatory taxa Dactylella rhombospora and D. oxyspora. Some species with more than one trapping device show some insight into how trapping devices have evolved in nematode trapping fungi. The constricting rings show to be most effective method as the rings inflate in a short time to strangle nematodes. On the other hand, the knobs trap the nematodes only at one point making them easily able to escape[23]. Species with more than one trapping device is evidence into how trapping-devices evolved in nematode trapping fungi from knobs to networks and constricting rings.

Characters of nematode trapping fungi have been divided into four different genres:[23].

  1. Dectylellin- which are known for its staked adhesive knobs
  2. Gamylella- characterized by adhesive branches and unstalked knobs
  3. Arthrobotrys- characterized by adhesive networks
  4. Drechlerella- in which is characterized by constricting rings

[edit] Evolution

Phylogenetic tree describing the evolution of trapping organs in predatory fungi.  Trapping devices are drawn on the left. SSK, sessile adhesive knob; SK, stalked adhesive knob; AN, adhesive net; AC, adhesive column; NCR, nonconstricting ring; CR, constricting ring.
Phylogenetic tree describing the evolution of trapping organs in predatory fungi. Trapping devices are drawn on the left. SSK, sessile adhesive knob; SK, stalked adhesive knob; AN, adhesive net; AC, adhesive column; NCR, nonconstricting ring; CR, constricting ring.[24]

The differentiation of trapping organs among the major clades demonstrates a evolutionary path. Recent studies find carnivorous fungi with active trapping structures and fungi using more passive, adhesive trapping structures are derived from a common unknown ancestor. It is believed that the use of adhesive columns originally diverged from fungi utilizing sessile adhesive knobs. The formation of these knobs into a column would have resulted in an increased adhesive surface and predatory efficiency.[24]

Early fossils show the presence of predatory fungi using a unicellular ring (considered the lowest predatory efficiency) until its divergence into two lineages. One side of this divergence resulting in the formation of adhesive nets, likely by the proliferation of the unicellular ring into a network of rings. The other side of this divergence resulted in the formation of non-constricting rings paired with stalked adhesive knobs. It is likely that the single-celled rings gave rise to the three-celled rings, unicellular knobs and stalked adhesive knobs.[24] Furthermore, two likely hypothesis exist around the possible evolutionary relationship between fungi utilising stalked adhesive knobs alone, and those that have paired them with non-contractile rings.

  1. It is possible that the non-contractile rings were adapted by species using stalked knobs in order to increase predatory efficiency.[24]
  2. It is also possible that fungal species with both non-contractile rings and adhesive knobs diverged into only producing the knobs in order to limit the energy expenditure of producing the ring organs.[24]

[edit] Food Sources

The genus Zoophagus produces what was described by Howard Whistler from the University of Washington as “lethal lollipops.” The swollen ends of the fungi have a ball at the end (lollipop) in which attracts rotifers. These microscopic animals attach to the ends by their mouths and try to swallow the “lollipop” but, end up getting stuck. Once they become attached, the tip of the hyphae sprouts and colonizes the organism.[25]

Pleurotus ostreatus
Pleurotus ostreatus[26]

Like many organisms, fungi also need a source of protein in their diet. Protein can be a primary source for nitrogen in many fungi. Wood-decay fungus have the challenge of obtaining their source of nitrogen within nitrogen poor environments. They face the carbon/nitrogen ratio of 500:1[25]. There are known to be a substantial amount of fungi in which exhibit a Jekyll-Hyde type characteristic in which they can switch between being herbivorous and carnivorous as it pertains to their needs.

The oyster mushroom (Pleurotus ostreatus) and the wood blewit(Lepista nuda) have been found to exhibit this sort of behavior. The oyster mushroom produces secretory cells that in which contain a droplet of fluid. Once the nematode comes in contact with the fluid, the toxins within the fluid cause structural damage and immobilizes is it. Once the nematode has become completely paralyzed, the hypha of the fungus will grow into the nematode’s mouth and begin to digest the remaining living tissue[25].

[edit] Benefits and Practical Applications

[edit] Potential Treatment for Nematode Parasites in Livestock

Parasites are a common problem found in many livestock farm animals, including cows, pigs, goats, horses and sheep. These animals are susceptible to infection due to grazing in contaminated pastures. The parasites are found in the soil and the animal ingests the larvae while eating, causing the lifecycle to continue in the ruminant of the host.

These parasites, specifically helminth nematode, interfere with digestion and absorption, therefore depleting the nutrients available to the animal. The result is illness, stunted growth and poor quality yields for farmers. There is a need to control parasitic nematodes to prevent economical loss, however, the practice of using anthelmintics has caused resistance in some populations. Thus a need to find alternatives has gained attention for the potential use of biological controls. There are specific types of fungi that are known for their predatory behaviors with nematodes. This variety of species uses a predatory style of attack such as adhesive knobs, networks, rings etc. to capture nematodes for their main source of nutrients[28]. These unique characteristics lead to studies involving Duddingtonia flagrans a known nematophagous fungi and the parasite Oesophagostomum .

This parasite is a common nematode that is found worldwide and in some instances the prevalence rate has reached 50% of farms [31]. Duddingtonia flagrans has shown to be most promising with potential treatment applications due to its ability to survive in the GI tract of pigs. In actual research trials involving administration of the fungus by feeding grazing animals fungal spores for 3-4 months resulted in a prevented build up of infective larvae on the pasture [32]. Other studies have found that sheep feed a supplement of D. flagrans chlamydospores had lower egg counts and improved weight gains compared to untreated animals [33]. Other potential fungi for biological control of nematode parasites include Candelabrella musiformis and 'Monacrosporium thaumasium[34] Antibiotics consist of using biological properties of one species against another. The use of predatory fungi to eliminate or reduce the infection of parasitic worms in farm animals has shown to be a very promising, which may also translate into potential for treatment on humans in the future. live

[edit] 'Practical Applications Continue: Use of Predatory Fungi for Root-Knot Disease

Environment and human safety factors have prompted the discovery of alternative controls for the agricultural world. Currently, there is concern regarding chemical residue on food and drug use on animals and the consequence of these actions. Moreover, resistance to current applications and price of these pesticides, especially in third world countries is also a prevalent issue. [35] As mentioned above in Predatory Fungi in Livestock the use of fungi as a biological control for combating nematode parasites has shown great promise. [36] Another nematode that has sparked the inquiry of predatory fungi as a biological control is known as Meloidogyne graminicola. M. graminicola can devastate wheat crops with a disease known as root knot

However, the trapping and killing mechanism of the predacious fungi known as Dactylaria brochopaga might be an important application at combating M. graminicola and saving agricultural crops. D. brochopaga kills parasitic nematodes using the constricting ring mechanism discussed in Common Mechanisms of Predation. D. brochopaga can be commonly found in agricultural soil. Therefore, since D. brochopaga is commonly found in agricultural soil, this predatory fungi might be easily inserted to soil infested with root knot disease, which further emphasizes its possible use and importance as a biological control [37] According to a study by Kumar and Singh 5 different isolates of D. brochopaga from sources such as soil, leafs and decaying roots were used in a laboratory setting in order to observe the abilities of D. brochopaga as a biological control of root knot disease. The study revealed that in just 48 hours the inoculated parasitic nematodes were captured by the constricting ring mechanism of the predatory fungi. All 5 isolates were effective because parasitic nematodes were captured and wheat plant growth increased, however undiluted spore suspensions appeared to produce greater results[38]. Consequently, the following study reveals the important implications of the predacious fungi D. brcohopaga and its use as natural biological control for root knot disease.

[edit] Modern Day Lab Work

The notion that predatory fungi have both the ability to trap and ability to digest their prey has been well understood for years. One of the first recognized methods used to trap prey was the ability of a hyphomycete to capture nematodes with a constricting ring[39].

Despite scientists and researchers having knowledge of this ability to trap and the type of traps used, the origins and divergence of how predatory fungi developed these specific trapping mechanisms was not well known. Looking at the ribosomal DNA in the internal transcribed region, two distinct lineages were found to have evolved resulting in distinct trapping mechanism[1]. The resulting two mechanisms developed were constricting rings and an adhesive trap. These two traps developed from the fungi’s need to adapt to its present environment[1].

[edit] Nitrogen Cycle

The Nitrogen Cycle
The Nitrogen Cycle[40]

Research on this topic at Brock University has led to the discovery of the role in the nitrogen cycle for plants in the ecosystem that some predatory fungi play. The research group would inject insects with Nitrogen 15 which is a rare element not abundantly found in nature, and let the fungi Metarhizium spp. attack and kill the insects[41]. The fungi were then placed near the plant roots of a haricot bean (phaseolus vulgaris) and switchgrass (panicum virgatum) and set aside for a couple weeks. After 14 days, results showed that 30% of the nitrogen contained in both the plants was Nitrogen 15 which had come from the fungi. After 28 days, the level of Nitrogen 15 in the haricot bean had decreased to 14% but in the switchgrass that percentage had risen to 48% [41]. The results showed that predatory fungi have a role in the survival of plant life by helping the plant absorb nitrogen, which is then used by the plant to make amino acids it needs to survive.

[edit] Medicine

A Nanoparticle Delivering A Drug to a Cell
A Nanoparticle Delivering A Drug to a Cell[42]

A new technique that is being tested in cancer treatments involves the use of the predatory fungi A. oligospora as this fungus was observed to produce and secrete nanoparticles. Nanoparticles are used in cancer research as they have the ability to readily pass through cell membranes[43]. An in vitro study showed that fungal nanoparticles have the ability to stimulate white blood cells in the immune system. In a separate study the fungal nanoparticles had slight cytotoxicity towards human lung cancer cells[43]. One method researchers suggest is to combine the nanoparticles with another known drug used in treating cancer patients to help increase the lethal potential of the nanoparticles as the study showed they had a moderate lethality[43]. This research suggests fungal nanoparticles could potentially have a big role in chemotherapy, drug delivery or immune regulation but further research and tests will need to be done to see the full potential of this new revolutionary technique.

[edit] Ecological

[edit] Regulatory Forces in Terrestrial Ecosystems

The Role of Fungi in the Phosphorus Cycle.
The Role of Fungi in the Phosphorus Cycle[44].
Nematode-Killing Fungi and their Role within the Soil Food Web.
Nematode-Killing Fungi and their Role within the Soil Food Web[45].

Within terrestrial ecosystems, fungi are among the most important decomposers[46]. In fact, they play such an essential role in the decomposition of carbon and nitrogen that their absence would cause serious effects on both the carbon and nitrogen cycles[46]. However, it should be noted that the role of fungi is not limited to these two cycles[46]. They are also imperative forces in the decomposition of phosphorus, among other elements[46]. These decomposers, also known as saprotrophs, recycle these elements so that they can be made readily available to re-enter the metabolic pathways of other organisms[47]. In this way, predatory fungi are also important agents within the food web [47].

This Predatory Oyster Mushroom, Pleurotus ostreatus, Re-Cycles Nutrients Through the Process of Decomposition.
This Predatory Oyster Mushroom, Pleurotus ostreatus, Re-Cycles Nutrients Through the Process of Decomposition[48].

The process of decomposition begins when a fungus comes in contact with decaying organic matter[47]. These organic substrates include various species of plants and animals[47]. Once it has infected a host, the fungus begins breaking down tissue through the release of various types of enzymes[47]. Critical building blocks, such as carbon and nitrogen, are then re-circulated into the ecosystem once the organic matter has been exposed to these catalysts[47]. The speed at which this process occurs is called the rate of decomposition [49]. According to scientific observation and testing, this rate is affected by variables such as temperature, moisture, availability of oxygen, and so on[49]. For example, since fungi require oxygen for growth, decomposition occurs much faster in areas that have an abundance of oxygen than areas that have relatively little oxygen [49].

[edit] The Carbon Cycle

The Carbon Cycle
The Carbon Cycle[50]
Predatory fungi are a crucial aspect of the carbon cycle. Fungi, including large quantities of predatory fungi, outweigh all other biomass in forest soils and organic material. [20]. Fungi play the major role of decay organisms in the forest environment, as well in the mycorrhizal which provide the tree with essential minerals and organic carbon compounds.[20] During this process of decay, biodegradation of cellulose and lignin occurs, causing the return of hundreds of billions of tons of CO2 into the atmosphere rendering these forest dwelling fungi as major biological contributors to the terrestrial carbon cycle.[20] Thus because each tree in a forest is associated with thousands of kilometres of hyphae, ultimately, the photosynthetic processes of the entire forest are mediated almost completely by fungi- that in fact account for 90% of the biomass in forest soils. [20].

[edit] Notes and References

  1. 1.0 1.1 1.2 1.3 1.4 1.5 Yang, Y., Yang, E., An, Z., & Liu, X. (2007). Evolution of nematode-trapping cells of predatory fungi of the orbiliaceae based on evidence from rrna-encoding dna and multiprotein sequences. PNAS, 104(20), 8379-8384.
  2. Burdass, D. (2009). Nematode-killing fungi. Microbiology today. 8:202-205.
  3. Zoophagus
  5. 5.0 5.1 5.2 Doddington, C. "Fungi that attack microscopic animals." Botanical Review. 21.1 (1955): 377-439.
  6. Drechsler, C. "Morphological features of some fungi capturing and killing amoebae." Journal of the Washington Academy of Sciences . 28.4 (1933): 200-202.
  7. Drechsler, C. "Several more fungi that prey on nematodes."Journal of the Washington Academy of Sciences . 28.7 (1933): 355-357.
  8. 8.0 8.1 8.2 8.3 8.4 8.5 8.6 Duddington, C. L. (1951). The ecology of predacious fungi: I. Preliminary survey. Transactions of the British Mycological Society, 34(3), 322-331.
  14. 14.0 14.1 14.2 Moore, D., Robson, G. D., & Trinci, A. P. (2011). 21st Century Guidebook to Fungi with CD. Cambridge University Press.
  15. 15.0 15.1 Nordbring-Hertz, B., & Mattiasson, B. (1979). Action of a nematode-trapping fungus shows lectin-mediated host–microorganism interaction.
  16. 16.0 16.1 Jacobs, Phillip.[1] Retrieved on March 18, 2013
  17. n.a. [2]. Retrieved on March 19, 2013
  18. Jansson, H. B., & Nordbring-Hertz, B. (1979). Attraction of nematodes to living mycelium of nematophagous fungi. Journal of General Microbiology, 112(1), 89-93.
  19. 19.0 19.1 Balan, J., & Gerber, N. N. (1972). Attraction and killing of the nematode Panagrellus redivivus by the predaceous fungus Arthrobotrys dactyloides.Nematologica, 18(2), 163-173.
  20. 20.0 20.1 20.2 20.3 20.4 Barron, G. L. 2003. Predatory fungi, wood decay, and the carbon cycle. Biodiversity, Volume 4: 3-9
  21. Jansson, H. B. (1982). Predacity by nematophagous fungi and its relation to the attraction of nematodes. Microbial Ecology, 8(3), 233-240.
  22. Jansson, H. B., & Nordbring-Hertz, B. (1980). Interactions between nematophagous fungi and plant-parasitic nematodes: attraction, induction of trap formation and capture. Nematologica, 26(4), 383-389.
  23. 23.0 23.1 23.2 23.3 23.4 Li, Yan et al. (2005). Phylogenetics and evolution of nematode-trapping fungi (orbiliales) estimated from nuclear and protein coding gens. Mycologia issue 97, vol:5 pp1034-1046
  24. 24.0 24.1 24.2 24.3 24.4 Yang, E, L Xu, Y Yang, X Zhang, M Xiang, C Wang, Z An, and X Liu. "Origin and evolution of carnivorism in the Ascomycota (fungi)." PNAS. 109.27 (2011): 10960-10965. doi: 10.1073/pnas.1120915109
  25. 25.0 25.1 25.2 Barron, George (1992). Jekyll-Hyde mushrooms. Natural History. Vol. 101, Issue 3.
  26. Michael Wood & Fred Stevens (1996-2010) retrieved from:
  28. De,S., Sanyal, P.K., (2009). Biological control of heminth parasites by predatory fungi. Department of Parasitology. 31: 1-8.
  31. Ferreira, S.R., Araujo, J.V., Braga, F.R., Araujo, J.M., Fernandes, F.M. (2011). In vitro predatory activity of nematophagous fungi Duddingtonia flagranson infective larvae of Oesphagostomum spp. after passing through gastrointestinal tract of pigs. Trop Anim Health Prod. 43: 1589-1593
  32. De,S., Sanyal, P.K., (2009). Biological control of heminth parasites by predatory fungi. Department of Parasitology. 31: 1-8.
  33. De,S., Sanyal, P.K., (2009). Biological control of heminth parasites by predatory fungi. Department of Parasitology. 31: 1-8
  34. Assis, R.C.L., Luns, F.D., Araujo, J.V., Braga., F.R., Assis, R.L., Marcelino, J.L., Freitas, P.C., Andrade, M.A.S.(2013). Comparison between the action of nematode predatory fungi Duddingtonia flagrans and Monacrosporium thaumasium in the biological control of bovine gastrointestinal nematodiasis in tropical southeastern brazil. Veterinary Paristology. 193:134-140
  35. De, S. and Sanyal. (2009). Biological Control of Helminth Parasites by Predatory Fungi. VetScam Vol 4 No 1
  36. Kumar, N. and Singh, P. (2011). Use of Dactylaria brochopaga, a Predacious Fungus, for Managing Root-Knot Disease of Wheat Caused by Meloidogyne graminicola. Mycobiology 39 (2) pages 113-117
  37. Kumar, N. and Singh, P. (2011). Use of Dactylaria brochopaga, a Predacious Fungus, for Managing Root-Knot Disease of Wheat Caused by Meloidogyne graminicola. Mycobiology 39 (2) pages 113-117
  38. Kumar, N. and Singh, P. (2011). Use of Dactylaria brochopaga, a Predacious Fungus, for Managing Root-Knot Disease of Wheat Caused by Meloidogyne graminicola. Mycobiology 39 (2) pages 113-117
  39. Duddington, C. L. (1955). Notes on the technique of handling predacious fungi. British Mycological Society, 38(2), 97-103.
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