Skip to main content
SpringerLink
Log in

Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Several studies have been conducted using fungi in the biological control of domestic animals and humans. In this respect, a large amount of research has been undertaken to understand the particularities of each fungus used. These fungi have been demonstrated to act on all classes of helminthes. Therefore, they should not only be called nematophagous but also helmintophagous. Evidence of enzymatic action has also revealed their mechanism of action, as well as potential metabolites that could be synthesized as bioactive molecules. Cultural barriers to the use of fungi should be broken down, since the impact on the environment is minimal. In this context, much is already known about the mechanism of interaction of these organisms with their ‘targets’. Recent research has pointed to the search for substances derived from nematophagous fungi that have demonstrated their ovicidal and/or larvicidal activity, thus being a global premise to be studied further. Crude extracts derived from nematophagous fungi of predator and ovicidal groups reduce the amount of larvae of gastrointestinal nematodes and prevent the hatching of their eggs, since they have been demonstrated to act with extracellular proteases and other enzymes. Furthermore, the activity of these enzymes has begun to be explored regarding their possible interaction with the exoskeleton of arthropods, which could emerge as an alternative method of tick control. Finally, it should be clear that nematophagous fungi in general are ‘old friends’ that are ready to the ‘fight with our old enemies’, the gastrointestinal helminth parasites harmful to human and animal health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alves PH, Araújo JV, Guimarães MP, Assis RCL, Sarti P, Campos AK (2003) Aplicação de formulação do fungo predador de nematóides Monacrosporium thaumasium (Drechsler, 1937) no controle de nematóides de bovinos. Arq Bras Med Vet Zootec 55:568–573

    Google Scholar 

  • Araújo JV, Guimarães MP (2002a) Acão do fungo predador de nematóides Monacrosporium thaumasium sobre Rhabditis spp. Cienc Anim 12:129–132

    Google Scholar 

  • Araújo JV, Guimarães MP (2002b) Acão do fungo predador de nematóides Arthrobotrys conoides sobre larvas infectantes de Cooperia punctata. Rev Bras Ciênc Vet 9:5–7

    Google Scholar 

  • Araújo JV, Maia AS (1992) Controle de larvas infectantes de Haemonchus placei por fungos predadores da espécie Monacrosporium ellypsosporum em condicoes de laboratorio. Arq Bras Med Vet Zootec 44:521–526

    Google Scholar 

  • Araújo JV, Maia AS (1993) Antagonistic effect of predacious fungi Arthrobotrys on infective Haemonchus placei larvae. J Helminthol 67:136–138

    PubMed  Google Scholar 

  • Araújo JV, Salcedo PHJ (1995) Initial interaction between Haemonchus placei infective larvae and different Arthrobotrys isolates. Arq Bras Med Vet Zootec 47:733–738

    Google Scholar 

  • Araújo JV, Santos MA, Ferraz S, Maia AS (1994) Biological control in vitro of infective Haemonchus placei larvae by predacious fungi Arthrobotrys musiformis. Arq Bras Med Vet Zootec 46:197–204

    Google Scholar 

  • Araújo JV, Santos MA, Ferraz S (1995) Efeito ovicida de fungos nematófagos sobre ovos embrionados de Toxocara canis. Arq Bras Med Vet Zootec 47:37–42

    Google Scholar 

  • Araújo JV, Azevedo MHFP, Neto A (1996) Screening of parasitic nematode-trapping fungi Arthrobotrys to pass through the gastrointestinal tract of calves. Arq Bras Med Vet Zootec 48:543–552

    Google Scholar 

  • Araújo JV, Gomes APS, Guimarães MP (1998) Biological control of bovine gastrointestinal nematode parasites in southern Brazil by nematode-trapping fungus Arthrobotrys robusta. Rev Bras Parasitol Vet 7:117–122

    Google Scholar 

  • Araújo JV, Stephano MA, Sampaio WM (1999) Passage of nematode-trapping fungi through the gastrointestinal tract of calves. Vet Arh 69:69–78

    Google Scholar 

  • Araújo JV, Sampaio WM, Vasconcelos RS, Campos AK (2000) Effects of different temperatures and mineral salt on pellets of Monacrosporium thaumasium—a nematode-trapping fungus. Vet Arh 80:181–190

    Google Scholar 

  • Araújo JV, Campos AK, Vieira-Bressan MCR (2001) Efeito antagonista de fungos predadores do gênero Arthrobotrys sobre larvas infectantes de Oesophagostomum radiatum, Cooperia punctata e Haemonchus placei. Revista Brasileira de Ciência Veterinária 8:81–84

    Google Scholar 

  • Araújo JV, Ramos M, Araujo EF, Loures FH, Alves PH (2003) Diversidade genética de cepas do fungo Arthrobotrys spp. predador de nematóides por RAPD e PCR-RFLP do rDNA. Rev Bras Ciênc Vet 10:170–174

    Google Scholar 

  • Araújo JV, Mota MA, Campos AK (2004a) Controle biológico de helmintos parasitos de animais por fungos nematófagos. Revista Brasileira de Parasitologia Veterinária 13:165–170

    Google Scholar 

  • Araújo JV, Guimarães MP, Campos AK, Sá NC, Sarti P, Assis RCL (2004b) Control of bovine gastrointestinal nematode parasites using pellets of the nematode-trapping fungus Monacrosporium thaumasium. Ciênc Rural 34:457–463

    Google Scholar 

  • Araújo JV, Assis RCL, Campos AK, Mota MA (2006) Efeito antagônico de fungos predadores dos gêneros Monacrosporium, Arthrobotrys e Duddingtonia sobre larvas infectantes de Cooperia sp. e Oesophagostomum sp. Arq Bras Med Vet Zootec 58:373–380

    Google Scholar 

  • Araújo JV, Rodrigues MLA, Silva WW, Vieira LS (2007) Controle biológico de nematóides gastrintestinais de caprinos em clima semi-árido pelo fungo Monacrosporium thaumasium. Pesq Agrop Brasileira 42:1177–1181

    Google Scholar 

  • Araújo JV, Braga FR, Milani JA, Silva AS, Tavela AO (2008) In vitro evaluation of the effect of the nematophagous fungi Duddingtonia flagrans, Monacrosporium sinense and Pochonia chlamydosporia on Ascaris suum eggs. Parasitol Res 102:787–790

    PubMed  Google Scholar 

  • Araujo JM, Araújo JV, Braga FR, Carvalho RO, Ferreira SR (2009) Activity of the nematophagous fungi Pochonia chlamydosporia, Duddingtonia flagrans and Monacrosporium thaumasium on egg capsules of Dipylidium caninum. Vet Parasitol 166:86–89

    PubMed  Google Scholar 

  • Araujo JM, Braga FR, Araújo JV, Soares FEF, Geniêr HLA (2010) Biological control of Taenia saginata eggs. Helminthology 47:189–192

    Google Scholar 

  • Araujo JM, Araújo JV, Braga FR, Soares FEF, Ferreira SR, Tavela AO, Frassy LN, Alves CDF, Carvalho GR (2012) Control of Strongyloides westeri by nematophagous fungi after passage through the gastrointestinal tract of donkeys. Rev Bras Parasitol 21:157–160

    Google Scholar 

  • Araujo JM, Araújo JV, Braga FR, Ferreira SR, Tavela AO (2013) Predatory activity of chlamydospores of the fungus Pochonia chlamydosporia on Toxocara canis eggs under laboratory conditions. Rev Bras Parasitol Vet 22:171–174

    PubMed  Google Scholar 

  • Arias MS, Suárez J, Cazapal-Monteiro CF, Francisco I, López-Arellano ME, Piñeiro P, Suárez JL, Sánchez-Andrade R, Mendoza de Gives P, Paz-Silva A (2013) Trematodes enhance the development of the nematode-trapping fungus Arthrobotrys (Duddingtonia) flagrans. Fungal Biol 117:540–544

    PubMed  Google Scholar 

  • Assis RCL, Araújo JV (2003) Avaliação da viabilidade de duas espécies de fungos predadores do gênero Monacrosporium sobre ciatostomíneos após a passagem pelo trato gastrintestinal de equinos em formulação de alginato de sódio. Rev Bras Parasitol Vet 12:109–113

    Google Scholar 

  • Assis RCL, Araújo JV, Gandra JR, Campos AK (2005) Avaliação de fungos predadores de nematóides do gênero Monacrosporium sobre larvas infectantes de Haemonchus contortus de caprinos. Rev Bras Ciênc Vet 12:42–45

    Google Scholar 

  • Assis RCL, Araújo JV, Luns FD, Braga FR (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. Vet Parasitol 193:134–140

    CAS  PubMed  Google Scholar 

  • Barron GL (1977) The nematode-destroying fungi. Topics in Mycobiology, No. 1. Canadian Biological Publications, Guelph, Canada, 140 pp

    Google Scholar 

  • Barron GL (2003) Predatory fungi, wood decay, and the carbon cycle. Biodivers Canberra 4:3–9

    Google Scholar 

  • Braga FR, Araújo JV, Campos AK, Carvalho RO, Silva AR, Tavela AO (2007) Observação in vitro da ação dos isolados fúngicos Duddingtonia flagrans, Monacrosporium thaumasium e Verticillium chlamydosporium sobre ovos de Ascaris lumbricoides (Lineu, 1758). Rev Soc Bras Med Trop 40:356–358

    PubMed  Google Scholar 

  • Braga FR, Araújo JV, Araujo JM, Carvalho RO, Silva AR (2008a) Efeito do fungo Paecilomyces lilacinus sobre ovos de Taenia saginata. Rev Soc Bras Med Trop 41:686–688

    PubMed  Google Scholar 

  • Braga FR, Araújo JV, Campos AK, Araujo JM, Silva AS, Carvalho RO, Tavela AO (2008b) In vitro evaluation of the action of the nematophagous fungi Duddingtonia flagrans, Monacrosporium sinense and Pochonia chlamydosporia on Fasciola hepatica eggs. World J Microbiol Biotechnol 24:1559–1564

    Google Scholar 

  • Braga FR, Araújo JV, Campos AK, Silva AR, Araujo JM, Carvalho RO, Correa DN, Pereira CAJ (2008c) In vitro evaluation of the effect of the nematophagous fungi Duddingtonia flagrans, Monacrosporium sinense and Pochonia chlamydosporia on Schistosoma mansoni eggs. World J Microbiol Biotechnol 24:2713–2716

    Google Scholar 

  • Braga FR, Araújo JV, Carvalho RO, Silva AR, Araujo JM, Tavela AO (2008d) Observação in vitro dos fungos nematófagos Duddingtonia flagrans, Monacrosporium thaumasium e Pochonia chamidosporia sobre ovos de Eurytrema coelomaticum. Parasitol Latinoam 63:40–45

    Google Scholar 

  • Braga FR, Araújo JV, Milani JA, Carvalho RO, Silva AR, Campos AK, Tavela AO (2008e) Ovicidal activity of Paecilomyces lilacinus on Moniezia sp. eggs. J Helminthol 10:1–3

    Google Scholar 

  • Braga FR, Araújo JV, Araujo JM, Silva AR, Carvalho RO, Campos AK (2009a) Avaliação in vitro do fungo predador de nematoides Duddingtonia flagrans sobre larvas infectantes de ciatostomíneos de equinos (Nematoda: Cyathostominae). Rev Bras Parasitol Vet 18:83–85

    PubMed  Google Scholar 

  • Braga FR, Araújo JV, Carvalho RO, Silva AR, Araujo JM, Tavela AO, Costa PRS, Campos AK (2009b) Ovicidal effect of nematophagous fungi on Taenia taeniaeformis eggs. World J Microbiol Biotechnol 25:533–535

    Google Scholar 

  • Braga FR, Araújo JV, Silva AR, Araujo JM, Carvalho RO, Tavela AO, Campos AK, Carvalho GR (2009c) Biological control of horse cyathostomin (Nematoda: Cyathostominae) using the nematophagous fungus Duddingtonia flagrans in tropical southeastern Brazil. Vet Parasitol 163:335–340

    PubMed  Google Scholar 

  • Braga FR, Carvalho RO, Araujo JM, Silva AR, Araujo JV, Lima WS, Tavela AO, Ferreira SR (2009d) Predatory activity of the fungi Duddingtonia flagrans, Monacrosporium thaumasium, Monacrosporium sinense and Arthrobotrys robusta on Angiostrongylus vasorum first stage larvae. J Helminthol 83:303–308

    CAS  PubMed  Google Scholar 

  • Braga FR, Silva AR, Araujo JM, Ferreira SR, Araújo JV, Frassy LN (2009e) Ação ovicida do fungo Pochonia chlamydosporia sobre ovos de Enterobius vermicularis. Rev Inst Adolfo Lutz (Impresso) 68:152–155

    Google Scholar 

  • Braga FR, Ferreira SR, Araújo JV, Araujo JM, Silva AR, Carvalho RO, Campos AK, Freitas LG (2010a) Predatory activity of Pochonia chlamydosporia fungus on Toxocara (syn. Neoascaris) vitulorum eggs. Trop Anim Health Prod 42:309–314

    PubMed  Google Scholar 

  • Braga FR, Silva AR, Araujo JM, Carvalho RO, Araújo JV, Frassy LN (2010b) Atividade predatória dos fungos nematófagos Duddingtonia flagrans, Monacrosporium thaumasium e Artrobotrys robusta sobre larvas infectantes de Strongyloides stercoralis. Rev Soc Bras Med Trop 43:588–590

    PubMed  Google Scholar 

  • Braga FR, Araújo JV, Silva ARE, Araujo JM, Carvalho RO, Campos AK, Tavela AO, Ferreira SR, Frassy LN, Alves CDF (2010c) Duddingtonia flagrans, Monacrosporium thaumasium and Pochonia chlamydosporia as a possible biological control agents of Oxyuris equi and Austroxyuris finlaysoni. J Helminthol 84:21–25

    CAS  PubMed  Google Scholar 

  • Braga FR, Silva AR, Carvalho RO, Araújo JV, Guimarães PHG, Fujiwara RT, Frassy LN (2010d) In vitro predatory activity of the fungi Duddingtonia flagrans, Monacrosporium thaumasium, Monacrosporium sinense and Arthrobotrys robusta on Ancylostoma ceylanicum third stage larvae. Vet Microbiol 146:183–186

    PubMed  Google Scholar 

  • Braga FR, Araújo JV, Araujo JM, Tavela AO, Ferreira SR, Soares FEF, Benjamin LA, Frassy LN (2011a) Influence of the preservation period in silica-gel on the predatory activity of the isolates of Duddingtonia flagrans on infective larvae of cyathostomins (Nematoda: Cyathostominae). Exp Parasitol 128:460–463

    PubMed  Google Scholar 

  • Braga FR, Araujo JM, Silva AR, Araújo JV, Carvalho RO, Soares FEF, Queiroz JH, Geniêr HLA (2011b) Ovicidal action of a crude enzymatic extract of fungus Pochonia chlamydosporia against Ancylostoma sp eggs. Rev Soc Bras Med Trop 44:116–118

    PubMed  Google Scholar 

  • Braga FR, Araujo JM, Silva AR, Araújo JV, Carvalho RO, Tavela AO, Silva ME, Fernandes FM, Melo AL (2011c) Destruição de larvas infectantes de Strongyloides venezuelensis pelos fungos Duddingtonia flagrans, Arthrobotrys robusta e Monacrosporium sinense. Rev Soc Bras Med Trop 44:389–391

    PubMed  Google Scholar 

  • Braga FR, Silva AR, Carvalho RO, Araújo JV, Pinto PSA (2011d) Ovicidal activity of different concentrations of Pochonia chlamydosporia chlamydospores on Taenia taeniaeformis eggs. J Helminthol 85:7–11

    CAS  PubMed  Google Scholar 

  • Braga FR, Araújo JV, Soares FEF, Araujo JM, Geniêr HLA, Silva AR, Carvalho RO, Queiroz JH, Ferreira SR (2011e) Optimizing protease production from an isolate of the nematophagous fungus Duddingtonia flagrans using response surface methodology and its larvicidal activity on horse cyathostomin. J Helminthol 85:164–170

    CAS  Google Scholar 

  • Braga FR, Araújo JV, Soares FEF, Araujo JM, Ferreira SR, Queiroz JH (2012a) Use of statistical tools in the study of the conditions of predation of Duddingtonia flagrans versus Panagrellus sp. Biochem Sci Technol 22:559–565

    Google Scholar 

  • Braga FR, Araújo JV, Soares FEF, Tavela AO, Araujo JM, Carvalho RO, Fernandes FM, Queiroz JH (2012b) Enzymatic analysis and in vitro ovicidal effect of Pochonia chlamydosporia and Paecilomyces lilacinus on Oxyuris equi eggs of horses. Biochem Sci Technol 22:685–696

    Google Scholar 

  • Braga FR, Araujo JM, Araújo JV, Soares FEF, Tavela AO, Frassy LN, Lima WS, Mozer LR (2013a) In vitro predatory activity of conidia of fungal isolates of the Duddingtonia flagrans on Angiostrongylus vasorum first-stage larvae. Rev Soc Bras Med Trop 46:108–110

    PubMed  Google Scholar 

  • Braga FR, Araújo JV, Tavela AO, Vilela VLR, Soares FEF, Araujo JM, Queiroz LM, Silveira WF, Feitosa TF, Dantas ES, Athayde ACR (2013b) First report of the interaction of nematophagous fungi on Libyostrongylus douglassii (Nematoda: Trichostrongilidae) of ostrich. Rev Bras Parasitol Vet 22:147–151

    PubMed  Google Scholar 

  • Campos AK, Araújo JV, Assis RCL, Gandra JR, Guimarães MP (2007) Viabilidade de formulação peletizada do fungo nematófago Monacrosporium sinense, no controle biológico de nematóides parasitos gastrintestinais de bezerros. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 59:14–20

    Google Scholar 

  • Campos AK, Araújo JV, Guimarães MP (2008) Interaction between the nematophagous fungus Duddingtonia flagrans and infective larvae of Haemonchus contortus (Nematoda: Trichostrongyloidea). J Helminthol 82:337–341

    CAS  PubMed  Google Scholar 

  • Campos AK, Araújo JV, Guimarães MP, Dias AS (2009) Resistance of different fungal structures of Duddingtonia flagrans to the digestive process and predatory ability on larvae of Haemonchus contortus and Strongyloides papillosus in goat feces. Parasitol Res 105: 913–919

  • Carvalho RO, Araújo JV, Braga FR, Araujo JM, Silva AR, Tavela AO (2009) Predatory activity of nematophagous fungi on Ancylostoma spp. infective larvae: evaluation in vitro and after passing through gastrointestinal tract of dogs. J Helminthol 15:1–6

    Google Scholar 

  • Carvalho RO, Araújo JV, Braga FR, Araujo JM, Alves CDF (2010) Ovicidal activity of Pochonia chlamydosporia and Paecilomyces lilacinus on Toxocara canis eggs. Vet Parasitol 169:123–127

    CAS  PubMed  Google Scholar 

  • Castro AA, Oliveira C, Anjos D, Bittencourt V, Araújo JV, Rodrigues M (2003) Potencial de fungos nematófagos Arthrobotrys sp e Monacrosporium thaumasium para o controle de larvas de ciatostomíneos de eqüinos (Nematoda–Cyathostominae). Rev Bras Parasitol Vet 12:53–57

    Google Scholar 

  • Cooke RC, Godfrey BES (1964) A key of nematode-destroying fungi. Trans Br Mycol Soc 47:61–74

    Google Scholar 

  • Dallemole-Giaretta R, Freitas LG, Lopes EA, Pereira OL, Zooca RJF, Ferraz S (2012) Screening of Pochonia chlamydosporia Brazilian isolates as biocontrol agents of Meloidogyne javanica. Crop Prot 42:102–107

    Google Scholar 

  • Dias AS, Araújo JV, Campos AK, Braga FR (2007) Application of a formulation of the nematophagous fungus Duddingtonia flagrans in the control of cattle gastrointestinal nematodiosis. World J Microbiol Biotechnol 38:1245–1252

    Google Scholar 

  • Dias AS, Araújo JV, Braga FR, Pupim AC, Perboni WR (2013) Pochonia chlamydosporia in the biological control of Fasciola hepatica in cattle in Southeastern Brazil. Parasitol Res 112:2131–2136

    CAS  PubMed  Google Scholar 

  • Faedo M, Larsen M, Thamsborg S (2000) Effect of different times of administration of the nematophagous fungus Duddingtonia flagrans on the transmission of ovine parasitic nematodes on pasture – a plot study. Vet Parasitol 94:55–65

    CAS  PubMed  Google Scholar 

  • Fernandes FM, Araújo JV, Braga FR, Guimarães PHG, Araujo JM, Ferreira SR, Carvalho RO, Mello IK, Fujiwara RT (2012) In vitro biological control of infective larvae of Ancylostoma ceylanicum. Rev Bras Parasitol Vet 21:283–286

    PubMed  Google Scholar 

  • Ferreira SR, Araújo JV, Braga FR, Araujo JM, Carvalho RO, Silva AR, Frassy LN, Freitas LG (2011) Ovicidal activity of seven Pochonia chlamydosporia fungal isolates on Ascaris suum eggs. Trop Anim Health Prod 43:639–642

    PubMed  Google Scholar 

  • Ferreira SR, Araújo JV, Braga FR, Tavela AO, Lafisca A (2012) In-vitro sensitivity of infective larvaeof Oesophagostomum species to nematophagous fungi. Vet Scan 7:60–67

    Google Scholar 

  • Fitz-Aranda JA, Mendoza-de-Gives P, Torres-Acosta JF, Liébano-Hernández E, López-Arellano ME, Sandoval-Castro CA, Quiroz-Romero H (2013) Duddingtonia flagrans chlamydospores in nutritional pellets: effect of storage time and conditions on the trapping ability against Haemonchus contortus larvae. J Helminthol 16:1–6

    Google Scholar 

  • Frassy LN, Braga FR, Silva AR, Araújo JV, Ferreira SR, Freitas LG (2010) Destruição de ovos de Toxocara canis pelo fungo nematófago Pochonia chlamydosporia. Rev Soc Bras Med Trop 43:102–104

    PubMed  Google Scholar 

  • Gams W, Zare R (2001) A revision of Verticillium sect. Prostrata: III. Generic classification. Nova Hedwig 73:329–337

    Google Scholar 

  • Gomes APS, Araújo JV, Guimarães MP (2000) Arthrobotrys robusta no controle biológico de nematóides parasitos gastrointestinais de bovinos. Rev Bras Ciênc Vet 7:69–74

    Google Scholar 

  • Gortari C, Cazau C, Hours R (2007) Nematophagous fungi of Toxocara canis eggs in a public park of La Plata, Argentina. Rev Iberoam Micol 24:24–28

    PubMed  Google Scholar 

  • Gronvold J, Henriksen SA, Larsen M, Nansen P, Wolstrup J (1996) Aspects of biological control with special reference to arthropods, protozoans and helminths of domesticated animals. Vet Parasitol 64:47–64

    CAS  PubMed  Google Scholar 

  • Jackson F, Miller J (2006) Alternative approaches to control—Quo vadit? Vet Parasitol 139:371–384

    PubMed  Google Scholar 

  • Jansson H-B, Nordring-Hertz B (1988) Infection events in the fungus-nematode system. In: Poinar GO Jr, Jansson H-B (eds) Diseases of nematodes. Boca RatonCRC Press, Boca Raton, pp 59–72

  • Kahn LP, Norman TM, Walkden-Brown SW, Crampton A, O’Connor LJ (2007) Trapping efficacy of Duddingtonia flagrans against Haemonchus contortus at temperatures existing at lambing in Australia. Vet Parasitol 46(1-2):83–89

    Google Scholar 

  • Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441

    CAS  PubMed  Google Scholar 

  • Kerry BR, Hidalgo L (2004) Application of Pochonia chlamydosporia in the integrated control of root-knot nematodes on organically grown vegetable crops in Cuba. IOBC Bulletin 27(1):123–126

    Google Scholar 

  • Kerry BR, Simon A, Rovira AD (1984) Observations on the introduction of Verticillium chlamydosporium and other parasitic fungi into soil for control of the cereal cystnematode Heterodera avenae. Ann Appl Biol 105:509–516

    Google Scholar 

  • Khan A, Williams KL, Nevalainen KM (2004) Effects of Paecilomyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biol Control 31:346–352

    CAS  Google Scholar 

  • Knox MR, Josh PF, Aanderson LJ (2002) Deployment of Duddingtonia flagrans in an improved pasture system: dispersal, persistence, and effects on free-living soil nematodes and microarthropods. Biol Control 24:176–182

    Google Scholar 

  • Larsen M (1999) Biological control of helminths. Int J Parasitol 29:139–146

    CAS  PubMed  Google Scholar 

  • Lopez-Llorca LV, Maciá-Vicente JG, Jansson H-B (2008) Mode of action and interactions of nematophagous fungi. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, Dordrecht, pp 51–76

    Google Scholar 

  • Lysek H (1976) Classification of ovicide fungi according to type of ovicidity. Acta Univ Palacki Olomuc 76:9–13

    Google Scholar 

  • Lysek H, Nigenda G (1989) Capacidad de autodeshelmintizacón del suelo. Salud Pública Méx 31:763–771

    CAS  PubMed  Google Scholar 

  • Lysek H, Sterba J (1991) Colonization of Ascaris lumbricoides eggs by the fungus Verticillium chlamydosporium Goddard. Folia Parasitol 38:255–259

    CAS  PubMed  Google Scholar 

  • Lysek H, Fassatiová O, Pineda NC, Hernández NL (1982) Ovicidal fungi in soils of Cuba. Folia Parasitol 29:265–270

    Google Scholar 

  • Maciel AS, Araújo JV, Cecon PR (2006) Atividade predatória in vitro dos fungos Arthrobotrys robusta, Duddingtonia flagrans e Monacrosporium thaumasium sobre larvas infectantes de Ancylostoma spp. de cães. Rev Bras Parasitol Vet 15:71–75

    PubMed  Google Scholar 

  • Maciel AS, Araújo JV, Campos AK, Benjamin LA, Freitas LG (2009a) Scanning electron microscopy of Ancylostoma spp. dog infective larvae captured and destroyed by the nematophagous fungus Duddingtonia flagrans. Micron 40:463–470

    CAS  PubMed  Google Scholar 

  • Maciel AS, Araújo JV, Campos AK, Lopes E, Freitas LG (2009b) Predation of Ancylostoma spp. dog infective larvae by nematophagous fungi in different conidial concentrations. Vet Parasitol 161:239–247

    CAS  PubMed  Google Scholar 

  • Maciel AS, Freitas LG, Campos AK, Lopes E, Araújo JV (2010) The biological control of Ancylostoma spp. dog infective larvae by Duddingtonia flagrans in a soil microcosm. Vet Parasitol 173: 262–270

    Google Scholar 

  • Mauchline TH, Kerry BR, Hirsch P (2003) The biocontrol fungus Pochonia chlamydosporia shows nematode host preference at the infraspecific level. Mycol Res 108:161–169

    Google Scholar 

  • Mello INK, Braga FR, Monteiro T, Freitas LG, Araujo JM, Soares FEF, Araújo JV (2013) Biological control of infective larvae of Ancylostoma spp. in beach sand. Rev Iberoam Micol. doi:10.1016/j.riam.2013.05.003

    Google Scholar 

  • Melo LM, Araújo JV, Pessoa LM, Reis IF, Bevilacqua C (2001) Testes in vivo e in vitro com o fungo nematófago Monacrosporium thaumasium. Cienc Anim 11:70–73

    Google Scholar 

  • Melo LM, Bevilaqua CML, Araújo JV (2003) Atividade predatória do fungo Monacrosporium thaumasium contra o nematóide Haemonchus contortus, após passagem pelo trato gastrintestinal de caprinos. Ciênc Rural 33:169–171

    Google Scholar 

  • Mota M, Bevbilacqua C, Araújo JV (2000) Atividade predatória dos fungos Arthrobotrys conoides e Monacrosporium thaumasium sobre larvas infectantes de Haemonchus contortus de caprinos. Ciência Animal 10:37–41

    Google Scholar 

  • Mota M, Campos AK, Araújo JV (2002) Evaluation of the predatory capacity of the fungi Arthrobotrys robusta and Monacrosporium thaumasium submitted to different preservation methods against gastrointestinal parasitic nematodes of bovines. Rev Bras Parasitol Vet 11:13–17

    Google Scholar 

  • Pastor FJ, Guarro J (2006) Clinical manifestations, treatment and outcome of Paecilomyces lilacinus infections. Clin Microbiol Infect 12:948–960

    CAS  PubMed  Google Scholar 

  • Paula AT, Braga FR, Carvalho LM, Lelis RT, Mello INK, Tavela AO, Soares FEF, Junior AM, Garcia JS, Araújo JV (2013) First report of the activity of predatory fungi on Angiostrongylus cantonensis (Nematoda: Angiostrongylidae) first-stage larvae. Acta Trop 127:187–190

    PubMed  Google Scholar 

  • Paz-Silva A, Francisco I, Valero-Coss RO, Cortiñas FJ, Sánchez JA, Francisco R, Arias M, Suárez JL, López-Arellano ME, Sánchez-Andrade R, de Gives PM (2011) Ability of the fungus Duddingtonia flagrans to adapt to the cyathostomin egg-output by spreading chlamydospores. Vet Parasitol 30:277–282

    Google Scholar 

  • Redua CRO, Siciliano S, Mujica F, Araújo JV, Rodrigues M (2002) Avaliação da passagem do fungo nematófago Monacrosporium thaumasium pelo trato gastrintestinal de equinos. Cienc Anim 12:133–136

    Google Scholar 

  • Rocha RA, Araújo JV, Amarante AFT (2007) Efficacy of the nematode-trapping fungus Duddingtonia flagrans against infections by Haemonchus and Trichostrongylus species in lambs at pasture. J Helminthol 81:387–392

  • Rodrigues M, Castro AA, Oliveira C, Anjos DHS, Bittencourt V, Araújo JV (2001) Capacidade predatória de Arthrobotrys sp e Monacrosporium thaumasium sobre larvas de ciatostomíneos. Rev Bras Parasitol Vet 10:51–54

    Google Scholar 

  • Sagüés MF, Purslow P, Fernández S, Fusé L, Iglesias L, Saumell C (2011) Nematophagous fungi used for the biological control of gastrointestinal nematodes in livestock and administration routes. Rev Iberoam Micol 28:143–147

    PubMed  Google Scholar 

  • Saxena G, Mittal T (1995) Trap formation by conidia of nematode-trapping Monacrosporium thaumasium spp. Mycol Res 7:839–840

    Google Scholar 

  • Silva AR, Araújo JV, Braga FR, Carvalho RO, Tavela AO, Frassy LN, Castejon FV (2009) Biological control of sheep gastrointestinal nematodiosis in a tropical region of the southeast of Brazil with the nematode predatory fungi the nematode predatory fungi Duddingtonia flagrans and Monacrosporium thaumasium. Parasitol Res 105:1707–1713

    PubMed  Google Scholar 

  • Silva AR, Araújo JV, Braga FR, Alves CDF, Filho JDR (2010a) Destruction of Anoplocephala perfoliata eggs by the nematophagous fungus Pochonia chlamydosporia. J Equine Vet Sci 30:701–704

    Google Scholar 

  • Silva AR, Araújo JV, Braga FR, Alves CDF, Frassy LN (2010b) In vitro ovicidal activity of the nematophagous fungi Duddingtonia flagrans, Monacrosporium thaumasium and Pochonia chlamydosporia on Trichuris vulpis eggs. Vet Parasitol 172:76–79

    CAS  PubMed  Google Scholar 

  • Silva BF, Mauad JRC, Braga FR, Araújo JV, Campos AK, Amarante AFT (2010c) Efficacy of Duddingtonia flagrans and Arthrobotrys robusta in controlling sheep parasitic gastroenteritis. Parasitol Res 106:1343–1350

    PubMed  Google Scholar 

  • Silva AR, Araújo JV, Braga FR, Alves CDF, Frassy LN (2011) Activity of fungal conidia of the Duddingtonia flagrans and Monacrosporium thaumasium on Haemonschus contortus infective larvae. J Helminthol 85:138–141

    Google Scholar 

  • Silva ME, Araújo JV, Braga FR, Soares FEF (2013) Control of infective larvae of gastrointestinal nematodes of heifers by isolates of the nematophagous fungi. Rev Bras Parasitol Vet 26:1–6

    Google Scholar 

  • Soares FEF, Braga FR, Araújo JV, Lima WS, Mozer LR, Queiróz JH (2012) In vitro activity of a serine protease from Monacrosporium thaumasium fungus against first-stage larvae of Angiostrongylus vasorum. Parasitol Res 110:2423–2427

    PubMed  Google Scholar 

  • Soares FEF, Braga FR, Araújo JV, Mozer LR, Lima WS, Queiroz JH (2013) Nematicidal activity of three novel extracellular proteases of the nematophagous fungus Monacrosporium sinense. Parasitol Res 112:1557–1565

    PubMed  Google Scholar 

  • Steiner B, Aquino VR, Paz AA, Silla Rocha LM, Zavascki A, Goldani L (2013) Paecilomyces variotii as an emergent pathogenic agent of pneumonia. Case Reports in Infectious Diseases. ID 273848, 3 pp, 2013. doi:10.1155/2013/273848

  • Stirling GR, West LM (1991) Fungal parasites of root-knot nematodes eggs from tropical and sub tropical regions of Austrália. Australas Plant Pathol 20:149–154

    Google Scholar 

  • Tavela AO, Araújo JV, Braga FR, Silva AR, Araujo JM, Carvalho RO, Ferreira SR, Carvalho GR (2010) Biological control of cyathostomin (Nematoda: Cythostominae) with nematophagous fungus Monacrosporium thaumasium in tropical southeastern Brazil. Vet Parasitol 175:92–96

    Google Scholar 

  • Tavela AO, Araújo JV, Braga FR, Araujo JM, Queiroz LM, Silveira WF, Borges LA (2012) In vitro association of nematophagous fungi Duddingtonia flagrans (AC001), Monacrosporium thaumasium (NF34) and Pochonia chlamydosporia (VC1) to control horse cyathostomin (Nematoda: Strongylidae). Biochem Sci Technol 22:607–610

    Google Scholar 

  • Tavela AO, Araújo JV, Braga FR, Silveira WF, Silva VHD, Junior MC, Araujo JM, Benjamin LA, Carvalho GR, Paula AT (2013) Coadministration of sodium alginate pellets containing the fungi Duddingtonia flagrans and Monacrosporium thaumasium on cyathostomin infective larvae after passing through the gastrointestinal tract of horses. Res Vet Sci 94:568–572

    Google Scholar 

  • Van Ooij C (2011) Fungal pathogenesis: hungry fungus eats nematode. Nat Rev Microbiol 9:766–767

    PubMed  Google Scholar 

  • Vilela VL, Feitosa TF, Braga FR, Araújo JV, Souto DVO, Santos HES, Athayde ACR (2012) Biological control of goat gastrointestinal helminthiasis by Duddingtonia flagrans in a semi-arid region of the Northeastern Brazil. Vet Parasitol 188:127–133

    PubMed  Google Scholar 

  • Vilela VLR, Feitosa TF, Braga FR, Araújo JV, Lucena SC, Dantas ES, Athayde ACR, Silva AR (2013) Effect of Monacrosprorium thaumasium in the control of the goat gastrointestinal helminthiasis in the semi-arid of Brazil. Parasitol Res 112:871–877

    PubMed  Google Scholar 

  • Waller PJ (2005) Sustainable nematode parasite control strategies for ruminant livestock by grazing management and biological control. Anim Feed Sci Technol 126:277–289

    Google Scholar 

  • Waller PJ, Faedo M (1996) The prospect for biological control of the free living stages of nematode parasite of livestock. Int J Parasitol 26:915–925

    CAS  PubMed  Google Scholar 

  • Wang Y, Sun L, Yi S, Huang Y, Lenaghan SC, Zhang M (2013) Naturally occurring nanoparticles from arthrobotrys oligospora as a potential immunostimulatory and antitumor agent. Advanced Functional Materials 26: 2175–2184

    Google Scholar 

  • Ward E, Kerry BR, Manzanilla-López RH, Mutua G, Devonshire J, Kimenju J, Hirsch PR (2012) The Pochonia chlamydosporia serine protease gene vcp1 is subject to regulation by carbon, nitrogen and pH: implications for nematode biocontrol. Plos One 7:35657

    Google Scholar 

  • Yang J, Tian B, Liang L, Zhang KQ (2007) Extracellular enzymes and the pathogenesis of nematophagous fungi. Appl Microbiol Biotechnol 75:21–31

    Google Scholar 

  • Yang J, Wang L, Ji X, Feng Y, Li X, Zou C, Xu J, Ren Y, Mi Q, Wu J, Liu S, Liu Y, Huang X, Wang H, Niu X, Li J, Liang L, Luo Y, Ji K, Zhou W, Yu Z, Li G, Liu Y, Li L, Qiao M, Feng L, Zhang KQ (2011) Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathog 7:1002179

    Google Scholar 

  • Yeates PJ, Waller KL (1997) Soil nematodes as indicators of the effect of management on grass-lands in the New England Tablelands NSW: effect of measures for control of parasites of sheep. Pedobiology 41:537–548

    Google Scholar 

  • Yeates GW, Dimander SO, Waller PJ, Hoglund J (2002) Environmental impact on the soil nematodes following the use of either ivermectin sustained release boluses or the nematophagous fungus Duddingtonia flagrans to control nematode parasites of cattle in Sweden. Acta Agric Scand A Anim Sci 52:233–242

    CAS  Google Scholar 

  • Zhang Y, Yu Z-F, Xu J, Zhang K-Q (2011) Divergence and dispersal of the nematode-trapping fungus Arthrobotrys oligospora from China. Environ Microbiol Rep 3:763–773

    PubMed  Google Scholar 

  • Zhang Y, Quiao M, Xu J, Cao Y, Zhang KQ, Yu ZFY (2013) Genetic diversity and recombination in natural populations of the nematode-trapping fungus Arthrobotrys oligospora from China. Ecol Evol 3:312–325

    PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Veterinária, Universidade Federal de Viçosa, Viçosa, MG, Brazil

    Fabio Ribeiro Braga & Jackson Victor de Araújo

  2. Universidade Vila Velha, Vila Velha, ES, Brazil

    Fabio Ribeiro Braga

Authors
  1. Fabio Ribeiro Braga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jackson Victor de Araújo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jackson Victor de Araújo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Braga, F.R., de Araújo, J.V. Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Appl Microbiol Biotechnol 98, 71–82 (2014). https://doi.org/10.1007/s00253-013-5366-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5366-z

Keywords

Search

Navigation