A pilot study of the in vitro efficacy of different concentrations of Duddingtonia flagrans for the control of gastrointestinal nematodes of sheep

Authors

  • Barbara Paoletti Department of Veterinary Medicine, University of Teramo, Teramo, Italy
  • Raffaella Iorio Department of Veterinary Medicine, University of Teramo, Teramo, Italy
  • Simone Morelli Department of Veterinary Medicine, University of Teramo, Teramo, Italy
  • Lisa Di Teodoro Department of Veterinary Medicine, University of Teramo, Teramo, Italy
  • Elisabetta De Angelis Vet Practitioner, Teramo, Italy
  • Roberto Bartolini Department of Veterinary Medicine, University of Teramo, Teramo, Italy
  • Angela Di Cesare Department of Veterinary Medicine, University of Teramo, Teramo, Italy

DOI:

https://doi.org/10.17420/ap7002.528

Abstract

Duddingtonia flagrans is a nematode trapping fungus used for the control of gastrointestinal nematodes in livestock. The quantity of chlamydospores of D. flagrans required for the reduction of third-stage larvae (L3) of sheep gastrointestinal nematodes (GIN) is largely unknown, and a matter of discussion. The aim of this experiment was to determine in vitro the nematophagous activity of four different concentrations of D. flagrans (1000, 3000, 6250, or 11000 chlamydospores/ml) in the presence of varying numbers of GIN third-stage larvae (L3) (500, 1000, 1500). Additionally, the study sought to evaluate the efficacy of this fungus on Haemonchus contortus, Teladorsagia circumcincta, Trichostrongylus colubriformis and Chabertia ovina. The results showed that as fungal concentrations increased, so did the larval reduction of third-stage infective larvae in each test. L3s number was not a determining factor in the efficacy against GIN. The comparison between various concentrations of chlamydospores revealed significant differences, particularly between 1000 and 11000 chlamydospores (P≤0.05). Regarding the larval reduction of the GIN species considered, D. flagrans demonstrated the same effectiveness across all species tested. The results of the current study confirm the efficacy and underscore the importance of D. flagrans as an alternative for controlling of GIN.

Author Biographies

Raffaella Iorio, Department of Veterinary Medicine, University of Teramo, Teramo, Italy

Department of Veterinary Medicine

Lisa Di Teodoro, Department of Veterinary Medicine, University of Teramo, Teramo, Italy

Department of Veterinary Medicine

Elisabetta De Angelis, Vet Practitioner, Teramo, Italy

Vet Practitioner

Roberto Bartolini, Department of Veterinary Medicine, University of Teramo, Teramo, Italy

Department of Veterinary Medicine

Angela Di Cesare, Department of Veterinary Medicine, University of Teramo, Teramo, Italy

Department of Veterinary Medicine

References

Mavrot F., Hertzberg H., Torgerson P. 2015. Effect of gastro-intestinal nematode infection on sheep performance: a systematic review and metaanalysis. Parasites & Vectors 8: 557. https://doi.org/10.1186/s13071-015-1164-z

Charlier J., Rinaldi L., Musella V., Ploeger H., Chartier C., Vineer H., Hinney B., von Samson- Himmelstjerna G., Băcescu B., Mickiewicz M., Mateus T., Martinez-Valladares M., Quealy S., Azaizeh H., Sekovska B., Akkari H., Petkevicius S., Hektoen L., Höglund J., Morgan E., Bartley D., Claerebout E. 2020. Initial assessment of the economic burden of major parasitic helminth infections to the ruminant livestock industry in Europe. Preventive Veterinary Medicine 182: 105103. https://doi.org/10.1007/s13205-019-2042-8

Sargison N.D. 2012. Pharmacceutical treatments of gastrointestinal nematode infections of sheep-future of anthelimintic drugs. Veterinary Parasitology 189: 79–84. https://doi.org/10.1016/j.vetpar.2012.03.035

Kaplan R.M., Vidyashankar A.N. 2012. An inconvenient truth: global worming and anthelmintic resistance. Veterinary Parasitology 186: 70–78. https://doi.org/10.1016/j.vetpar.2011.11.048

Papadopoulos E., Gallidis E., Pthochos S. 2012. Anthelmintic resistance in sheep in Europe: a selected review. Veterinary Parasitology 189: 85–88. https://doi.org/10.1016/j.vetpar.2012.03.036

Rose H., Rinaldi L., Bosco A., Mavrot F., De Waal T., Skuce P., Charlier J., Torgerson P.R., Hertzberg H., Hendrickx G., Vercruysse J., Morgan E.R. 2015. Widpread anthelmintic reistance in European farmed ruminants: a systematic review. Veterinary Record 176: 546. https://doi.org/10.1136/vr.102982

Charlier J., Hoste H., Sotiraki S. 2023. COMBAR – Combatting anthelmintic resistance in ruminants. Parasite 30: E1. https://doi.org/10.1016/bs.apar.2021.12.002

Larsen M. 1999. Biological control of helminths. International Journal for Parasitology 29: 139–146. https://doi.org/10.1016/S0020-7519(98)00185-4

Sagües M.F., Fusé L.A., Iglesias L.E., Moreno F.C., Saumell C.A. 2013. Optimization of production of chlamydospores of the nematode-trapping fungus Duddingtonia flagrans in solid culture media. Parasitology Research 112: 1047–1051. https://doi.org/10.1007/s00436-012-3231-0

Braga F.R., Araujo J.V. 2014. Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Applied Microbiology and Biotechnology 98: 71–82. https://doi.org/10.1007/s00253-013-5366-z

da Silva M.E., Braga F.R., de Gives P.M., Uriostegui M.A.M., Reyes M., de Freitas Soares F.E., de Carvalho L.M., Rodrigues F.B., de Araújo J.V. 2015. Efficacy of Clonostachys rosea and Duddingtonia flagrans in reducing the Haemonchus contortus infective larvae. Biomed Research International 2015: 474879. https://doi.org/10.1155/2015/474879

Terril T.H., Larsen M., Samples O., Hsted S., Miller J.E., Kaplan R.M., Gelaye S. 2004. Capability of the nematode-trapping fungus Duddingtonia flagrans to reduce infective larvae of gastrointestinal nematodes in goat feces in the southeastern United States: dose titration and dose time interval studies. Veterinary Parasitology 120: 85–296. https://doi.org/10.1016/j.vetpar.2003.09.024

Dias A.S., Araújo J.V., Campos A.K., Braga F.R., Fonseca T.A. 2007. Application of a formulation of the nematophagus fungus Duddingtonia flagrans in the control of cattle gastrointestinal nematodiosis. World Journal of Microbiology 28: 1000–1007. https://doi.org/10.1007/s11274-007-9356-0

Braga F.R., Ferraz C.M., da Silva E.N., de Araújo J.V. 2020. Efficiency of the Bioverm® (Duddingtonia flagrans) fungal formulation to control in vivo and in vitro of Haemonchus contortus and Strongyloides papillosus in sheep. 3 Biotech 10: 62.

Li S., Wang D., Gong J., Zhang Y. 2022. Individual and combined application of nematophagous fungi as biological control agents against gastrointestinal nematodes in domestic animals. Pathogens 11: 172. https://doi.org/10.3390/pathogens11020172

Zegbi S., Sagües F., Saumell C., Guerrero I., Iglesias L., Fernández S. 2021. In vitro efficacy of different concentrations of Duddingtonia flagrans on varying egg densities of gastrointestinal nematodes of cattle. Experimental Parasitology 230: 108156. https://doi.org/10.1016/j.exppara.2021.108156

Shams Ghahfarokhi M., Razzaghi Abyaneh M., Ranjbar Bahadori S., Eslami A., Zare R., Ebrahimi M. 2004. Screening of soil and sheep faecal samples for predacious fungi: isolation and characterization of the nematodetrapping fungus Arthrobotrys oligospora. Iranian Biomedical Journal 8: 135–142.

M.A.F.F. 1986. Manual of veterinary parasitological laboratory techniques, Ministry of Agriculture, Fisheries and Food, Reference book 418, H.M.S.O. London.

Knoll S., Dessì G., Tamponi C., Meloni L., Cavallo L., Mehmood N., Jacquiet P., Scala A., Cappai M.G., Varcasia A. 2020. Practical guide for microscopic identification of infectious gastrointestinal nematode larvae in sheep from Sardinia, Italy, backed by molecular analysis. Parasite & Vectors 14: 505. https://doi.org/10.1186/s13071-021-05013-9

Gasser R.B., Chilton N.B., Hoste H., Beveridge I. 1993. Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21: 2525–2526. https://doi.org/10.1093/nar/21.10.2525

Flores-Crespo J., Herrera-Rodríguez D., Prats V.V., Gaytan J.C.M., de Gives P.M. 1999. Capacidad nematófaga de dos cepas del hongo Duddingtonia flagrans desarrollada en harina de maíz-agar. Veterinaria México 30: 199–203 (in Spanish with summary in English)..

Mendoza de Gives P., Crespo J.P., Rodriguez D.H., Prats V.M.V., Rodriguez D.H., Hernández E.L., Ontiveros Fernandez G.E. 1998. Biological control of Haemonchus contortus infective larvae in ovine faeces by administering an oral suspensionof Duddingtonia flagrans chlamydospores to sheep. Journal of Helminthology 72: 343–347. https://doi.org/10.1017/s0022149x00016710

Braga F.R., Araujo J.M., Araújo J.V., Soares F.E.F., Tavela A.O., Frassy L.N., dos Santos Lima W., Lanuze Rose Mozzer L.R. 2013. In vitro predatory activity of conidia of fungal isolates of the Duddingtonia flagrans on Angiostrongylus vasorum first-stage larvae. Revista da Sociedade Brasileira de Medicina Tropical 46: 108–110. https://doi.org/10.1590/0037-86829612013

Simin S., Djuric S., Kuruca L., Hajnal-Jafari I., Stamenov D., Lalošević V. 2012. Nematophagous activity of Duddingtonia flagrans MUCL 9827 against sheep gastrointestinal nematodes. Contemporary Agriculture 65: 13–20. https://doi.org/10.1515/contagri-2016-0012

Rosenzweig W.D. 1984. Role of amino acids, peptides, and medium composition in trap formation by nematode-trapping fungi. Canadian Journal of Microbiology 30: 265–267.

Den Belder E., Jansen E. 1994. Capture of plantparasitic nematodes by an adhesive hyphae forming isolate of Arthrobotrys oligospora and some other nematode-trapping fungi. Nematologica 40: 423–437.

Anan’ko G.G., Teplyakova T.V. 2011. Factors responsible for transition of the Duddingtonia flagrans carnivorous fungus from the saprotrophic to the zootrophic nutrition type. Microbiology 80: 188–193. https://doi.org/10.1134/S00262617111020020

Grønvold J., Wolstrup J., Larsen M., Gillespie A., Giacomazzi F. 2004. Interspecific competition between the nematode-trapping fungus, Duddin - gtonia flagrans, and selected microorganisms and the effect of spore concentration on the efficacy of nematode trapping. Journal of Helminthology 78: 41–46. https://doi.org/10.1079/joh2003195

Sagües M.F., Zegbi S., Guerrero I., Fernández S., Iglesias I., Junco M., Saumell C. 2020. Biological control of trichostrongylid infections in calves on pasture in Lithuania using Duddingtonia flagrans, a nematode-trapping fungus. Journal of Helminthology 74: 335–359. https://doi.org/10.1017/s0022149x00000524

Larsen M., Wolstrup J., Henriksen S.A., Dackman C., Grønvold J., Nansen P. 1991. In vitro stress selection of nematophagous fungi for biocontrol of parasitic nematodes in ruminants. Journal of Helminthology 65: 193–200. https://doi.org/10.1017/s0022149x00010701

Araújo J.V., Santos M.A., Ferraz S., Maia A.S. 1993. Antagonistic effect of predacious Arthrobotrys fungi on infective Haemonchus placei larvae. Journal of Helminthology 67: 136–138. https://doi.org/10.1017/s0022149x00013018

Fernández A.S., Larsen M., Wolstrup J., Grønvold J., Nansen P., Bjørn H. 1999. Growth rate and trapping efficacy of nematode-trapping fungi under constant and fluctuating temperatures. Parasitology Research 85: 661–668. https://doi.org/10.1007/s004360050611

Mendoza de Gives P., Vazquez-Prats V.M. 1994. Reduction of Haemonchus contortus infective larvae by three nematophagous fungi in sheep faecal cultures. Veterinary Parasitology 55: 197–203. https://doi.org/10.1016/0304-4017(93)00646-g

Mendoza de Gives P., Davies K.G., Clark S.J., Behnke J.M. 1999. Predatory behaviour of trapping fungi against srf mutants of Caenorhabditis elegans and different plant and animal parasitic nematodes. Parasitology 119: 95–104. https://doi.org/10.1017/s0031182099004424

Oliveira I.C., Vieira S., de Carvalho L.M., Campos A.K., Freitas S.G., de Ara’ujo J.M., Braga F.R., de Ara’ujo J.V. 2018. Reduction of bovine strongilides in naturally contaminated pastures in the southeast region of Brazil. Experimental Parasitology 194: 9–15. https://doi.org/10.1016/j.exppara.2018.09.008

Vieira I.S., de Castro Oliveira I., Campos A.K., de Ara´ujo J.V. 2020. In-vitro biological control of bovine parasitic nematodes by Arthrobotrys cladodes, Duddingtonia flagrans and Pochonia chlamydosporia under different temperature conditions. Journal of Helminthology 94: e194. https://doi.org/10.1017/s0022149x20000796

Flores-Crespo J., Herrera-Rodríguez D., Mendoza de Gives P., Liébano-Hernández E., Vázquez-Prats V.M., López-Arellano M.E. 2003. The predatory capability of three nematophagous fungi in the control of Haemonchus contortus infective larvae in ovine faeces. Journal of Helminthology 77: 297–303. https://doi.org/10.1079/joh2003197

Paraud C., Chartier C. 2003. Biological control of infective larvae of a gastro-intestinal nematode (Teladorsagia circumcincta) and a small lungworm (Muellerius capillaris) by Duddingtonia flagrans in goat faeces. Parasitology Research 89: 102–106. https://doi.org/10.1007/s00436-002-0717-1

Liu X.Y., Chang F.F., Zhao T.Y., Huang H.Y., Li F.D., Wang F., Wang B.B., Wang F.H., Liu Q., Luo Q.H., Cai K.Z., Zhong R.M. 2020. Biological control of sheep gastrointestinal nematode in three feeding systems in Northern China by using powder drug with nematophagous fungi. Biocontrol Science and Technology 30: 701–715. https://doi.org/10.51585/gjvr.2021.2.0010

Charlier J., Bartley D.J., Sotiraki S., Martinez- Valladares M., Claerebout E., von Samson- Himmelstjerna G., Thamsborg S.M., Hoste H., Morgan E.R., Rinaldi L. 2022. Anthelmintic resistance in ruminants: challenges and solutions. Advances in Parasitology 115: 171–227. https://doi.org/10.1016/bs.apar.2021.12.002

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Published

2024-08-18

How to Cite

Paoletti, B., Iorio, R., Morelli, S., Di Teodoro, L., De Angelis, E., Bartolini, R., & Di Cesare, A. (2024). A pilot study of the in vitro efficacy of different concentrations of Duddingtonia flagrans for the control of gastrointestinal nematodes of sheep . Annals of Parasitology, 70(2), 113–118. https://doi.org/10.17420/ap7002.528

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