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Licensed Unlicensed Requires Authentication Published by De Gruyter July 5, 2017

In vitro and in vivo studies of nematophagous fungi Arthrobotrys musiformis and Arthrobotrys robusta against the larvae of the trichostrongylides

Kui Zheng Cai, Bo Bo Wang, Qiang Xu, Jun Lin Liu, Kang Ying Wang, Yu Jia Xue, Hai Yan Zhang, Hai Yu Wang, Xin Cao and Zhong Ren Ma
From the journal Acta Parasitologica

Abstract

Six isolates of Arthrobotrys musiformis and five isolates of Arthrobotrys robusta were assessed in in vitro test regarding the capacity of prey larvae of the natural mixed trichostrongylides. In 5 isolates of A. robusta, the decrease percentage of infective larvae (L3) of trichostrongylides ranged from 97.71%–99.98% and for the isolates of A. musiformis, 5 isolates ranged from 97.99%–99.95% and only NF015 isolate 60.72%. In the following, the isolate (NPS045) of A. musiformis was selected to assess its excretion time in feces after oral administration of goats. Regarding L3 reduction rate, results demonstrated by NPS045 at each time point after fungal administration were 31.65% (12 h), 51.25% (24 h), 41.07% (48 h), 6.44% (72 h), 0% (96 h) and (120 h) (p<0.05) respectively, when compared to the control group. In the plates of the treated groups, the presence of the isolate (NPS045) was detected in samples at 12, 24 and 48 h after the fungus dose and 72 h later was not done. All native isolates of nematophagous fungi, including 6 isolates of A. musiformis and 5 isolates of A. robusta were assessed in vivo regarding the capacity of supporting the passage through goat gastrointestinal tract. The 3 isolates of A. musiformis could be able to pass through the digestive tract of goats without complete loss of ability of preying larvae of trichostrongylides in feces and their efficacies ranged from 47.60% to 55.93%. The two isolates of A. robusta survived the passage and the percentage reduction of L3 in feces were 41.96% and 66.97%, respectively. The remaining isolates were negative for both the efficacy of L3 reduction and the fungal examination in feces. In this study, the native isolates whose efficacies are good in vivo test have preliminarily demonstrated to be potential for the biological control of small ruminant parasite.

  1. Conflict of interest statement: All authors declare no financial or commercial conflicts of interest.

Acknowledgements

We gratefully acknowledge the financial support of the Key Cultivation Project of the Central University (31920170159) and National Natural Science Foundation of China (NSFC) (31660708).

References

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, 200–206. 10.1134/S0026261711020020Search in Google Scholar

Araújo J.V., Santos M.A., Ferraz S., Maia A.S. 1993. Antagonistic effect of predacious fungi Arthrobotrys on infective Haemonchus placei larvae. Journal Helmintholohy, 67, 136–138. 10.1017/S0022149X00013018Search in Google Scholar

Araújo J.V., Assis R.C.L., Campos A.K., Mota M.A. 2006. Efeito antagônico de fungos predadores dos gêneros Monacrosporium, Arthrobotrys e Duddingtonia sobre larvas infectantes de Cooperia sp. e Oesophagostomum sp.. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 58, 373–380. 10.1590/S0102-09352006000300014. (In Spanish)Search in Google Scholar

Araújo J.M., Araújo J.V., Braga F.R., Carvalho R.O. 2010. In vitro predatory activity of nematophagous fungi and after passing through gastrointestinal tract of equine on infective larvae of Strongyloides westeri. Parasitology Research, 107, 103–107. 10.1007/s00436-010-1841-ySearch in Google Scholar

Assis R.C., Luns F.D., Araújo J.V., Braga F.R., Assis R.L., Marcelino J.L., et al. 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 Parasitology, 193, 134–140. 10.1016/j.vetpar.2012.12.005Search in Google Scholar PubMed

Barcante J.M., Barcante T.A., Dias S.R., Vieira L.Q., Lima W.S., Negraocorrea D. 2003. A method to obtain axenic Angiostrongylus vasorum first-stage larvae from dog feces. Parasitology Research, 89, 89–93. 10.1007/s00436-002-0719-zSearch in Google Scholar

Barger I.A. 1999. The role of epidemiological knowledge and grazing management for helminth control in small ruminants. International Journal for Parasitology, 29, 41–47. 10.1016/S0020-7519(98)00176-3Search in Google Scholar

Braga F.R., Araújo J.V., Araujo J.M., Silva A.R., Carvalho R.O., Campos A.K. 2009a. Avaliação in vitro do fungo predador de nematoides Duddingtonia flagrans sobre larvas infectantes de ciatostomíneos deequinos (Nematoda: Cyathostominae). Revista Brasileira De Parasitologia Veterinaria, 18, 83–85. 10.1016/j.vetpar.2012.12.005. (In Spanish)Search in Google Scholar

Braga F.R., Carvalho R.O., Araujo J.M., Silva A.R., Araújo J.V., Lima W.S, et al. 2009b. Predatory activity of the fungi Duddingtonia flagrans, Monacrosporium thaumasium, Monacrosporium sinense and Arthrobotrys robusta on Angiostrongylus vasorum first-stage larvae, Journal of Helminthology, 83, 303–308. 10.1017/S0022149X09232342Search in Google Scholar PubMed

Braga F.R., Silva A.R., Carvalho R.O., Araújo J.V., Guimarães P.H.G., Fujiwara R.T., Frassy L.N. 2010. In vitro predatory activity of the fungi Duddingtonia flagrans, Monacrosporium thaumasium, Monacrosporium sinense and Arthrobotrys robusta on Ancylostoma ceylanicum third stage larvae. Veterinary Microbiology, 146, 183–186. 10.1016/j.vetmic.2010.05.003Search in Google Scholar PubMed

Braga F.R., Araujo J.V. 2014. Nematophagous fungi for biologicalcontrol of ga-trointestinal nematodes in domestic animals. Applied Microbiology and Biotechnology, 98, 71–82. 10.1007/s00253-013-5366-zSearch in Google Scholar

Cai K.Z., Liu J.L., Liu W., Wang B.B., Xu Q., Sun L.J., et al. 2016. Screening of different sample types associated with sheep and cattle for the presence of nematophagous fungi in China. Journal of Basic Microbiology, 56, 214–228. 10.1002/jobm.201500281Search in Google Scholar

Craig T. M. 2006. Anthelmintic resistance and alternative control methods. Veterinary Clinics of North America–Food Animal Practice, 22, 567–581. 10.1016/j.cvfa.2006.07.003Search in Google Scholar

De Gives P.M., Crespo J.F., Rodriguez D. H., Prats V. M. V., Rodríguez D.H., Hernández E. L., Ontiveros Fernandez G.E. 1998. Biological control of Haemonchus contortus infective larvae in ovine faeces by administering an oral suspension of Duddingtonia flagrans chlamydospores to sheep. Journal of Helminthology, 72, 343–347. 10.1017/S0022149X00016710Search in Google Scholar

Dias A.S., Araújo J.V., Campos A.K., Braga F.R., Fonseca T.A. 2007. Application of a formulation of the nematophagous fungus Duddingtonia flagrans in the control of cattle gastrointestinal nematodioses. World Journal of Microbiology, 28, 1000–1007. 10.1007/s11274-007-9356-0Search in Google Scholar

Faizal A.C.M., Rajapakse R.P.V.J. 2004. A preliminary study to determine the efficacy of a nematophgous fungus, Arthrobotry oligospora, against nematode larvae in cattle and goat dung. Journal of the National Science Foundation of Sri Lanka, 32, 29–33. 10.1016/j.vetpar.2008.09.026Search in Google Scholar

Falzon L.C., van Leeuwen J., Menzies P.I., Shakya K.P., Jones-Bitton A., Sears W., et al. 2013. Anthelmintic resistance in sheep flocks in Ontario, Canada. Veterinary Parasitology, 193, 150–162. org/10.1016/j.vetpar.2012.11.014Search in Google Scholar

Ferreira S.R., Araújo J.V., Braga F.R., Araujo J.M., Carvalho R.O., Silva A.R., et al. 2011. Ovicidal activity of seven Pochonia chlamydosporia fungal isolates on Ascaris suum eggs. Tropical Animal Health and Production, 43, 639–642. 10.1007/s11250-010-9744-6Search in Google Scholar

Gr⊘nvold J., Nansen P., Henriksen S.A., Larsen M., Wolstrup J., Bresciani J., et al. 1996. Induction of traps by Ostertagia ostertagi larvae, chlamydospore production and growth rate in the nematode-trapping fungus Duddingtonia flagrans. Journal of Helminthology, 70, 291–297. .1017/S0022149X00015571Search in Google Scholar

Larsen M., Faedo M., Waller P.J., Hennessy D.R. 1998. The potential of nematophagous fungi to control the free-living stages of nematode parasites of sheep: Studies with Duddingtonia flagrans. Veterinary Parasitology, 76, 121–128. 10.1016/S0304-4017(97)00056-3Search in Google Scholar

Larsen M. 1999. Biological control of helminths. International Journal For Parasitology, 29, 139–146. 10.1016/S0020-7519(98)00185-4Search in Google Scholar

Menkir M.S., Asefa A., Uggla A., Waller P.J. 2006. Anthelmintic resistance of nematode parasites of small ruminantsineastern Ethiopia: exploitation of refugia to restore anthelmintic efficacy. Veterinary Parasitology, 135, 337–346. 10.1016/j.vetpar.2005.09.005Search in Google Scholar

Mota M.A., Campos A.K., Araújo J.V. 2003. Controle biológico de helmintos parasitos de animais: estágio atual e perspectivas futuras. Pesquisa Veterinaria Brasileira, 23, 93–100. 10.1590/S0100-736X2003000300001. (In Spanish)Search in Google Scholar

Nansen P., Foldager J., Hansen J., Henriksen S.A., Jorgensen R.J. 1988. Grazing pressure and acquisition of Ostertagia ostertagi in calves. International Journal Parasitology, 27, 325–335. 10.1016/0304-4017(88)90046-5Search in Google Scholar

Paz-Silva A., Francisco I., Valero-Coss R.O., Cortiñas F.J., Sánchez J.A., Francisco R., et al. 2011. Ability of the fungus Duddingtonia flagrans to adapt to the cyathostomin egg-output by spreading chlamdospores. Veterinary Parasitology, 179, 277–282. 10.1016/j.vetpar.2011.02.014Search in Google Scholar

Petkevicius S., Larsen M., Bach Knudsen E. K., Nansen P., Gronvolda J., Henriksen S. A. A., Wolstrup J. 1998. The effect of the nematode-destroying fungus Duddingtonia flagrans against Oesophagostomum dentatum larvae in faeces from pigs fed different diets. Helminthologia, 35, 111–116Search in Google Scholar

Sargison N.D. 2012. Pharmaceutical treatments of gastrointestinal nematode infections of sheep—future of anthelmintic drugs, Veterinary Parasitology, 189, 79–84. 10.1016/j.vetpar.2012.03.035Search in Google Scholar

Scholler M., Rubner A. 1994. Predacious activity of the nematode-destroying fungus Arthrobotrys oligospora in dependence of the medium composition. Microbiological research, 149, 145–149. 10.1016/S0944-5013(11)80110-2Search in Google Scholar

Silva B.F., Mauad J.R.C., Braga F.R., Araújo J.V., Campos A.K., Amarante A.F.T. 2010. Efficacy of Duddingtonia flagrans and Arthrobotrys robusta in controlling sheep parasitic gastroenteritis. Parasitology Research, 106, 1343–1350. 10.1007/s00436-010-1805-2Search in Google Scholar PubMed

Tavela A.O., Araújo J.V., Braga F.R., Araújo J.M., Queiroz L.M., Silveira W.F., Borges L.A. 2012. In vitro association of nematophagous fungi Duddingtonia flagrans (AC001), Monacrosporium thaumasium (NF34) and Pochonia chlamydosporia (VC1) to control horse cyathostomin (Nematoda: Strongylidae). Biochemisty Science Technology, 22, 607–610. 10.1080/09583157.2012.672952Search in Google Scholar

Tavela A.O, Araújo J.V., Braga F.R., Silveira W.F., Dornelas e Silva V.H., Carretta Júnior M., et al. 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. Research Veterinary, 94, 568–572. 10.1016/j.rvsc.2012.11.011Search in Google Scholar PubMed

Terril T.H., Larsen M., Samples O., Hsted S., Miller J.E., Kaplan RM., 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. 10.1016/j.vetpar.2003.09.024Search in Google Scholar

Van Wyk J.A., Cabaret J., Michael L.M. 2004. Morphological identification of nematode larvae of small ruminants and cattle simplified. Veterinary Parasitology, 119, 277–306. 10.1016/j.vetpar.2003.11.012Search in Google Scholar

Waghorn T.S., Leathwick D.M., Chen L.Y., Skipp R.A. 2003. Efficacy of the nematode-trapping fungus Duddingtonia flagrans against threespecies of gastro-intestinal nematodesin laboratory faecal cultures from sheep and goats. Veterinary Parasitology, 118, 227–234. 10.1016/j.vetpar.2003.09.018.Search in Google Scholar

Waller P.J., Faedo M. 1993. The potential of nematophagous fungi to control the free-living stages of nematode parasites of sheep: screening studies. Veterinary Parasitology, 49, 285-297. 10.1016/0304-4017(93)90127-9Search in Google Scholar

Wang B.B., Liu W., Chen M.Y., Li X., Han Y., Xu Q., et al. 2015. Isolation and characterization of china isolates of Duddingtonia flagrans, a candidate of the nematophagous fungi for biocontrol of animal parasitic nematodes. Journal of Parasitology, 101, 476–484. 10.1645/14-715.1Search in Google Scholar PubMed

Received: 2016-10-29
Revised: 2017-4-27
Accepted: 2017-5-17
Published Online: 2017-7-5
Published in Print: 2017-9-26

© 2017 W. Stefański Institute of Parasitology, PAS