Hostname: page-component-745bb68f8f-d8cs5 Total loading time: 0 Render date: 2025-02-04T12:05:20.801Z Has data issue: false hasContentIssue false
  • English
  • Français

Predatory activity of nematophagus fungus Duddingtonia flagrans in infective larvae after gastrointestinal transit: biological control in pasture areas and in vitro

Published online by Cambridge University Press:  14 June 2021

Barbara Haline Buss Baiak Open the ORCID record for Barbara Haline Buss Baiak [Opens in a new window] ,
Jennifer Mayara Gasparina ,
Letícia Ianke ,
Karolini Tenffen de Sousa ,
Matheus Deniz ,
Leticia Macedo Pereira ,
Jackson Victor Araújo ,
Raquel Abdallah da Rocha  and
João Ricardo Dittrich
Barbara Haline Buss Baiak*
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba, 80035-050, Paraná, Brazil
Jennifer Mayara Gasparina
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Estadual de Ponta Grossa, Ponta Grossa, 84030-900, Paraná, Brazil
Letícia Ianke
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Estadual de Ponta Grossa, Ponta Grossa, 84030-900, Paraná, Brazil
Karolini Tenffen de Sousa
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba, 80035-050, Paraná, Brazil
Matheus Deniz
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba, 80035-050, Paraná, Brazil
Leticia Macedo Pereira
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba, 80035-050, Paraná, Brazil
Jackson Victor Araújo
Affiliation:
Departamento de Veterinária, Universidade Federal de Viçosa, Viçosa, 36570-000, Minas Gerais, Brazil
Raquel Abdallah da Rocha
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Estadual de Ponta Grossa, Ponta Grossa, 84030-900, Paraná, Brazil
João Ricardo Dittrich
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba, 80035-050, Paraná, Brazil
*
Author for correspondence: Barbara Haline Buss Baiak E-mail: barbara_baiak@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Biological control is a strategy to decrease parasitic populations, and the action takes place through natural antagonists in the environment. We studied the predatory activity of the fungus Duddingtonia flagrans in infective larvae (L3) of gastrointestinal nematodes after gastrointestinal transit. Ten heifers were divided into two groups: treated (animals received pellets containing fungus) and control (animals received pellets without fungus). Twelve hours after administration, faeces samples were collected for in vitro efficacy tests. The animals then remained for 7 h in the experimental pasture area. At the end of this period, 20 faecal pads (ten treated and ten control) were selected at random. Pasture, faecal pad and soil collections occurred with an interval of 7 days, totalling four assessments. In vitro activity demonstrated that fungi effectively preyed on L3, achieving a reduction percentage of 88%. In the faecal pad of the pasture area, there was a difference (P < 0.05) between collections 3 and 4 for both groups; in the treated group a reduction of 65% was obtained, while in the control group there was an increase of 217% in the number of L3. The recovery of L3 in the soil and in the pasture was similar in both groups. There was no influence (P = 0.87) of the passage time on the fungus predatory activity. Duddingtonia flagrans demonstrated the ability to survive gastrointestinal transit in the animals, reducing the number of L3 in the faeces, indicating that this biological control has great potential in the control of worm infections.

Keywords

Biological controlheifersworms
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e31
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almeida, LR (2013) Manejo de parasitoses em sistema orgânico de produção de leite. Arquivos do Instituto Biológico 80, 129–134.CrossRefGoogle Scholar
Alvares, CA, Stape, JL, Sentelhas, PC, Moraes Gonçalves, JL and Sparovek, G (2013) Köppen's climate classification map for Brazil. Meteorologische Zeitschrift 22, 711–728. doi:10.1127/0941-2948/2013/0507CrossRefGoogle Scholar
Amarante, AFT (2014) Classe nematoda. pp. 13–97. In Os parasitas de ovinos [online]. São Paulo, Editora UNESP, ISBN 978-85-68334-42-3. Available from SciELO Books.CrossRefGoogle Scholar
Antonello, AM, Cezar, AS, Sangioni, LA and Vogel, FSF (2010) Contagens de ovos por grama de fezes para o controle anti-helmíntico em bovinos de leite de diferentes faixas etárias. Ciência Rural 40, 1227–1230. doi:10.1590/s0103-84782010005000067CrossRefGoogle Scholar
Araújo, JV, Assis, RCL, Campos, AK and Mota, MA (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 Veterinaria e Zootecnia 58, 373–380.CrossRefGoogle Scholar
Assis, RCL, Luns, FD, Araújo, JV, Braga, FR, Assis, RL, Marcelino, JL, 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. doi:10.1016/j.vetpar.2012.12.005CrossRefGoogle ScholarPubMed
Baiak, BHB, Lehnen, CR and Rocha, RA (2018) Anthelmintic resistance in cattle: A systematic review and meta-analysis. Livestock Science 217, 127–135. doi:10.1016/j.livsci.2018.09.022CrossRefGoogle Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–47. doi:10.18637/jss.v067.i01CrossRefGoogle Scholar
Bilotto, F, Fusé, LA, Sagües, MF, Iglesias, LE, Fernández, AS, Zegbi, S, et al. (2018) Predatory effect of Duddingtonia flagrans on infective larvae of gastro-intestinal parasites under sunny and shaded conditions. Experimental Parasitology 193, 27–32. doi:10.1016/j.exppara.2018.07.016CrossRefGoogle ScholarPubMed
Braga, FR and Araújo, JV (2014) Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Applied Microbiology and Biotechnology 98, 71–82. doi:10.1007/s00253-013-5366-zCrossRefGoogle ScholarPubMed
Braga, FR, Araújo, JV, Silva, AR, Araujo, JM, Carvalho, RO and Tavela, AO (2009) Biological control of horse cyathostomin (Nematoda: Cyathostominae) using the nematophagous fungus Duddingtonia flagrans in tropical southeastern Brazil. Veterinary Parasitology 163, 4.CrossRefGoogle ScholarPubMed
Braga, FR, Araújo, JV, Soares, FEF, Araujo, JM, Ferreira, SR, Frassy, LN and Queiroz, JH (2011) Production and partial characterization of Duddingtonia flagrans (AC001) crude extract and its in vitro larvicidal action against trichostrongylid infective larvae. Biocontrol Science and Technology 21, 1313–1320. doi:10.1080/09583157.2011.619258CrossRefGoogle Scholar
Braga, FR, Ferraz, CM, da Silva, EN and de Araújo, JV (2020) Efficiency of the Bioverm® (Duddingtonia flagrans) fungal formulation to control in vivo and in vitro of haemonchus contortus and strongyloides papillosus in sheep. Biotechnology 10, 62. doi: 10.1007/s13205-019-2042-8Google Scholar
Campos, AK, Araújo, JV and Guimarães, MP (2008) Interaction between the nematophagous fungus Duddingtonia flagrans and infective larvae of haemonchus contortus (Nematoda: Trichostrongyloidea). Journal of Helminthology 82, 337–341. doi:10.1017/S0022149X08032203CrossRefGoogle Scholar
Charles, TP, Santos, C. de P and Alvim, GP (1993) Atividade predatória de duas espécies de fungos nematófagos nos estágios de vida livre dos nematódeos trichostrongilídeos. Revista Brasileira de Parasitologia Veterinária 2, 46.Google Scholar
Duddington, CL (1955) Notes on the technique of handling predaceous fungi. Transactions of the British Mycological Society 38, 97–103.CrossRefGoogle Scholar
Faedo, M, Larsen, M, Dimander, SO, Yeates, GW, Höglund, J and Waller, PJ (2002) Growth of the fungus Duddingtonia flagrans in soil surrounding feces deposited by cattle or sheep fed the fungus to control nematode parasites. Biological Control 23, 64–70. doi:10.1006/bcon.2001.0987CrossRefGoogle Scholar
Fernandes, FM, Aguiar, AR, Costa Silva, LP, Senna, T, Mello, INK, Oliveira, T, et al. (2017) Biological control on gastrointestinal nematodes in cattle with association of nematophagous fungi. Biocontrol Science and Technology 27, 1445–1453. doi:10.1080/09583157.2017.1406063CrossRefGoogle Scholar
Geurden, T, Chartier, C, Fanke, J, Regalbono, AF, Traversa, D, von Samson-Himmelstjerna, G, et al. (2015) Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe. International Journal for Parasitology: Drugs and Drug Resistance 5, 163–171. doi:10.1016/j.ijpddr.2015.08.001Google ScholarPubMed
Gordon, HM and Whitlock, HV (1939) A technique for counting trematode eggs in sheep faeces. Journal of the Council for Scientific and Industrial Research 12, 50–52. doi:10.1017/S0022149X00019106Google Scholar
Hasanzadeh, M, Mohammadifar, M, Sahebany, N and Etebarian, HR (2012) Effect of cultural condition on biomass production of some nematophagous fungi as biological control agent. Egyptian Academic Journal of Biological Sciences. A, Entomology 5, 115–126. doi:10.21608/eajbsa.2012.14947Google Scholar
Healey, K, Lawlor, C, Knox, MR, Chambers, M and Lamb, J (2018) Field evaluation of Duddingtonia flagrans IAH 1297 for the reduction of worm burden in grazing animals: Tracer studies in sheep. Veterinary Parasitology 253, 48–54. doi:10.1016/j.vetpar.2018.02.010CrossRefGoogle Scholar
Jobim, MB, Santurio, JM and De La Rue, ML (2008) Duddingtonia flagrans: Controle biológico de nematodeos de bovinos a campo. Ciencia Rural 38, 2256–2263. doi:10.1590/S0103-84782008000800026CrossRefGoogle Scholar
Keith, RK (1952) The differentiation of the infective larvae of some common nematode parasites of cattle. Australian Journal of Zoology 1, 223–235.CrossRefGoogle Scholar
Knox, MR, Josh, PF and Anderson, LJ (2002) Deployment of Duddingtonia flagrans in an improved pasture system: Dispersal, persistence, and effects on free-living soil nematodes and microarthropods. Biological Control 24, 176–182. doi:10.1016/S1049-9644(02)00012-9CrossRefGoogle Scholar
Lacau-Mengido, IM, Mejía, ME, Díaz-Torga, GS, Gonzalez Iglesias, A, Formía, N, Libertun, C and Becú-Villalobos, D (2000) Endocrine studies in ivermectin-treated heifers from birth to puberty. Journal of Animal Science 78, 817–824. doi:10.2527/2000.784817xCrossRefGoogle ScholarPubMed
Mauad, J.R.C (2008) Eficácia dos fungos nematófagos Duddingtonia flagrans e Arthrobotrys robusta na profilaxia das infecções naturais por nematódeos gastrintestinais em ovinos. In: Tese (Doutorado em MedicinaVeterinária) Universidade Estadual Paulista, Botucatu, Brasil.Google Scholar
Mota, MDA, Campos, AK and Araújo, JV (2003) Controle biológico de helmintos parasitos de animais: Estágio atual e perspectivas futuras. Pesquisa Veterinaria Brasileira 23, 93–100. doi:10.1590/s0100-736 ( 2003000300001CrossRefGoogle Scholar
Nansen, P, Gronvold, J and Henriksen, SA (1986) Predacious activity of the nematode-destroying fungus Arthrobotrys oligospora, on preparasitic larvae of Cooperia oncophora and on soil nematodes. Proceedings of the Helminthological Society of Washington 53, 237–243.Google Scholar
Peña, MT, Miller, JE, Fontenot, ME, Gillespie, A and Larsen, M (2002) Evaluation of Duddingtonia flagrans in reducing infective larvae of haemonchus contortus in feces of sheep. Veterinary Parasitology 103, 259–265. doi:10.1016/S0304-4017(01)00593-3CrossRefGoogle ScholarPubMed
Pinheiro Machado, LC (2010) Pastoreio racional voisin: Tecnologia agroecológica para o terceiro milênio/luiz carlos pinheiro machado. 2nd edn. São Paulo, Extensão Popular, 376p.Google Scholar
Ravinet, N, Chartier, C, Bareille, N, Lehebel, A, Ponnau, A, Brisseau, N and Chauvin, A (2016) Unexpected decrease in milk production after fenbendazole treatment of dairy cows during early grazing season. PLoS One 11, 1–19. doi:10.1371/journal.pone.0147835CrossRefGoogle ScholarPubMed
R Core Team (2017) R: A language and environment for statistical com- puting. Vienna, Austria, R Foundation for Statistical Computing, https://www.R-project.org/.Google Scholar
Roberts, F and O'Sullivan, P (1950) Methods for egg counts and larval cultures for strongyles infesting the gastro-intestinal tract of cattle. Australian Journal of Agricultural Research 1, 99. doi:10.1071/ar9500099CrossRefGoogle Scholar
Sagüés, MF, Fusé, LA, Fernández, AS, Iglesias, LE, Moreno, FC and Saumell, CA (2011) Efficacy of an energy block containing Duddingtonia flagrans in the control of gastrointestinal nematodes of sheep. Parasitology Research 109, 707–713. doi:10.1007/s00436-011-2302-yCrossRefGoogle ScholarPubMed
Saumell, CA, Fernández, AS, Fusé, LA, Rodríguez, M, Sagüés, MF and Iglesias, LE (2015) Nematophagous fungi from decomposing cattle faeces in Argentina. Revista Iberoamericana de Micologia 32, 252–256. doi:10.1016/j.riam.2014.09.003CrossRefGoogle ScholarPubMed
Sciacca, J, Ketschek, A, Forbes, WM, Boston, R, Guerrero, J, Ashton, FT, et al. (2002) Vertical migration by the infective larvae of three species of parasitic nematodes: Is the behaviour really a response to gravity? Parasitology 125, 553–560. doi:10.1017/S0031182002002391CrossRefGoogle ScholarPubMed
Silva, ME, Araújo, JV, Braga, FR, Soares, FEF and Rodrigues, DS (2013) Control of infective larvae of gastrointestinal nematodes in heifers using different isolates of nematophagous fungi. Revista Brasileira de Parasitologia Veterinária 22, 78–83. doi:10.1590/s1984-29612013005000012CrossRefGoogle ScholarPubMed
Silveira, WF, Oliveira, GD, Braga, FR, Carvalho, LM, Domingues, RR, Silva, LA, et al. (2017) Predation rate of nematophagous fungi after passing through the gastrointestinal tract of goats. Small Ruminant Research 147, 101–105. doi:10.1016/j.smallrumres.2016.12.025CrossRefGoogle Scholar
Skinner, WD and Todd, KS (1980) Lateral migration of Haemonchus contortus larvae on pasture. American Journal of Veterinary Research 41, 395–398.Google ScholarPubMed
Staniland, LN (1954) A modification of the Baermann funnel technique for the collection of Nematodes from plant material. Journal of Helminthology 28, 115–118. doi:10.1017/S0022149X00032739CrossRefGoogle ScholarPubMed
Ueno, H and Gonçalves, PC (1998) Manual para diagnóstico das helmintoses de ruminantes. 4.ed, JICA, 166p.Google Scholar
Voisin, A., 2001. Productivité de l'herbe. France Agricole, Paris [1957].Google Scholar