Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T09:48:54.491Z Has data issue: false hasContentIssue false
  • English
  • Français

Predation of the fungus Duddingtonia flagrans on infective larvae of gastrointestinal nematodes from heifers in a silvopastoral system under shaded and sunny conditions

Published online by Cambridge University Press:  08 March 2022

Barbara Haline Buss Baiak Open the ORCID record for Barbara Haline Buss Baiak [Opens in a new window] ,
Karolini Tenffen de Sousa ,
Matheus Deniz ,
Jennifer Mayara Gasparina ,
Letícia Ianke ,
Leticia Macedo Pereira ,
Jackson Victor Araújo ,
Raquel Abdallah Rocha  and
João Ricardo Dittrich
Barbara Haline Buss Baiak*
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba80035-050, Paraná, Brazil
Karolini Tenffen de Sousa
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba80035-050, Paraná, Brazil
Matheus Deniz
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba80035-050, Paraná, Brazil
Jennifer Mayara Gasparina
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Estadual de Ponta Grossa, Ponta Grossa84030-900, Paraná, Brazil
Letícia Ianke
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Estadual de Ponta Grossa, Ponta Grossa84030-900, Paraná, Brazil
Leticia Macedo Pereira
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba80035-050, Paraná, Brazil
Jackson Victor Araújo
Affiliation:
Universidade Federal de Viçosa, Minas Gerais, Brazil
Raquel Abdallah Rocha
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Estadual de Ponta Grossa, Ponta Grossa84030-900, Paraná, Brazil
João Ricardo Dittrich
Affiliation:
Programa de Pós-graduação em Zootecnia, Departamento de Zootecnia, Universidade Federal do Paraná, Curitiba80035-050, Paraná, Brazil
*
Author for correspondence: B.H. Buss Baiak, E-mail: barbara_baiak@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The objective of this study was to evaluate the predatory activity of the nematophagous fungus Duddingtonia flagrans on infective larvae of gastrointestinal nematodes from dairy heifers in different conditions (shaded and sunny) of a silvopastoral system (SPS) on an agroecological farm. Ten Jersey heifers were divided into two groups: treated (received pellets containing fungus); and control (received pellets without fungus). Twelve hours after fungus administration, faeces samples were collected for in vitro efficacy tests. The animals then remained for 8 h in the experimental pasture area. At the end of this period, 20 faecal pads (10 treated and 10 control) were selected. Pasture, faecal pad and soil collections occurred at intervals of seven days (d), totalling four assessments over 28 d. To evaluate the influence of the conditions shaded and sunny, we registered the condition of the location of each faecal pad per hour. After 12 h of gastrointestinal transit in dairy heifers, a reduction of 65% was obtained through the in vitro test. The treated group presented a lower number of infective larvae (L3) in the faecal pad and upper pasture. Differences in numbers of L3 were observed between the conditions (sunny and shaded) in the faecal pad of the control group; while in the treated group there were no differences between the conditions. The predatory activity of the fungus was efficient over time in the shaded and sunny conditions of an SPS, decreasing the parasite contamination during the pasture recovery time in a subtropical climate.

Keywords

Biological controlcattlenematophagous fungiworms
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e20
Copyright
Copyright © The Author(s), 2022. 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

Alvares, CA, Stape, JL, Sentelhas, PC, et al. (2013) Köppen's climate classification map for Brazil. Meteorol Zeitschrift 22(6), 711–728.CrossRefGoogle Scholar
Araújo, JV, Assis, RCL, Campos, AK, et al. (2006) Efeito antagônico de fungos predadores dos gêneros Monacrosporium, Arthrobotrys e Duddingtonia sobre larvas infectantes de Cooperia sp. e Oesophagostomum sp [Antagonistic effect of predatory fungi of the genera Monacrosporium, Arthrobotrys and Duddingtonia on infective larvae of Cooperia sp. and Oesophagostomum sp]. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 58(3), 373–380. [In Portuguese.]CrossRefGoogle Scholar
Araújo, JV, Braga, FR, Mendoza-de-Gives, P, et al. (2021) Recent advances in the control of helminths of domestic animals by helminthophagous fungi. Parasitologia 1(3), 168–176.CrossRefGoogle Scholar
Baiak, BHB, Lehnen, CR and Rocha, RA (2018) Anthelmintic resistance in cattle: a systematic review and meta-analysis. Livestock Science 217, 127–135.CrossRefGoogle Scholar
Baiak, BHB, Gasparina, JM, Ianke, L, et al. (2021) Predatory activity of nematophagus fungus Duddingtonia flagrans in infective larvae after gastrointestinal transit: biological control in pasture areas and in vitro. Journal of Helminthology 95, e31.CrossRefGoogle ScholarPubMed
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1), 1–47.Google Scholar
Bilotto, F, Fusé, LA, Sagües, MF, et al. (2018) Predatory effect of Duddingtonia flagrans on infective larvae of gastro-intestinal parasites under sunny and shaded conditions. Experimental Parasitology 193(1), 27–32.CrossRefGoogle Scholar
Bowman, DD (2010) Georgis, parasitologia veterinária. 9th edn. Rio de Janeiro, Elsevier.Google 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(2), 62.Google Scholar
Braga, FR, Araújo, JV, Silva, AR, et al. (2009) Biological control of horse cyathostomin (Nematoda: Cyathostominae) using the nematophagous fungus Duddingtonia flagrans in tropical southeastern Brazil. Veterinary Parasitology 163(4), 335–340.Google Scholar
Buske, R, Santurio, JM, De Oliveira, CV, et al. (2013) In vitro influence of temperature on the biological control activity of the fungus Duddingtonia flagrans against Haemonchus contortus in sheep. Parasitology Research 112(2), 473–478.CrossRefGoogle ScholarPubMed
Deniz, M, Schmitt Filho, AL, Farley, J, et al. (2019) High biodiversity silvopastoral system as an alternative to improve the thermal environment in the dairy farms. International Journal of Biometeorology 63(1), 83–92.CrossRefGoogle Scholar
Deniz, M, Schmitt Filho, AL, Hötzel, MJ, et al. (2020) Microclimate and pasture area preferences by dairy cows under high biodiversity silvopastoral system in southern Brazil. International Journal of Biometeorology 64, 1877–1887.CrossRefGoogle ScholarPubMed
de Sousa, KT, Deniz, M, do Vale, MM, et al. (2021a) Influence of microclimate on dairy cows’ behavior in three pasture systems during the winter in south Brazil. Journal of Thermal Biology 97, 102873.CrossRefGoogle Scholar
de Sousa, KT, Deniz, M, Moro, MF, et al. (2021b) Developing of a model to predict lying behavior of dairy cows on silvopastoral system during the winter season. International Journal of Biometeorology 65(10).CrossRefGoogle Scholar
Deniz, M, de Sousa, KT, Gomes, IC, et al. (2021) Development and application of an autonomous data loggerto measure environmental variables in livestock farming. International Journal of Environmental Science and Technology, https://doi.org/10.1007/s13762-021-03734-z.CrossRefGoogle Scholar
Dias, AS, Araújo, JV, Campos, AK and Braga, FR (2007) Application of a formulation of the nematophagous fungus Duddingtonia flagrans in the control of cattle gastrointestinal nematodiosis. World Journal of Microbiology and Biotechnology 38, 1245–1252.CrossRefGoogle Scholar
Duddington, CL (1955) Notes on the technique of handling predaceous fungi. Transactions of the British Mycological Society 38(2), 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(1), 64–70.CrossRefGoogle Scholar
Gordon, HM and Whitlock, HV (1939) A technique for counting trematode eggs in sheep faeces. Journal of Council of Scientific and Industrial Research 12(1), 50–52.Google Scholar
Gronvold, J, Henriksen, SA, Larsen, M, Nansen, P and Wolstrup, J (1996) Biological control. Aspects of biological control—with special reference to arthropods, protozoans and helminths of domesticated animals. Veterinary Parasitology 64(1–2), 47–64.CrossRefGoogle Scholar
Keith, RK (1953) The differentiation of the infective larvae of some common nematode parasites of cattle. Australian Journal of Zoology 1(2), 223–235.CrossRefGoogle Scholar
Lettini, SE and Sukhdeo, MVK (2006) Anhydrobiosis increases survival of trichostrongyle nematodes. Journal of Parasitology 92(5), 1002–1009.CrossRefGoogle Scholar
Machado Filho, LCP (2011) Conceituando o ‘tempo ótimo de repouso’ em Pastoreio Racional Voisin [Conceptualizing the “‘optimal rest time”’ in Pastoreio Racional Voisin]. Cadernos de Agroecologia, 6(1), 1–2. [In Portuguese.]Google Scholar
Mauad, JRC (2008) Eficácia dos fungos nematófagos Duddingtonia flagrans e Arthrobotrys robusta na profilaxia das infecções naturais por nematódeos gastrintestinais em ovinos [Efficacy of nematophagous fungi Duddingtonia flagrans and Arthrobotrys robusta in the prophylaxis of natural infections by gastrointestinal nematodes in sheep]. Tese (Doutorado em MedicinaVeterinária) Universidade Estadual Paulista, Botucatu, Brazil. [In Portuguese.]Google Scholar
Novaes, SFD, Schreiner, LL, Silva, IP and Franco, RM (2017) Residues of veterinary drugs in milk in Brazil. Ciência Rural 47(8), 1–7.Google Scholar
Perissinoto, M, Moura, DJ, Cruz, VF, et al. (2009) Conforto térmico de bovinos leiteiros confinados em clima subtropical e mediterrâneo pela análise de parâmetros fisiológicos utilizando a teoria dos conjuntos fuzzy [Thermal comfort on subtropical and Mediterranean climate analysing some physiological data through fuzzy theory]. Ciência Rural 39(5), 1492–1498. [In Portuguese.]CrossRefGoogle Scholar
Pezzopane, JRM, Nicodemo, MLF, Bosi, C, et al. (2019) Animal thermal comfort indexes in silvopastoral systems with different tree arrangements. Journal of Thermal Biology 79, 103–111.CrossRefGoogle ScholarPubMed
Poppi, DP, Quigley, SP, da Silva, TACC and McLennan, SR (2018) Challenges of beef cattle production from tropical pastures. Revista Brasileira de Zootecnia 47.CrossRefGoogle Scholar
R Core Team (2021) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at https://www.R-project.org/, (accessed 10 August 2021).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(1), 99–102.Google Scholar
Rodrigues, JA, Alvares, FBV, Silva, JT, et al. (2020) Predatory effects of the fungus Arthrobotrys cladodes on sheep gastrointestinal nematodes. Biocontrol Science and Technology 30(8), 830–839.CrossRefGoogle Scholar
Rodrigues, JA, Roque, FL, Álvares, FBV, et al. (2021) Efficacy of a commercial fungal formulation containing Duddingtonia flagrans (Bioverm®) for controlling bovine gastrointestinal nematodes. Revista Brasileira de Parasitologia Veterinária 30, e026620.CrossRefGoogle ScholarPubMed
Santos, CP, Padilha, T and Rodrigues, MLA (2001) Predatory activity of Arthrobotrys Oligospora and Duddingtonia Flagrans on pre parasitic larval stages of cyathostominae under different constant temperatures. Ciência Rural 31(5), 839–842.CrossRefGoogle Scholar
Saumell, CA, Fernández, AS, Fusé, LA, et al. (2015) Nematophagous fungi from decomposing cattle faeces in Argentina. Revista Iberoamericana de Micologia 32(4), 252–256.CrossRefGoogle Scholar
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(1), 78–83.CrossRefGoogle Scholar
Skinner, WD and Todd, KS (1980) Lateral migration of Haemonchus contortus larvae on pasture. American Journal Of Veterinary Research 41(3), 395–398.Google Scholar
Staniland, LN (1954) A modification of the Baermann funnel technique for the collection of nematodes from plant material. Journal of Helminthology 28(1–2), 115–118.CrossRefGoogle Scholar
Sutherland, IA and Leathwick, DM (2011) Anthelmintic resistance in nematode parasites of cattle: a global issue? Trends of Parasitology 27(4), 176–181.CrossRefGoogle Scholar
Vieira, Í, Oliveira, I, Campos, A, et al. (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.CrossRefGoogle ScholarPubMed
Voisin, A (2001) Productivité de l'herbe [Grass productivity]. [1957]. Paris, France Agricole.[In French.].Google Scholar
Wu, D-K, Zhang, C-P, Zhu, C-Y, et al. (2013) Metabolites from carnivorous fungus Arthrobotrys entomopaga and their functional roles in fungal predatory ability. Journal of Agricultural and Food Chemistry 61(17), 4108–4113.CrossRefGoogle Scholar
Zhang, Z, Gasser, RB, Yang, X, et al. (2016) Two benzimidazole resistance-associated SNPs in the isotype-1 β-tubulin gene predominate in Haemonchus contortus populations from eight regions in China. International Journal for Parasitology: Drugs Drug Resistance 6(3), 199–206.Google Scholar
Supplementary material: File

Buss Baiak et al. supplementary material

Buss Baiak et al. supplementary material

Download Buss Baiak et al. supplementary material(File)
File 22.4 KB