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In vitro biological control of bovine parasitic nematodes by Arthrobotrys cladodes, Duddingtonia flagrans and Pochonia chlamydosporia under different temperature conditions

Published online by Cambridge University Press:  21 September 2020

Ítalo Stoupa Vieira*
Affiliation:
Laboratório de Parasitologia e Doenças Parasitárias, Departamento de Veterinária, Universidade Federal de Viçosa, Av. P.H Rolfs, s/n, Viçosa, Minas GeraisCEP 36570-900, Brazil
Isabela de Castro Oliveira
Affiliation:
Laboratório de Parasitologia e Doenças Parasitárias, Departamento de Veterinária, Universidade Federal de Viçosa, Av. P.H Rolfs, s/n, Viçosa, Minas GeraisCEP 36570-900, Brazil
Artur Kanadani Campos
Affiliation:
Laboratório de Parasitologia e Doenças Parasitárias, Departamento de Veterinária, Universidade Federal de Viçosa, Av. P.H Rolfs, s/n, Viçosa, Minas GeraisCEP 36570-900, Brazil
Jackson Victor de Araújo
Affiliation:
Laboratório de Parasitologia e Doenças Parasitárias, Departamento de Veterinária, Universidade Federal de Viçosa, Av. P.H Rolfs, s/n, Viçosa, Minas GeraisCEP 36570-900, Brazil
*
Author for correspondence: Ítalo Stoupa Vieira, E-mail: italosvieira@hotmail.com

Abstract

Variations in temperature can affect the development of nematophagous fungi, especially when they are used in the biological control of parasitic nematodes in the pastures where cattle are reared. The aim of this work was to evaluate the effects of temperature on the performance of nematophagous fungi in the biological control of bovine parasitic nematodes. The mycelial growth, chlamydospore production and nematicidal activity of Duddingtonia flagrans, Arthrobotrys cladodes and Pochonia chlamydosporia were evaluated at 15, 20, 25, 30 and 35°C. The fungal strains achieved mycelial growth, chlamydospore production and nematicidal activity on parasitic nematodes under all temperature conditions tested. The fungi showed higher growth at intermediate temperatures (20, 25 and 30°C) than at the extremes of 15 and 35°C. At 25 and 30°C, D. flagrans realized 96.8 and 94.5% nematicidal activity on bovine parasitic nematodes, respectively. Arthrobotrys cladodes effected nematicidal activity of 85.3 and 83.5%, at 20 and 25°C, respectively. At 20 and 30°C, P. chlamydosporia achieved nematicidal activity of 81.3 and 87.4%, respectively. The maximum chlamydospore production was reached at 20, 25 and 30°C for D. flagrans, at 20 and 25°C for A. cladodes and P. chlamydosporia. The results of this study demonstrated that the tested fungal strains of D. flagrans, A. cladodes and P. chlamydosporia, when used in the biological control of bovine parasitic nematodes, were not limited by in vitro temperature variations. Therefore, the use of these strains of fungi as biological control agents of parasitic nematodes is promising.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Braga, FR and Araújo, JV (2014) Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Applied Microbiology and Biotechnology 98, 7182.CrossRefGoogle ScholarPubMed
Braga, FR, Freitas Soares, FE, Araujo, JM, Fonseca, LA, Hiura, E and Garschagen Gava, M (2014) Statistical experimental design to assess the influence of enzymes of nematophagous fungi versus helminths. Research in Veterinary Science 97, 527532.CrossRefGoogle ScholarPubMed
Buske, R, Santurio, JM, Oliveira, CV, Bianchini, LA, Silva, JH and Rue, ML (2013) In vitro influence of temperature on the biological control activity of the fungus Duddingtonia flagrans against Haemonchus contortus in sheep. Parasitology Research 112, 473478.CrossRefGoogle Scholar
Carrillo-Inungaray, ML, Hidalgo-Morales, M, Rodríguez-Jimenes, GD, García-Alvarado, , Ramírez-Lepe, M, Munguìa, AR and Robles-Olvera, V (2014) Effect of temperature, pH and water activity on Penicillium digitatum growth. Journal of Applied Mathematics 2, 930937.Google Scholar
Fazzio, LE, Sánchez, RO, Streitenberger, N, Galvan, WR, Giudici, CJ and Gimeno, EJ (2014) The effect of anthelmintic resistance on the productivity in feedlot cattle. Veterinary Parasitology 206, 240245.CrossRefGoogle ScholarPubMed
Fernández, AS, Larsen, M, Wolstrup, J, Grønvold, J, Nansen, P and Bjørn, H (1999) Growth rate and trapping efficacy of nematode-trapping fungi under constant and fluctuating temperatures. Parasitology Research 85, 661668.Google ScholarPubMed
Gasbarre, LC (2014) Anthelmintic resistance in cattle nematódeos in the US. Veterinary Parasitology 204, 311.CrossRefGoogle Scholar
Grisi, L, Leite, RC, Martins, JRS, Barros, ATM, Andreotti, R, Cançado, PHD, León, AAP, Pereira, JB and Villela, HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Brazilian Journal of Veterinary Parasitology 23, 150156.Google ScholarPubMed
Grønvold, J, Nansen, P, Henriksen, SA, Larsen, M, Wolstrup, J, Bresciani, J, Rawat, H and Fribert, L (1996) Induction of traps by Ostertagia ostertagi larvae, chlamydospore production and growth rate in the nematode-trapping fungus Duddingtonia flagrans. Journal of Helminthology 70, 291297.CrossRefGoogle Scholar
INMET, Instituto Nacional de Meteorologia (2018) Normais Climatológicas do Brasil 1981–2010. Available at http://www.inmet.gov.br/portal/index.php?r=clima/normaisClimatologicas (accessed 25 March 2019).Google Scholar
Keith, RK (1953) The differentiation on the infective larvae of some common nematode parasites of cattle. Australian Journal of Zoology 1(2), 223235.CrossRefGoogle Scholar
Lasram, S, Oueslati, S, Valero, A, Marin, S, Ghorbel, A and Sanchis, V (2010) Water activity and temperature effects on fungal growth and ochratoxin a production by ochratoxigenic Aspergillus carbonarius isolated from Tunisian grapes. Journal of Food Science 75, 8997.CrossRefGoogle ScholarPubMed
Li, Y, Wadsö, L and Larsson, L (2009) Impact of temperature on growth and metabolic efficiency of Penicillium roqueforti – correlations between produced heat, ergosterol content and biomass. Journal of Applied Microbiology 106, 14941501.CrossRefGoogle ScholarPubMed
Mukhtar, T and Pervaz, I (2003) In vitro evaluation of ovicidal and larvicidal effects of culture filtrate of Verticillium chlamydosporium against Meloidogyne javanica. International Journal of Agriculture and Biology 5, 576579. Available at http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.319.239&rep=rep1&type=pdf (accessed 1 March 2019).Google Scholar
Muller, WH (1956) Influence of temperature on growth and sporulation of certain fungi. Botanical Gazette 117(4), 336343. Available at https://www.jstor.org/stable/2473142 (accessed 27 February 2019).CrossRefGoogle Scholar
Oliveira, JA (1991) Efeito do tratamento fungicida em sementes no controle de tombamento de plântulas de pepino (Cucumis sativas L.) e pimentão (Capsicum annanum L.). Dissertation, Escola Superior de Agricultura de Lavras.Google Scholar
Oliveira, IC, Carvalho, LM, Vieira, IS, Campos, AK, Freitas, SG, Araujo, JM, Braga, FR and Araújo, JV (2018a) Using the fungus Arthrobotrys cladodes var. macroides as a sustainable strategy to reduce numbers of infective larvae of bovine gastrointestinal parasitic nematódeos. Journal of Insect Pathology 158, 4651.CrossRefGoogle Scholar
Oliveira, IC, Vieira, IS, Carvalho, LM, Campos, AK, Freitas, SG, Araujo, JM, Braga, FR and Araújo, JV (2018b) Reduction of bovine strongilides in naturally contaminated pastures in the southeast region of Brazil. Experimental Parasitology 194, 915.CrossRefGoogle Scholar
Paz-Silva, A, Francisco, I, Valero-Coss, RO, et al. (2011) Ability of the fungus Duddingtonia flagrans to adapt to the cyathostomin egg-output by spreading chlamydospores. Veterinary Parasitology 79, 277282.CrossRefGoogle Scholar
Ranjbar-Bahadori, S, Rhazzagi-Abyaneh, M, Baya, M, Eslami, A, Pirali, K, Shams-Ghahfarokhi, M and Lotfollahzadeh, S (2010) Studies on the effect of temperature, incubation time and in vivo gut passage on survival and Nematophagous activity Arthrobotrys oligospora var. Oligospora and A. cladodes var. macroides. Global Veterinaria 4, 112117. Available at https://idosi.org/gv/gv4(2)10/3.pdf (accessed 1 March 2019).Google Scholar
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. Ciencia Rural 31, 839842.CrossRefGoogle Scholar
Silva, AR, Braga, FR, Araújo, JV, Benjamim, LA, Souza, DL and Carvalho, RO (2011) Comparative analysis of destruction of the infective forms of Trichuris trichiura and Haemonchus contortus by nematophagous fungi Pochonia chlamydosporia; Duddingtonia flagrans and Monacrosporium thaumasium by scanning electron microscopy. Veterinary Microbiology 147, 214219.CrossRefGoogle ScholarPubMed
Stroze, CT, Santiago, DC and Baida, FC (2013) Isolamento, caracterização e avaliação do potencial de fungos nematófagos no parasitismo de Meloidogyne javanica ‘in vitro’. Nematropica 43, 1823. Available at http://journals.fcla.edu/nematropica/article/download/82426/79460 (accessed 25 March 2019).Google Scholar
Van Ooij, C (2011) Fungal pathogenesis: hungry fungus eats nematode. Nature Reviews. Microbiology. 9, 766767.CrossRefGoogle ScholarPubMed
Vieira, ÍS, Oliveira, IC, Campos, AK and Araújo, JV (2019) Association and predatory capacity of fungi Pochonia chlamydosporia and Arthrobotrys cladodes in the biological control of parasitic helminths of bovines. Parasitology 146, 13471351.CrossRefGoogle ScholarPubMed
Yang, J, Liang, L, Li, J and Zhang, KQ (2013) Nematicidal enzymes from microorganisms and their applications. Applied Microbiology and Biotechnology 97, 70817095.CrossRefGoogle ScholarPubMed
Zare, R, Gams, W and Evans, HC (2001) A revision of Verticilium section Prostrata. V. The genus Pochonia, with notes on Rotiferophthora. Nova Hedwigia 73, 5158.Google Scholar
Zouhar, M, Douda, O, Novotny, D, Novakova, J and Mazakova, J (2010) Evaluation of the pathogenicity of selected nematophagous fungi. Czech Mycology 61, 139147. Available at http://www.czechmycology.org/_cm/CM61202.pdf (accessed 1 March 2019).CrossRefGoogle Scholar