Predatory activity of Butlerius nematodes and nematophagous fungi against Haemonchus contortus infective larvae

Atividade predatória de nematóides Butlerius e fungos nematófagos contra larvas infectantes de Haemonchus contortus

Manoel Eduardo da Silva Miguel Angel Mercado Uriostegui Jair Millán-Orozco Pedro Mendoza de Gives Enrique Liébano Hernández Fabio Ribeiro Braga Jackson Victor de Araújo About the authors

Abstract

The purpose of this study was to evaluate the predatory activity of the nematode Butlerius spp. and fungal isolates of Duddingtonia flagrans, Clonostachys rosea, Arthrobotrys musiformis and Trichoderma esau against H. contortus infective larvae (L3) in grass pots. Forty-eight plastic gardening pots containing 140 g of sterile soil were used. Panicum spp. grass seeds (200 mg) were sown into each pot and individually watered with 10 mL of tap water. Twelve days after seeding, the pots were randomly divided into 6 groups (n=8). Two thousand H. contortus infective larvae (L3) were added to each group. Additionally, the following treatments were established: Group 1 – 2000 Butlerius spp. larvae; group 2 – A. musiformis (1x107 conidia); group 3 – T. esau (1x107 conidia); group 4 – C. rosea (1x107 conidia), group 5 – D. flagrans (1x107conidia) and Group 6 – no biological controller (control group). The larval population of H. contortus exposed to Butlerius spp. was reduced by 61.9%. Population reductions of 90.4, 66.7, 61.9 and 85.7% were recorded in the pots containing A. musiformis, T. esau, C. rosea and D. flagrans, respectively. The results of this study indicate that the predatory nematode Butlerius spp. and the assessed fungi display an important predatory activity can be considered suitable potential biological control agents.

Keywords:
Biological control; nematodes; Duddingtonia flagrans; Clonostachys rosea; Arthrobotrys musiformis; Haemonchus contortus

Resumo

O objetivo deste estudo foi avaliar a atividade predatória do nematoide Butlerius spp. e isolados fúngicos de Duddingtonia flagrans, Clonostachys rosea, Arthrobotrys musiformis e Trichoderma esau contra larvas infectantes (L3) de Haemonchus contortus em vasos plantados com Panicum spp. Foram utilizados quarenta e oito potes plásticos de jardinagem contendo 140 g de solo estéril, 200 mg de sementes de Panicum spp.. Cultivar colonião, foi semeado em cada vaso e, diariamente, molhados com 10 mL de água da torneira. Doze dias após, os vasos foram divididos em 6 grupos (n = 8), e duas mil L3 de H. contortus foram adicionadas a cada vaso. Foram estabelecidos os seguintes tratamentos: Grupo 1 - 2.000 larvas de Butlerius spp.; Grupo 2 - A. musiformis (1x107 conídios); grupo 3 - T. esau (1x107 conídios); grupo 4 - C. rosea (1x107 conídios); grupo 5 - D. flagrans (1x107conidia); e Grupo 6 – somente L3 de H. contortus que serviu como controle negativo. A população de L3 de H. contortus expostas a Butlerius spp. foi reduzida em 61,9%. Redução populacional de 90,4, 66,7, 61,9 e 85,7% foram observadas nos vasos contendo A. musiformis, T. esau, C. rosea e D. flagrans, respectivamente. Os resultados deste estudo indicaram que o nematoide Butlerius spp. e os fungos avaliados exibiram importante atividade predatória e podem ser considerados como agentes de controle biológico.

Palavras-chave:
Controle biológico; nematóides; Duddingtonia flagrans; Clonostachys rosea; Arthrobotrys musiformis; Haemonchus contortus

Haemonchus contortus is considered one of the most important gastrointestinal parasitic nematodes due to its hematophagic habits and its high prevalence and pathogenicity (ROEBER et al., 2013Roeber F, Jex AR, Gasser RB. Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance - an Australian perspective. Parasit Vectors 2013; 6(1): 153. PMid:23711194. http://dx.doi.org/10.1186/1756-3305-6-153.
http://dx.doi.org/10.1186/1756-3305-6-15...
). Massive infections of this parasite cause the death of animals, especially young ones, which are more susceptible (GILLEARD, 2013Gilleard JS. as a paradigm and model to study anthelmintic drug resistance. Haemonchus contortusParasitology 2013; 140(12): 1506-1522. PMid:23998513. http://dx.doi.org/10.1017/S0031182013001145.
http://dx.doi.org/10.1017/S0031182013001...
). This and other parasites are normally controlled with chemical anthelmintic drugs (TAYLOR et al., 2013Taylor CM, Wang Q, Rosa BA, Huang SCC, Powell K, Schedl T, et al. Discovery of Anthelmintic Drug Targets and Drugs Using Chokepoints in Nematode Metabolic Pathways. PLoS Pathog 2013; 9(8): e1003505. PMid:23935495. http://dx.doi.org/10.1371/journal.ppat.1003505.
http://dx.doi.org/10.1371/journal.ppat.1...
). This method helps to reduce the parasitic burden in the animals, but it has some disadvantages, including the imminent emergence of anthelmintic resistance in the parasites (MÁRQUEZ-LARA, 2003Márquez-Lara D. Resistencia a los antihelmínticos: origen, desarrollo y control. Rev Corpoica 2003; 4(1): 55-71.; FORTES et al., 2013Fortes FS, Kloster FS, Schafer AS, Bier D, Buzatti A, Yoshitani UY, et al. Evaluation of resistance in a selected field strain of to ivermectin and moxidectin using the Larval Migration on Agar Test. Haemonchus contortusPesqui Vet Bras 2013; 33(2): 183-187. http://dx.doi.org/10.1590/S0100-736X2013000200008.
http://dx.doi.org/10.1590/S0100-736X2013...
). This situation a serious problem to animal health because it diminishes the efficacy of anthelmintics, and new reports of anthelmintic resistance are being recorded every year (KLAUCK et al., 2014Klauck V, Pazinato R, Lopes LS, Cucco DC, Lima HL, Volpato A, et al. and anthelmintic resistance in naturally infected sheep from southern Brazil. TrichostrongylusHaemonchusAn Acad Bras Cienc 2014; 86(2): 777-784. http://dx.doi.org/10.1590/0001-3765201420130061.
http://dx.doi.org/10.1590/0001-376520142...
).

Biological control using natural nematode antagonists has gained increasing attention in recent decades (WANG et al., 2014Wang W, Meng Q, Qiao J, Wang J, Yang L, Luo J, et al. Isolation of from soil of the Chinese Northern Tianshan Mountain slope pasture show predatory ability against larvae. Arthrobotrys oligosporaHaemonchus contortusBiocontrol Sci Technol 2014; 24(2): 170-179. http://dx.doi.org/10.1080/09583157.2013.853727.
http://dx.doi.org/10.1080/09583157.2013....
). Some species of the genus Trichoderma (Hypocreales, Hypocreaceae), which are considered important nematode bio-regulator, can be used on agricultural soils without causing environmental problems (MARTÍNEZ et al., 2013Martínez B, Infante D, Reyes Y. Trichoderma spp. y su función en el control de plagas en los cultivos. Rev Proteccíon Veg 2013; 28(1): 1-11.). Other genera/species of fungi such as Clonostachys rosea (Hypocreales, Bionectriaceae) are considered mycoparasites that produce invasive hyphae, nematicidal toxins and induce resistance in their hosts (SCHROERS, 2001Schroers HJ. A monograph of (Ascomycota, Hypocreales, Bionectriaceae) and its . BionectriaClonostachys anamorphsStud Mycol 2001; 46: 1-214.; COSTA et al., 2012Costa LB, Rangel DEN, Morandi MAB, Bettiol W. Impact of UV-B radiation on Clonostachys rosea germination and growth. World J Microbiol Biotechnol 2012; 28(7): 2497-2504. PMid:22806155. http://dx.doi.org/10.1007/s11274-012-1057-7.
http://dx.doi.org/10.1007/s11274-012-105...
).

On the other hand, the ascomycete Duddingtonia flagrans (Helotiales, Orbiliaceae) produces resistant resting spores (i.e., chlamydospores) that are able to survive after being orally administered to animals. Once these spores are expelled to the soil through the animal deposition’s, they germinate in situ and develop trapping devices that capture nematode larvae recently hatched from nematode eggs and eventually feed on them (MENDOZA-de-GIVES & TORRES-ACOSTA, 2012Mendoza-de-Gives P, Torres-Acosta F. Biotechnological use of Fungi in the control of ruminant parasitic nematodes. In: Arias MS, Paz-Silva A. Fungi: types, environmental impact and role in disease. New York: Nova Editorial; 2012. p. 389-408.). Recent studies have demonstrated that the use of sodium alginate pellets as a vehicle for D. flagrans and Monacrosporium thaumasium (Helotiales, Orbiliaceae) can be considered a suitable tool for the control of cattle parasites (SILVA et al., 2014Silva ME, Braga FR, Borges LA, Oliveira JM, Lima WS, Guimarães MP, et al. Evaluation of the effectiveness of Duddingtonia flagrans and in the biological control of gastrointestinal nematodes in female bovines bred in the semiarid region. Monacrosporium thaumasiumVet Res Commun 2014; 38(2): 101-106. PMid:24477840.). Arthrobotrys species (Helotiales, Orbiliaceae) are probably the most extensively studied nematophagous fungi worldwide. They show a remarkable ability to form three-dimensional adhesive traps that produce substances which paralyze nematodes, facilitating their capture and destruction (EPE et al., 2008Epe C, Holst C, Koopmann R, Schnieder T, Larsen M, von Samson-Himmelstjerna G. Investigation on the influence of nematophagous fungi as feed additive on nematode infection risk of sheep and goats on pasture. Agricul Forestry Res 2008; 58(3): 191-202.).

Butlerius spp. and other nematodes of the group Diplogasteridae are considered predators of nematode species (GAUGLER & BILGRAMI, 2004Gaugler R, Bilgrami AL. Feeding behaviour. In: Gaugler R, Bilgrami AL. Nematode behaviour. New Jersey: CABI Publishing, 2004. p. 91-126.). They inhabit decomposing organic matter, are prolific and resistant to adverse conditions, and are considered possible biological control agents of parasitic nematodes in nature (KHAN & KIM, 2007Khan Z, Kim HY. A review on the role of predatory soil nematodes in the biological control of plant parasitic nematodes. Appl Soil Ecol 2007; 35(2): 370-379. http://dx.doi.org/10.1016/j.apsoil.2006.07.007.
http://dx.doi.org/10.1016/j.apsoil.2006....
). The focus of this study was to evaluate the predatory activity of Butlerius spp. and different genera/species of nematophagous fungi, including D. flagrans, C. rosea, Arthrobotrys musiformis and T. esau in pots containing Panicum spp. grass against H. contortus infective larvae (L3) kept under outdoor conditions.

The following genera/species of nematophagous fungi were used: D. flagrans (FTHO-8 strain); A. musiformis (Am-1 strain) and T. esau (Te-1 strain). These three strains belong to the Centro Nacional de Investigación Disciplinaria – CENID - Parasitología Veterinaria, INIFAP collection, Mexico; while C. rosea (Yucatán strain) was provided by the Centro de Investigación Científica de Yucatán (CICY-CONACYT, Mexico). All the fungi were maintained on 2% water agar plates.

The Butlerius spp. strain (called Tres Marías strain) was used. This strain, which belongs to the CENID-PAVET-INIFAP collection in Jiutepec, Morelos, Mexico, was obtained from an area of undisturbed woodland near the village of Tres Marías in the state of Morelos, Mexico (LlERANDI-JUÁREZ & MENDOZA-DE-GIVES, 1998Llerandi-Juárez RD, Mendoza-de Gives P. Resistance of chlamydospores of nematophagous fungi to the digestive processes of sheep in Mexico. J Helminthol 1998; 72(2): 155-158. http://dx.doi.org/10.1017/S0022149X00016345.
http://dx.doi.org/10.1017/S0022149X00016...
).

A H. contortus strain originally obtained from a naturally infected sheep at “Las Margaritas” farm (Hueytamalco, Puebla, Mexico) was used. The infective larvae (L3) of this parasite were obtained from an egg donor sheep previously infected with the parasite LlERANDI-JUÁREZ & MENDOZA-DE-GIVES, 1998Llerandi-Juárez RD, Mendoza-de Gives P. Resistance of chlamydospores of nematophagous fungi to the digestive processes of sheep in Mexico. J Helminthol 1998; 72(2): 155-158. http://dx.doi.org/10.1017/S0022149X00016345.
http://dx.doi.org/10.1017/S0022149X00016...
). Thereafter, the donor animal was kept under suitable conditions to prevent further infection with gastrointestinal nematodes, GIN. Fecal cultures from this sheep were prepared in plastic containers and mixed with polystyrene particles and were maintained under laboratory conditions (26, 5ºC) for six days. Infective larvae were extracted from fecal cultures using the Baermann technique (VALCARCEL SANCHO, 2009Valcarcel Sancho, F. Atlas de parasitología ovina. España: S. L. Servet Diseño y Comunicación; 2009.) and identified according to the descriptions of Keith (1953)Keith RK. The differentiation of infective larvae of some common nematode parasites of cattle. Aust J Zool 1953; 1(2): 223-235. http://dx.doi.org/10.1071/ZO9530223.
http://dx.doi.org/10.1071/ZO9530223...
.

Forty-eight 90 x 65 mm plastic gardening pots were used. One hundred and forty grams of sterile (autoclaved) nursery soil were placed in each pot. Two hundred milligrams of commercial Panicum spp (colonião). grass seeds (containing approximately 50 seeds) were added to each pot and watered daily with 10 mL of tap water for 12 days. After the pots were filled with grown grass, they were randomly divided into six groups of 8 pots each, and 2000 H. contortus infective larvae were added to each pot.

The predatory microorganisms used in the present study were used into an aqueous suspension and they were sprayed on the experimental pots as follows: Group 1 – 2000 Butlerius spp. larvae; Group 2 – 1x107 A. musiformis conidia/chlamydospores; Group 3 – 1x107 T. esau conidia; Group 4 – 1x107 C. rosea conidia, and Group 5 – 1x107 D. flagrans chlamydospores; Group 6 – contained only the parasitic larvae and served as negative control. The pots were placed outdoors in an area of native grass, where they were exposed to the weather and watered daily with 10 mL of top water for 12 days. Meteorological data, i.e., ambient temperature, rainfall and relative humidity, were recorded.

After 12 days, the larvae were extracted from the entire content of each pot, using a Baermann funnel for 24 h, and were quantified. The results are expressed based on the mean number of live larvae recovered from each treatment. The larvae extracted from the control group were considered 100% live larvae, and were used to estimate the mortality rate.

The data were analyzed by ANOVA, the mean number of recovered larvae were compared among groups using the BioEstat 5.0 program, and Tukey test at P<0.05 was used as a complementary test.

Table 1 lists the mean and standard deviation of the number of H. contortus L3 recovered from the pots, and the percent reduction in the larvae population attributable to the nematode-predatory nematode Butlerius and to the different genera/species of nematophagous fungi. The results indicate that the 61.9% reduction in the H. contortus larvae population is attributable to the predatory activity of Butlerius spp. The nematophagous fungi showed the following population reductions: A. musiformis (90.4%), T. esau (66.7%), C. rosea (61.9%) and D. flagrans (85.7%) (p<0.05). No statistical difference was found in the predatory activity of the different nematode antagonists (p>0.05). The following meteorological data were recorded during the experiment: Temperature 23.6ºC (16-32ºC), relative humidity 53% (27.2-68.9%) and average daily rainfall 6.4 mm. These environmental conditions are favorable for good larval development (HERNÁNDEZ, 2011Hernández EL. Ecología de larvas de nematodos gastrointestinales de bovinos, ovinos y caprinos. In: Romero EQ, Castillo JAF, Velarde FI, Arellano MEL, editors. Epidemiología de enfermedades parasitarias en animales domésticos. México: Inifap, 2011. p. 254-272.) and also for nematophagous fungi (DHINGRA & SINCLAIR, 2005Dhingra OD, Sinclair JB. Basic plant pathology methods. 2nd ed. Boca Raton: CRC Press, 2005.). The highest fungal efficacy (90.4%) was exhibited by A. musiformis. Assessing the predatory capability of predatory nematodes i.e., Butlerius sp. and nematophagous fungi like the ones used in the present study is crucial to future works focused to find an sustainable alternative method of control that helps to reduce the nematode populations like H. contortus and perhaps other parasites of importance in the sheep and goat industry. This result is similar to that found by Graminha et al. (2005)Graminha EBN, Monteiro AC, Silva HC, Oliveira GP, Costa AJ. Controle de nematóides parasitos gastrintestinais por em ovinos naturalmente infestados mantidos em pastagens. Arthrobotrys musiformisPesq Agropec Bras 2005; 40(9): 927-933. http://dx.doi.org/10.1590/S0100-204X2005000900013.
http://dx.doi.org/10.1590/S0100-204X2005...
, who reported a 94.4% reduction in H. contortus larvae in sheep feces using a local strain of A. musiformis from Brazil.

Table 1
Mean and standard deviation of Haemonchus contortus infective larvae (L3) recovered from Panicum spp. grass pots after 12 days of interaction with Butlerius spp. and with different nematophagous fungi kept outdoors, and percent reduction caused by the different antagonists of nematodes.

Acevedo-Ramírez et al. (2011)Acevedo-Ramírez PMC, Quiroz-Romero H, Valero-Coss RO, Mendoza-de-Gives P, Gómez JL. Nematophagous fungi from Mexico with activity against the sheep nematode Haemonchus contortus.Rev Ibero-Latinoam Parasitol 2011; 70(1): 101-108. also reported 50% reduction in H. contortus larvae in vitro, using a Mexican strain of A. musiformis. On the other hand, Chauhan et al. (2005)Chauhan JB, Sanyal PK, Subramanian RB. The nematode-trapping efficacy of two chlamydospore-forming fungi against in sheep. Haemonchus contortusJ Helminthol 2005; 79(4): 315-319. PMid:16336714. http://dx.doi.org/10.1079/JOH2005291.
http://dx.doi.org/10.1079/JOH2005291...
observed that A. musiformis and D. flagrans significantly reduced the population of H. contortus larvae in feces after it was orally administered to sheep and passed through the gastrointestinal tract. Similarly, D. flagrans chlamydospores reduced the larvae population of trichostrongylidae by 95% after passing through the gastrointestinal tract of sheep (CRUZ et al., 2008Cruz DG, Cordeiro RC, Lopes AJ, Rocha LV, Santos CP. Comparison of the efficacy of different isolates of the nematode-trapping fungi spp. and . ArthrobotrysDuddingtonia flagrans in reducing infective larvae of nematodes after passage through the digestive tract of sheepRev Bras Parasitol Vet 2008;17(Suppl 1): 133-137. PMid:20059832.).

Nematophagous fungi are also being assessed against plant-parasitic nematodes, i.e., 85% reduction rates of Meloidogyne javanica (J2) in tomato plants using Arthrobotrys sp., and 25% reduction in egg viability and 74% reduction in J2 have been recorded using Trichoderma harzianum (JAMSHIDNEJAD et al., 2013Jamshidnejad V, Sahebani N, Etebarian H. Potential biocontrol activity of Arthrobotrys oligospora and Trichoderma harzianum BI against on tomato in the greenhouse and laboratory studies. Meloidogyne javanicaArch Phytopathol Plant Protect 2013; 46(13): 1632-1640. http://dx.doi.org/10.1080/03235408.2013.778476.
http://dx.doi.org/10.1080/03235408.2013....
). On the other hand, the C. rosea strain used in this study led to a 61.9% reduction in H. contortus larvae (L3), which is similar to the results reported by Jiménez (personal communication by Jiménez, S.R., 2013), who found reduction rates of 84.2 and 59.5% by C. rosea (Yucatán strain) and Clonostachys sp. (Campeche strain), respectively. Similar results were reported by Baloyi et al. (2011)Baloyi MA, Laing MD, Yobo KS. Isolation and in vitro screening of Bacillus thuringiensis and as biological control agents against sheep nematodes. Clonostachys roseaAfr J Agric Res 2011; 6(22): 5047-5054., who recorded reduction rates of 69.9 and 89.3% in the number of trichostrongylidae larvae using two C. rosea strains. In another study involving sheep feces and water, reduction rates of 71.9, 94.7, 92.7, 100 and 87.7% were recorded for Rhabditis sp., C. elegans, P. redivivus, Butlerius sp. and H. contortus, respectively (personal communication by Martínez, R.R., 2011).

The main prerequisite for the use of biocontrol agents is without doubt their ‘ability to colonize the external environment in large amounts’, and to provide an environmental decrease in the infecting free forms of target nematodes (BRAGA & ARAÚJO, 2014Braga FR, Araújo JV. Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Appl Microbiol Biotechnol 2014; 98(1): 71-82. PMid:24265027. http://dx.doi.org/10.1007/s00253-013-5366-z.
http://dx.doi.org/10.1007/s00253-013-536...
). In this sense, the predatory nematode Butlerius spp., as well as the different nematophagous fungi assessed here, namely, A. musiformis, T. esau, C. rosea and D. flagrans, reduced the population of infective H. contortus larvae in gardening pots maintained under outdoor conditions. This study provides evidence of the predatory activity of the nematode-predatory nematode Butlerius spp. and of four nematophagous fungi strains in reducing the H. contortus (L3) population in Panicum spp. grass pots under outdoor conditions. These organisms can therefore be considered potential candidates for the biological control of sheep haemonchosis in further studies.

Acknowledgements

The authors wish to thank Dr. Anwar L. Bilgrami of the Department of Mosquito Control, USDA, Maryland, USA for his values support in the taxonomic identification of Butlerius spp. and Dr. Marcela Gamboa of CICY-Yucatán, Mexico for kindly providing the Clonostachys rosea strain used in this study. The authors also acknowledge the Brazilian research funding agencies CNPq (National Council for Scientific and Technological Development), CAPES (Federal Agency for the Support and Improvement of Higher Education) FAPEMIG (Minas Gerais State Research Foundation) and FAPES (Espirito Santo Sate Research Foundation) for their financial support and award of a grant

References

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    » http://dx.doi.org/10.1016/j.apsoil.2006.07.007
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    » http://dx.doi.org/10.1590/0001-3765201420130061
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    » http://dx.doi.org/10.1017/S0022149X00016345
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Publication Dates

  • Publication in this collection
    26 Jan 2017
  • Date of issue
    Jan-Mar 2017

History

  • Received
    21 June 2016
  • Accepted
    23 Aug 2016
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br