Abstract
The tick Rhipicephalus microplus (Canestrini) is a major economic hurdle to the global livestock industry. The incorrect and indiscriminate control carried out by synthetic chemical compounds has contributed to the emergence of parasite resistance present today to many products available in the veterinary market. Effective, economically viable and potentially safe alternatives need to be investigated, including herbal medicine and biological control by entomopathogenic fungi. In this study, extracts from Achyrocline satureioides (Lam.) DC. obtained by extraction with solvents of different polarities associated and not associated with the entomopathogenic fungus Beauveria bassiana (Balsamo-Crivelli) Vuillemin were evaluated on different stages of the life cycle of R. microplus. The activity of plant extracts, fungus and their associations in ticks was analyzed in vitro through the adult immersion test, larval packet test and larval immersion test. The highest efficacy on engorged females (43.3%) was reached by the hexanic partition (ASh) at 5 mg/mL + fungus, reducing larval hatchability. ASh associated with B. bassiana also caused high mortality of larvae, reaching LC50 of 6.23 and 2.65 mg/mL in the packet and immersion tests, respectively. The results obtained showed that extracts, when used in combination with the fungus, have their action enhanced, reaching 100% mortality of larvae. Among the evaluated methodologies, it was observed that the larval immersion test allows better assessment, due to the time of contact with the larvae. The results obtained with A. satureioides associated with the fungus are considered promising and open new perspectives for future product development.
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Data Availability
The data sets analyzed during the current study are available from the corresponding author on reasonable request.
References
Barci LAG, Almeida JEM, Nogueira AHC, Prado AP (2009) Determination of LC 90 and LT 90 of IBCB66 Beauveria bassiana (Ascomycetes: Clavicipitaceae) isolate for Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) control. Rev Bras Parasitol Vet 18:34–39. https://doi.org/10.4322/rbpv.018e1006
Calabrese EJ (2005) Paradigm lost, paradigm found: The reemergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 138:378–411. https://doi.org/10.1016/j.envpol.2004.10.001
Chagas ACS, Barros LD, Cotinguiba F, Furlan M, Giglioti R, Oliveira MCS, Bizzo HR (2012) In vitro efficacy of plant extracts and synthesized substances on Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Parasitol Res 110:295–303. https://doi.org/10.1007/s00436-011-2488-z
Clinical and Laboratory Standards Institute (CLSI) (2008) Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi; Approved Standard, 2nd ed.; CLSI document M38-A2; CLSI: Wayne, PA, USA. https://clsi.org/media/1455/m38a2_sample.pdf
Dal Magro J, Renk MH, Garcia FRM, Yunes RA, Magro D (1998) Eficiência de repelentes à base de extratos de Achyrocline satureioides e Cucurbita pepo sobre simulídeos. XV Simpósio de Plantas Medicinais do Brasil, Águas de Lindóia. Anais do Congresso p.163
De Souza KCB, Schapoval EES, Bassani VL (2002) LC determination of favonoids: separation of quercetin, luteolin and 3-O-methylquercetin in Achyrocline satureioides preparations. J Pharmacol Biomed 28:771–777. https://doi.org/10.1016/s0731-7085(01)00693-8
Drummond RO, Ernest SE, Trevino JL, Gladney WJ, Graham OH (1973) Boophilus annulatus and Boophilus microplus: laboratory tests for insecticides. J Econ Entomol 66:130–133. https://doi.org/10.1093/jee/66.1.130
FAO (1971) Recommended methods for the detection and measurement of resistance of agricultural pests to pesticides. Tentative method for larvae of cattle ticks, Boophilus spp. FAO Method No. 7. FAO Plant Prot Bull 19:15–18. https://www.cabdirect.org/cabdirect/abstract/19711001927
Fernandes EKK, Bittencourt VREP (2008) Entomopathogenic fungi against South American tick species. Exp Appl Acarol 46:71–93. https://doi.org/10.1007/s10493-008-9161-y
Fernandes EKK, Bittencourt VREP, Roberts DW (2012) Perspectives on the potential of entomopathogenic fungi in biological control of ticks. Exp Parasitol 130:300–305. https://doi.org/10.1016/j.exppara.2011.11.004
George DR, Finn RD, Graham KM, Sparagano OAE (2014) Present and future potential of plant-derived products to control arthropods of veterinary and medical significance. Parasit Vectors 7:1–12. https://doi.org/10.1186/1756-3305-7-28
Islam MT, Omar DB (2012) Combined effect of Beauvera bassiana with neem on virulence of insect in case of two application approaches. J Anim Plant Sci 22:77–82. https://parasitesandvectors.biomedcentral.com/articles/https://doi.org/10.1186/1756-3305-7-28
Klafke G, Webster A, Dall Agnol B, Pradel E, Silva J, de La Canal LH et al (2017) Multiple resistance to acaricides in field populations of Rhipicephalus microplus from Rio Grande do Sul state, Southern Brazil. Ticks Tick Borne Dis 8(1):73–80. https://doi.org/10.1016/j.ttbdis.2016.09.019
Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: Back to the future. J Invertebr Pathol 132:1–41. https://doi.org/10.1016/j.jip.2015.07.009
Luckmann D(2013) Compatibilidade de produtos naturais comerciais a fungos entomopatogênicos e seletividade a Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). 2013; 69 f. Dissertação de Mestrado, Universidade Tecnológica Federal do Paraná, Pato Branco, PR, Brasil. http://bdtd.ibict.br/vufind/Record/UTFPR-12_b22857fec46d54c28f090e2e394ca7c7
Macêdo M, Consoli R, Grandi T, Dos Anjos A, De Oliveira A, Mendes N et al (1997) Screening of Asteraceae (Compositae) plant extracts for larvicidal activity against Aedes fluviatilis (Diptera: Culicidae). Mem Inst Oswaldo Cruz 92:565–570. https://doi.org/10.1590/S0074-02761997000400024
Matos RS, Oliveira PR, Britto LCM, de Paula LGF, Zeringota CSB, Oliveira Monteiro CM, Daemon E, Camargo-Mathias MI (2019) Thymol: effects on reproductive biology and Gene’s organ morphology in Rhipicephalus sanguineus sensu lato engorged females (Acari: Ixodidae). Ticks Tick Borne Dis 11(1):101308. https://doi.org/10.1016/j.ttbdis.2019.101308
Minho AP, Domingues LF, Gainza YA, Figueiredo A, Boligon AA, Domingues R, Chagas AC(2020) In vitro screening of plant extract on Haemonchus contortus and Rhipicephalus (Boophilus) microplus. J Essent Oil Res 32(3):269–278. https://doi.org/10.1080/10412905.2020.1746414
Mohan MC, Redoy NP, Devi UK, Kongara R, Sharma HC (2007) Growth and insect assays of Beauveria bassiana with neem to test their compatibility and synergism. Biocontrol Sci Technol 17:1059–1069. https://doi.org/10.1080/09583150701714551
Moraes CK, Schark A, Vainstein MH (2003) Regulation of extracellular chitinases and proteases in the entomophatology and acaricid Methahizium anisopliae. Curr Microbiol 46:205–2010. https://doi.org/10.1007/s00284-002-3863-x
Politi FAS, Figueira GM, Araújo AM, Sampieri BR, Camargo-Mathias MI, Szabó MPJ, Bechara GH, Santos LC, Vilegas W, Pietro RCLR (2012) Acaricidal activity of ethanolic extract from aerial parts of Tagetes patula L. (Asteraceae) against larvae and engorged adult females of Rhipicephalus sanguineus (Latreille, 1806). Parasit Vectors 295:1–11. https://doi.org/10.1186/1756-3305-5-295
Prette N, Monteiro AC, Garcia MV, Soares VE (2005) Patogenicidade de isolados de Beauveria bassiana para ovos, larvas e ninfas ingurgitadas de Rhipicephalus sanguineus. Ciência Rural 35:855–861. https://doi.org/10.1590/S0103-84782005000400017. https://www.scielo.br/j/cr/a/zydpDvtH9Fs
Rashid M, Rashid MI, Akbar H, Ahmad l, Hassan MAA, Ashraf K et al (2019) A systematic review on modelling approaches for economic losses studies caused by parasites and their associated diseases in cattle. Par 146:129–141. https://doi.org/10.1017/S0031182018001282
Reck J, Klafke GM, Webster A, Dall’Agnol B, Scheffer R, Souza UA et al (2014) First report of fluazuron resistance in Rhipicephalus microplus: A field tick population resistant to six classes of acaricides. Vet Parasitol 201(1–2):128–136. https://doi.org/10.1016/j.vetpar.2014.01.0127
Reis FS, Barros MC, Fraga EDC, Da Penha TA, Teixeira WC, Dos Santos ACG (2008) Ectoparasitos de pequenos mamíferos silvestres de áreas adjacentes ao rio Itapecuru e área de preservação ambiental do Inhamum, estado do Maranhão. Rev Bras Parasitol Vet 17:69–74
Retta D, Dellacassa E, Villamil J, Suárez SA, Bandoni AL (2012) Marcela, a promising medicinal and aromatic plant from Latin America: A review Ind Crops Prod. 38:27–38. https://doi.org/10.1016/J.INDCROP.2012.01.006
Ribeiro LP, Blume E, Bogorni PC, Dequech STB, Brand SC, Junges E (2012) Compatibility of Beauveria bassiana commercial isolate with botanical insecticides utilized in organic crops in southern Brazil. Biol Agric Hort 28:223–240. https://doi.org/10.1080/01448765.2012.735088
Rodríguez-Vivas RI, Pérez-Cogollo LC, Rosado-Aguilar JA, Ojeda-Chi MM, Trinidad-MartinezI, Miller RJ et al (2014) Rhipicephalus (Boophilus) microplus resistant to acaricides and ivermectin in cattle farms of Mexico. Rev Bras Parasitol Vet 23:113–122. https://doi.org/10.1590/s1984-29612014044
Rojas de Arias A, Ferro E, Inchausti A, Ascurra M, Acosta N, Rodriguez E et al (1995) Mutagenicity, insecticidal and trypanocidal activity of some Paraguayan Asteraceae. J Ethnopharmacol 45:35–41. https://doi.org/10.1016/0378-8741(94)01193-4
Sabatini GA, Kemp DH, Hughes S, Nari A, Hansen J (2001) Tests to determine LC50 and discriminating doses for macrocyclic lactones against the cattle tick, Boophilus microplus. Vet Parasitol 95:53–62. https://doi.org/10.1016/s0304-4017(00)00406-4
Santi L, Coutinho-Rodrigues CJB, Berger M, Klein LAS, De Souza EM, Rosa RL et al (2019) Secretomic analysis of Beauveria bassiana related to cattle tick, Rhipicephalus microplus, infection. Folia Microbiol (Praha) 64:361–372. https://doi.org/10.1007/s12223-018-0659-3
Saupe AC (2003) O chá de macela Achyrocline satureioides (Lam) D C no controle do pulgão verde Myzus persicae em cultivo protegido: uma alternativa aos agrotóxicos. Florianopolis,50 f. Dissertaçao (Mestrado em Agrossistemas) Centro de Ciências Agrarias, Universidade Federal de Santa Catarina. https://repositorio.ufsc.br/xmlui/handle/123456789/85142
Singh NK, Vemu B, Nandi A, Singh H, Kumar R, Dumka VK(2014) Laboratory assessment of acaricidal activity of Cymbopogon winterianus, Vitex negundo and Withania somnifera extracts against deltamethrin resistant Hyalomma anatolicum. Exp Appl Acarol 63:423–430. https://doi.org/10.1007/s10493-014-9791-1
Soares FB(2011) Impactos de inseticidas e fungicidas na densidade populacional de Beauveria bassiana no solo sob efeito da microbiota nativa. 82 f. Dissertação de Mestrado, Universidade Estadual Paulista, Jaboticabal, SP, Brasil. https://repositorio.unesp.br/bitstream/handle/11449/94876/soares_fb_me_jabo.pdf
Sousa LAD, Pires Junior HB, Soares SF, Ferri PH, Ribas P et al(2011) Potential synergistic effect of Melia azedarach fruit extract and Beauveria bassiana in the control of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in cattle infestations. Vet Parasitol 175:320–324. https://doi.org/10.1016/j.vetpar.2010.10.012
Southam CM, Ehrlich J(1943) Effects of Extract of western red-cedar heartwood on certain wood-decaying fungi in culture. Phytopathol 33:517–524. https://www.scienceopen.com/document?vid=9c2c5835-b6bf-4e77-8484-4a3ed6dadd6d
Sun M, Ren Q, Guan G, Li Y, Han X, Ma C et al (2013) Effectiveness of Beauveria bassiana sensu lato strains for biological control against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in China. Parasitol Int 62:412–415. https://doi.org/10.1016/j.parint.2013.04.008
Vasconcellos JSP, Fernandes F, Cadore GC, Ratzlaff FR, Felipetto LG et al (2018) Atividade acaricida de diferentes solventes sobre fêmeas ingurgitadas e larvas de Rhipicephalus microplus. Pesq Vet Bras 38:1125–1129. https://doi.org/10.1590/1678-5150-PVB-5410
Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Technol 17:553–596. https://doi.org/10.1080/09583150701309006
Acknowledgements
We thank to the National Council for Scientific and Technological Development (CNPq) for the scholarship granted (RRF), the School of Pharmaceutical Sciences of Araraquara (UNESP) and Embrapa Southeastern Livestock Unit for keeping the host donors by the project 20.18.03.017.00.02.002.
Funding
This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil), Process FAPESP N° 2018/14116-4 and in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.
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RRF: conceived and designed the experiments; performed the experiments; prepared the manuscript; YAG: provided support in collecting and identifying ticks, analyzing the data; AF: provided support in collecting and identifying ticks; RS: performed the experiment; ACSC: provided support in collecting and identifying ticks, analyzing the data, prepared the manuscript. RCLRP: conceived and designed the experiments; analyzing and interpreting data, prepared the manuscript, supervised the study. All authors read, agreed and approved the final manuscript.
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All procedures of the present study were approved by the Embrapa Pecuária Sudeste Ethics Committee on Animal Experimentation (CEUA process nº. 01/2019).
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Fantatto, R.R., Gainza, Y.A., Figueiredo, A. et al. The association of extracts of Achyrocline satureioides and the fungus Beauveria bassiana against the tick Rhipicephalus microplus. Exp Appl Acarol 87, 351–363 (2022). https://doi.org/10.1007/s10493-022-00736-5
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DOI: https://doi.org/10.1007/s10493-022-00736-5