Control of Rhipicephalus microplus (Acari: Ixodidae) using the entomopathogenic fungi Metarhizium anisopliae (Hypocreales: Clavicipitaceae). Review;Control de Rhipicephalus microplus (Acari: Ixodidae) mediante el uso del hongo entomopatógeno Metarhizium anisopliae (Hypocreales: Clavicipitaceae). Revisión

Revista Mexicana De Ciencias Pecuarias

Volumn 2, Issue 2, 2011, Pages 177-192

  Ojeda Chi, Melina Maribel ^a   Rodríguez Vivas, Roger Ivan ^a   Galindo Velasco, Edelmira ^b   Lezama Gutiérrez, Roberto ^b   Cruz Vázquez, Carlos ^c  

^a UNIVERSIDAD AUTÓNOMA DE YUCATÁN   (Mexico)

^b UNIVERSIDAD DE COLIMA   (Mexico)

^c Instituto Tecnologico El Llano   (Mexico)

Author keywords

Biological control; Fungi; Metarhizium anisopliae; Rhipicephalus (Boophilus) microplus

Indexed keywords

ACARI; ANAPLASMA MARGINALE; BABESIA BOVIS; BOOPHILUS; BOOPHILUS BIGEMINA; BOOPHILUS MICROPLUS; BOS; CLAVICIPITACEAE; FUNGI; HYPOCREALES; IXODIDA; IXODIDAE; METARHIZIUM ANISOPLIAE; RHIPICEPHALUS;

EID: 80555135987     PISSN: 20071124     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (74)

1. Rodríguez-Vivas RI, Quiñones AF, Fragoso SH. Epidemiología y control de la garrapata Boophilus en México. En: Enfermedades de importancia económica en producción animal. Rodríguez-Vivas RI editor. México DF: McGraw-Hill-UADY; 2005:571-592.
2. Alonso-Díaz MA, Rodríguez-Vivas RI, Fragoso-Sánchez H. Resistencia de la garrapata Boophilus microplus a los ixodicidas. Arch Med Vet 2006;38:105-113. (Pubitemid 44893740)
3. Rodríguez-Vivas RI, Alonso-Díaz MA, Rodríguez- Arévalo F, Fragoso-Sánchez H, Santamaria VM, Rosario-Cruz R. Prevalence and potential risk factors for organophosphate and pyrethroid resistance in Boophilus microplus ticks on cattle ranches from the State of Yucatan, Mexico. Vet Parasitol 2006;136:335-342.
4. Kay BH, Kemp H. Vaccines against arthropods. Am J Trop Med 1994;50:87-96. (Pubitemid 24225779)
5. Samish M, Ginsberg H, Glazer I. Biological control of ticks. Parasitol 2004;129:S389-S403. (Pubitemid 40780703)
6. Dantygni P, Nanguy S. Significance of the physiological state of fungal spores. Int J Food Microbiol 2009;134:16-20.
7. Frazzon GAP, Vaz Jr SI, Masuda A, Schrank A, Vainstein HM. In vitro assessment of Metarhizium anisopliae isolates to control the cattle tick Boophilus microplus. Vet Parasitol 2000;94:117-125.
8. Polar P, Aquino M, Kairo M, Moore D, Pegram S, John S. Thermal Characteristics of Metarhizium anisopliae isolates important for the development of biological pesticides for the control on cattle ticks. Vet Parasitol 2005;3:159-167. (Pubitemid 41539749)
9. Alonso-Díaz MA, García L, Galindo-Velasco E, Lezama-Gutiérrez R, Angel-Sahagún C, Rodríguez-Vivas RI, Fragoso-Sánchez H. Evaluation of Metarhizium anisopliae (Hyphomycetes) for the control of Boophilus microplus (Acari: Ixodidae) on naturally infested cattle in the Mexican tropics. Vet Parasitol 2007;147:336-340. (Pubitemid 46938622)
10. Ojeda-Chi MM, Rodriguez-Vivas RI, Galindo-Velasco E, Lezama-Gutierrez R. Laboratory and field evaluation of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) for the control of Rhipicephalus microplus (Acari: Ixodidae) in the Mexican tropics. Vet Parasitol 2010;170:348-354.
11. Barker SC, Murrell A. Systematic and evolution of ticks with a list of valid genus and species names. Parasitol 2004;129:15-36.
12. Estrada-Peña A, Venzal M. High resolution predictive mapping for Boophilus annulatus and Boophilus microplus (Acari:Ixodidae) in Mexico and Southern Texas. Vet Parasitol 2006;142:350-358. (Pubitemid 44750385)
13. Murrell A, Campbell JH, Barker SC. Phylogenic analysis of the Rhipicephalian ticks indicates that the genus Rhipicephalus is paraphiletic. Mol Phylog Evol 2000;16:1-7. (Pubitemid 30466872)
14. Núñez J. Taxonomía y ciclo biológico de Boophilus microplus. En: Nari A, Fiel C. editores. Enfermedades parasitarias de importancia económica en bovinos. Bases epidemiológicas para su prevención y control. Montevideo, Uruguay: Editorial Hemisferio Sur; 1994:289-299.
15. Taylor M, Coop MA, Wall RL. Veterinary parasitology. Third ed. London, UK: Blackwell Publishing; 2007.
16. Jonsson N. The productivity effects of cattle tick (Boophilus microplus) infestation on cattle, with particular reference to Bos indicus cattle and their crosses. Vet Parasitol 2006;137:1-10. (Pubitemid 43384021)
17. Pruett JH. Immunological control of arthropod ectoparasites a review. Int J Parasitol 1999;29:255-258.
18. Taylor MA. Recent developments in ectoparasiticides. Vet J 2001;61:253-268. (Pubitemid 32531763)
19. George JE, Pound JM, Davey RB. Chemical control of ticks on cattle and the resistance of these parasites to acaricides. Parasitol 2004;129:S353-S366. (Pubitemid 40780701)
20. Aguilar-Tipacamu G, Rodríguez-Vivas RI. Effect of moxidectin against natural infection of the cattle tick Boophilus microplus (Acari:Ixodidae) in the Mexican Tropics. Vet Parasitol 2003;111:211-216. (Pubitemid 36071553)
21. Rodríguez-Vivas RI, Arieta-Román JR, Perez-Cogollo LC, Rosado-Aguilar JA, Ramírez-Cruz GT, Basto-Estrella G. Uso de lactonas macrocíclicas para el control de la garrapata Rhipicephalus (Boophilus) microplus en el ganado bovino [en prensa]. Arch Med Vet 2010;(42).
22. Rodríguez-Vivas RI, Rodríguez-Arevalo F, Alonso-Díaz MA, Fragoso-Sánchez H, Santamaría VM, Rosario-Cruz R. Amitraz resistance in Boophilus microplus ticks in cattle farms from the state of Yucatan, Mexico: Potential risk factors. Prev Vet Med 2006;75:280-286.
23. Rodríguez-Vivas RI, Rivas AL, Chowell G, Fragoso SH, Rosario CR, García Z, Smith SD, Williams JJJ, Schwager, SJ. Spatial distribution of acaricide profiles Boophilus microplus strains susceptible or resistant to acaricides) in south eastern Mexico. Vet Parasitol 2007;146:158-169. (Pubitemid 46553772)
24. Miller RJ, Almazán GC, Estrada OM, Davey RB, George JE, A survey for fipronil-and-ivermectin-resistant Rhipicephalus (Boophilus) microplus collected in northern Mexico and the options for the management of acaricide-resitant ticks with pesticides. En: García VZ editor. VI Seminario Internacional de Parasitología. Impacto de las enfermedades parasitarias sobre la ganadería globalizada. INIFAP-INFARVET-AMPAVE- CNGUV. Veracruz, México. 2008.
25. Perez-Cogollo LC, Rodriguez-Vivas RI, Ramirez-Cruz GT, Miller RJ. First report of the cattle tick Rhipicephalus microplus resistant to ivermectin in Mexico. Vet Parasitol 2010;168:165-169.
26. FAO. Guidelines resistance management and integrated parasite control in ruminants. 2004; Module 1:56.
27. Da Silva I, Pohl P, De Freitas D. Caracterización de resistencia para acaricidas en garrapatas B. microplus. Acta Sci Vet 2005:109-117.
28. Kaaya GP, Hassan S. Entomogenous fungi as promising biopesticides for tick control. Exp Appl Acarol 2000;24:913-926. (Pubitemid 32382680)
29. López LlR, Galindo VE, Ángel SCA, Lezama GR, Silva AJM, López LM. Susceptibilidad de adultos de la mosca del cuerno Haematobia irritans (Díptera: Muscidae) a diversos aislados del hongo Metarhizium anisopliae (Hypomycetes). Congreso Nacional de Parasitología Veterinaria, Colima, México. INIFAPIndustria Farmacéutica Mexicana. 2004
30. Polar P, Moore D, Kairo M, Ramsubhag A.Topically applied myco-acaricides for the control of cattle ticks: overcoming the challenges. Exp Appl Acarol 2008;46:119-148.
31. Ferron P. Biological control of insect pests by entomogenous fungi. Rev Entomol 1978;23:409-442.
32. Biscoff JF, Rehener SA, Humber RA. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycol 2009;101:512-530.
33. Tulloch M. The genus Metarhizium. Trans Brit Mycol Soc 1976;66:407-411.
34. Driver F, Milner RJ, Trueman JWH. A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycol Res 2000;104:134-150. (Pubitemid 30446014)
35. Rath AC, Worledge D, Koen TB, Rowe BA. Long-term field efficacy of the entomogenous fungus, Metarhizium anisopliae against the subterranean scarab, Adoryphorus couloni. Biocontr Sci Technol 1995;5:439-451. (Pubitemid 3011245)
36. Soares GG, Marchal M, Ferron P. Susceptibilibly of Otiorhynchus sulcatus (Coleoptera:Curculionidae) larvae to Metarhiz ium anisopliae and Metarhizum flavoviridae (Deuteromycotina: Hyphomycetes) at two different temperatures. Environ Entomol 1993;12:1887-1891.
37. Humbert RA. Evolution of entomopathogenicity in fungi. J Invertebr Pathol 2008;98:262-266.
38. Kurtti T, Keyhani N. Intracellular infection of tick cell lines by the entomopathogenic fungus Metarhizium anisopliae. Microbiol 2008;154:1700-1709.
39. Li J, Feng M. Intraspecific tolerance of Metarhizium anisopliae conidia to the upper thermal limits of summer with a description of a quantitative assay system. Mycol Res 2009;113:93-99.
40. Arruda, W, Lübeck I, Achrank IA, Henning M. Morphological alterations of Metarhizium anisopliae during penetration of Boophilus microplus ticks. Exp Appl Acarol 2005;37:231-244. (Pubitemid 41739991)
41. Bittencourt VREP, Mascarenhas A, Horacio J. Mecanismo de infecção do fungo Metarhizium anisopliae no carrapato Boophilus microplus em condições experimentais. Ciência Rural 1999;29:351-354.
42. Silva W, Santi L, Berger M, Pinto A, Guimaraes J, Schrank A, Vaintein M. Characterization of a spore surface lipase from the biocontrol agent Metarhizium anisopliae. Proc Biochem 2009;34:829-834.
43. Fang W, Pava-ripoll MS, Wang S, Leger R. Protein kinase A regulates production of virulence determinants by the entomopathogenic fungus, Metarhizium anisopliae. Fung Genet Biol 2009;46:277-285.
44. Kaaya GP, Kokwaro ED, Seshu-Reddy KV, Munyinyi DM. Pathogenicity of Beauveria bassiana, Metarhizium anisopliae and Serratia marcencens to the banana weevil, Cosmopolites sordidus. Biocontrol Sci Technol 1993;3:177-183.
45. Asaff AT, Reyes VY, López EV, De la Torre M. Guerra entre insectos y microorganismos: una estrategia natural para el control de plagas. Avance y Perspectiva 2002;21:912.
46. Smith KE, Wall R, Berriatua E, French NP. The use of entomopathogenic fungi for the control of parasitic mites Psorotes spp. Vet Parasitol 2000;92:97-105. (Pubitemid 30628543)
47. Kaaya GP, Mwaigi E, Ouna E. Prospect for biologycal control of lives tock ticks, Rhipicephalus appendiculitatus and Amblyomma variagatum, using the entomogenous fungi Beauveria bassiana and Metarhizium anisopliae. J Invertebr Pathol 1996;67:15-20. (Pubitemid 126315841)
48. Skrobek B, Défago D, Butt G, Maurhofer M. Evaluation of different biological test systems to assess the toxicity of metabolites from fungal biocontrol agents. Toxicol Lett 2005;30:1-10.
49. Leyva CG, Galindo EV, Ángel SCA, Lezama GR, López LM, López LLR, Silva AJN, Neptalí J, Rebolledo DO, Molina OJ, Casillas MR. Pruebas de inocuidad del hongo entomopatógeno Metarhizum anisopliae cepa Ma2 (Deuteromycotina: Hyphomycetes) en rata blanca cepa wistar. Congreso Nacional de Parasitología Veterinaria. Colima, México: INIFAP, Industria Farmacéutica Mexicana. 2004.
50. Goettel MS, Johnson DL. Environmental impact and safety of fungal biocontrol agents, In: Biological control of Locusts and Grasshoppers, Lomer CJ, Prior C editors. CAB International, Wallingford, UK. 1992:356-361.
51. Rath AC, Koen TB, Anderson GC. Field evaluation of the entomogenous fungus, Metarhizium anisopliae (DAT F-001) as a biocontrol agent for the redheaded pasture Cockchafer, Adoryphorus couloni (Coleoptera: carabaeidae). Aust J Agric Res 1995;46:429-440. (Pubitemid 26449532)
52. Fernandes ED, Bittencourt VREP. Entomopathogenic fungi against South American tick species. Exp Appl Acarol 2008;46:71-93.
53. Bidochka MJ, Kamp AM, Lavender TM, Dekoning J, De Croos JNA. Habitat association in two genetic groups of the insect athogenic fungus Metarhizium anisopliae: Uncovering cryptic species? Appl Environ Microbiol 2001;67:1335-1342. (Pubitemid 33643579)
54. Lubekc I, Arruda W, Souzabk, Staniscuaski F, Carlini CR, Schrank A, Vainstein MH. Evaluation of Metarhizium anisopliae strains as potential biocontrol agents of the tick Rhipicephalus (Boophilus) microplus and the cotton stainer Dysdercus peruvianus. Fungal Ecol 2008;1:78-88.
55. Bahiense TC, Fernandes EKK, Bittencourt VREP. Compatibility of the fungus Metarhizium anisopliae and deltamethrin to control a resistant strain of Boophilus microplus tick. Vet Parasitol 2006;141:319-324. (Pubitemid 44528121)
56. Fernández-Ruvalcaba M, Zihoua E, García-Vázquez Z. Infectividad de Metarhizium anisopliae en contra de cepas de garrapata Boophilus microplus sensibles y resistentes a organofosforados. Tec Pecu Mex 2005;43:433-440.
57. Braga GU, Flint SD, Miller CD, Anderson AJ, Roberts DW. Both solar UVA and UVB radiation impair conidial culturability and delay germination in the entomopathologenic fungus. Photochem Photobiol 2001;74:734-739.
58. Ángel-Sahagún CA, Lezama-Gutiérrez R, Molina-Ochoa J, Pescador-Rubio A, Skoda SR, Cruz-Vázquez C, et al. Virulence of Mexican isolates of entomopathogenic fungi (Hypocreales: Clavicipitaceae) upon Rhipicephalus = Boophilus microplus (Acari: Ixodidae) larvae and the efficacy of conidia formulations to reduce larval tick density under field conditions. Vet Parasitol 2010;170:278-286.
59. Bittencourt VREP, Bahiense TC, Fernandes EKK, Souza EJ. Avalicao da acao en vivo Metarhizium anisopliae (Metschnikoff, 1879) Sorokin, 1883, aplicado sobre Brachiaria decumbes infestada com larvas de Boophilus microplus (Canestrini, 1887) (Acari.Ixodidae). Rev Bras Parasitol Vet 2003;12:73-82.
60. Basso LA, Monteiro A, Belo M, Soares V, García M, Alves D. Controle de larvas de Boophilus microplus por Metarhizium anisopliae em pastagens infestadas artificialmente. Pesq Agropec Bras Brasilia 2005;40:595-600. (Pubitemid 41127869)
61. De Castro ABA, Bittencourt VREP, Deamon E, Viegas EDC. Eficácia do fungo Metarhizium anosopliae sobreo carrapato Boophilis microplus em teste de estabúlado. Rev Univ Rural Ser Cien Vida 1997;19:73-82.
62. Polar P, Kairo M, Peterkin D, Moore D, Pegram R, John S.. Assessment of fungal isolates for development of a myco-acaricide for cattle tick control. Vector Borne Zoonot Dis 2005;5:276-284. (Pubitemid 41498459)
63. Correia A, Fiorin AC, Monteiro AC, Veríssimo. Efeccts of Metarhiziun anisopliae on the tick Boophilus microplus (Acari:Ixodidae) in stabled cattle. J Invertebr Pathol 1998;71:189-191. (Pubitemid 128349188)
64. Ángel CA, Lezama R, Molina J, Galindo E, López M, Rebolledo O, Cruz C, Reyes WP, De Skoda SR, Foster J. Susceptibility of biological stages of the horn fly, Haematobia irritans, to entomopathogenic fungi (Hyphomycetes). J Insect Sci 2005;5:1-8.
65. Galindo E. Uso de Hyphomycetes entomopatógenos para el control de Haematobia irritans (L.) sobre bovinos en el Estado de Colima [Tesis doctoral]. Colima, México: Universidad de Colima; 2005.
66. De Melo D, Verton E, Fernandes K, Da Costa G, Scott F, Bittencourt V. Virulence of Metarhizium anisopliae and Beauveria bassiana to Ctenocephalides felis felis. Animal Biodiversity and Emerging Diseases: Ann NY Acad Sci 2008;(1149):388-390.
67. Mohanty S, Raghavendra K, Mittal P, Dash A. Efficacy of culture filtrates of Metarhizium anisopliae against larvae of Anopheles stephensi and Culex quinquefasciatus. J Ind Microbiol Biotechnol 2008;35:1199-1202.
68. Kanga L, Jones W, James R. Field trials using the fungal pathogen, Metarhizium anisopliae (Deuteromycetes: Hyphomycetes) to control the ectoparasitic mite, Varroa destructor (Acari: Varroidae) in honey Bee, Apis mellifera (Hymenoptera: Apidae) colonies. J Econ Entomol 2003;96:1092-1099.
69. Meyling N, Eilenberg J. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: Potential for conservation biological control. Biol Control 2007;43:145-155. (Pubitemid 47513843)
70. Leemon D, Turner D, Jonsson N. Pen studies on the control of cattle tick (Rhipicephalus microplus) with Metarhizium anisopliae (Sorokin). Vet Parasitol 2008;156:248-260.
71. Fernandes KK, Rangel ED, Moraes A, Bittencourt VREP, Roberts D. Cold activity of Beauveria and Metarhizium and thermotolerance of Beauveria. J Inverter Pathol 2008;98:69-78.
72. Leemon D, Jonsson N. Laboratory studies on Australian of Metarhizium anisoplae as a biopesticide for the cattle tick Boophilus microplus J Invertebr Pathol 2008;97:40-49. (Pubitemid 350235480)
73. Hedimbi M, Kaaya G, Singh S, Chimwamurombe P, Gindin G, Glazer I, Samish M. Protection of Metarhizium anisopliae conidia from ultra-violet radiation and their pathogenicity to Rhipicephalus evertsi ever ts i ticks . Exp Appl Acarol 2008;46:149-156.
74. Kassa A, Brownbridge M, Parker BL, Skinner M, Gouli V, Gouli S, Guo, M, Lee F, Hata T. Whey for mass production of Beauveria bassiana and Metarhizium anisopliae. Mycol Res 2008;112;583-591.