Experimental and Applied Acarology

, Volume 46, Issue 1–4, pp 119–148 | Cite as

Topically applied myco-acaricides for the control of cattle ticks: overcoming the challenges

  • Perry Polar
  • Dave Moore
  • Moses T. K. Kairo
  • Adash Ramsubhag
Article
First Online:
Received:
Accepted:

Abstract

In the absence of commercially viable and environmentally friendly options, the management of cattle ticks is heavily dependent on the use of chemical acaricides. Due to recent advances in production, formulation and application technology, commercial fungus-based biological pesticides (myco-insecticides, myco-acaricides) are becoming increasingly popular for the control of plant pests; however, they have not been used against animal ectoparasites. The literature clearly demonstrates that entomopathogenic fungi are pathogenic to ticks under laboratory conditions. Pasture applications have also shown promise while experiments on topical application have had variable results. These results suggest that major research hurdles still exist especially for the latter. Although literature on ticks and their interactions with entomopathogenic fungi exists, there is not a clear understanding on how this can be influenced by the microenvironment of the cattle skin surface. This paper critically reviews pathogen, tick target and host skin microenvironmental factors that potentially affect pathogenicity of the applied entomopathogen. Factors influencing the route of infection for topically applied myco-acaricides are also reviewed. Major researchable constraints and recommendations are identified and prioritized. In particular, there is the need for basic studies to understand the interaction of entomopathogenic fungi with the components of the skin microenvironment, to identify suitable strains, and to develop improved formulations to overcome the various challenges.

Keywords

Biological pesticide Biological control Cattle Entomopathogen Metarhizium anisopliae Myco-insecticide Myco-acaricide Tick 
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References

  1. Allen TE, Bennett JW, Donegan SM, Hutchingson CD (1970) Moisture, its accumulation and site of evaporation in the coats of sweating cattle. J Agric Sci 74:247–258Google Scholar
  2. Al-Mazra’awi MS, Shipp L, Broadbent B, Kevan K (2006) Biological control of Lygus lineoralis (Hemiptera: Miridae) and Frankliniella occidentalis (Thysanoptera: Thripidae) by Bombus impatiens (Hymenoptera: Apidae) vectored Beauveria bassiana in greenhouse sweet pepper. Biol Control 37:89–97. doi: 10.1016/j.biocontrol.2005.11.014 Google Scholar
  3. Alonso-Díaz MA, García L, Galindo-Velasco E, Lezama-Gutierrez R, Angel-Sahagún CA, Rodríguez-Vivas RI et al (2007) Evaluation of Metarhizium anisopliae (Hyphomycetes) for the control of Boophilus microplus (Acari: Ixodidae) on naturally infested cattle in the Mexican tropics. Vet Parasitol 147:336–340. doi: 10.1016/j.vetpar.2007.03.030 PubMedGoogle Scholar
  4. Alves RT, Bateman RP, Gunn J, Prior C, Leather SR (2002) Effects of different formulations on viability and medium term storage of Metarhizium anisopliae conidia. Neotrop Entomol 31:91–99. doi: 10.1590/S1519-566X2002000100013 Google Scholar
  5. Aquino de Muro M, Moore D, Atkin D, Edgington S (2003) Sheep Scab Project ODO538: studies on the biological control of the sheep scab mite, Psoroptes ovis, using entomopathogenic fungi. Report for Department for Environment, Food and Rural Affairs (DEFRA), Government of the United Kingdom, 8 ppGoogle Scholar
  6. Baker EW, Evans TM, Gould DJ, Hull WB, Keegan HL (1956) Miscellaneous mesostigmatic mites. In: Baker EW, Evans TM, Gould DJ, Hull WB, Keegan HL (eds) A manual of parasitic mites. National Pest Control Association, Inc., United States of AmericaGoogle Scholar
  7. Barker SC, Murrell A (2004) Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 129:S15–S36. doi: 10.1017/S0031182004005207 PubMedGoogle Scholar
  8. Barnes SE, Moore D (1997) The effect of fatty, organic or phenolic acids on the germination of conidia of Metarhizium flavoviride. Mycol Res 101:662–666. doi: 10.1017/S0953756296003152 Google Scholar
  9. Bateman RP (1997) Methods of application of microbial pesticide formulations for the control of grasshopper and locusts. Mem Entomol Soc Can 171:69–81Google Scholar
  10. Bateman RP, Alves RT (2000) Delivery systems for mycoinsecticides using oil-based formulations. Asp Appl Biol 57:163–170Google Scholar
  11. Bateman RP, Chapple A (2001) The spray application of mycopesticide formulations. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents—progress, problems and potential. CAB International, WallingfordGoogle Scholar
  12. Benjamin MA, Zhioua E, Ostfeld RS (2002) Laboratory and field evaluation of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) for controlling questing adult Ixodes scapularis (Acari: Ixodidae). J Med Entomol 39:723–728PubMedGoogle Scholar
  13. Berman A, Volcani R (1961) Seasonal and regional variations in coat characteristics of dairy cattle. Aust J Agric Res 12:528–538. doi: 10.1071/AR9610528 Google Scholar
  14. Beugnet F, Chardonnet L (1995) Tick resistance to pyrethroids in New Caledonia. Vet Parasitol 56:325–338. doi: 10.1016/0304-4017(94)00686-7 PubMedGoogle Scholar
  15. Bittencourt VREP, Massard CL, de Lima AF (1994) Ação do fungo Metarhizium anisopliae em ovos e larvas do carrapato Boophilus microplus. Rev Univ Rural Ser Cienc Vida 16:41–47Google Scholar
  16. Bittencourt VREP, Massard CL, Veigas EDC, de Lima AF (1995a) Isolamento e cultivo do fungo Metarhizium anisopliae (Metschnikoff, 1879) Sorokin, 1883, a partir do carrapato Boophilus microplus (Canestrini, 1887) artificialmente infectado. Rev Univ Rural Ser Cienc Vida 17:55–60Google Scholar
  17. Bittencourt VREP, Massard CL, de Lima AF (1995b) Dinâmica da infecção do carrapato Boophilus microplus pelo fungo Metarhizium anisopliae. Rev Univ Rural Ser Cienc Vida 17:83–88Google Scholar
  18. Bittencourt VREP, Peralva SFLDS, de Souza EJ, Mascarenhas AG, Alves SG (1997) Ação do dois isolados do fungo entomopatogênico Beauveria bassiana sobre algumas charísticas biológicas de fêmeas ingurgitadas de Boophilus microplus em laboratorio. Rev Univ Rural Ser Cienc Vida 19:65–71Google Scholar
  19. Brooks JA, Aquino de Muro M, Moore D, Taylor MA, Wall R (2004) Growth and pathogenicity of isolates of the fungus Metarhizium anisopliae against the parasitic mite, Psoroptes ovis: effects of temperature and formulation. Pest Manag Sci 60:1043–1049. doi: 10.1002/ps.910 PubMedGoogle Scholar
  20. Burgner D, Eagles G, Burgess M, Procopis P, Rogers M, Muir D et al (1998) Disseminated invasive infection due to Metarrhizium [sic] anisopliae in an immunocompromised child. J Clin Microbiol 36:1146–1150PubMedGoogle Scholar
  21. Butt TM, Goettel MS (2000) Bioassays of entomopathogenic fungi. In: Navon A, Ascher KRS (eds) Bioassays of entomopathogenic microbes and nematodes. CAB International, WallingfordGoogle Scholar
  22. Butt TM, Carreck NL, Ibrahim L, Williams IH (1998) Honey-bee-mediated infection of pollen beetle (Meligethes aeneus Fab.) by the insect-pathogenic fungus, Metarhizium anisopliae. Biocontrol Sci Technol 8:533–538. doi: 10.1080/09583159830045 Google Scholar
  23. Butt TM, Jackson CW, Magan N (2001) Introduction—fungal biological control agents: progress, problems and potential. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents—progress, problems and potential. CAB International, WallingfordGoogle Scholar
  24. Campos RA, Arruda W, Boldo JT, da Silva MV, de Barros NV, de Azevedo JL et al (2005) Boophilus microplus infection by Beauveria amorpha and Beauveria bassiana: SEM analysis and regulation of subtilisin-like proteases and chitinases. Curr Microbiol 50:257–261. doi: 10.1007/s00284-004-4460-y PubMedGoogle Scholar
  25. Cannon PF, Kirk PM (2007) Fungal families of the world. CAB International, WallingfordGoogle Scholar
  26. Casasolas-Oliver A (1991) Pathogenicity of Rhizopus thailandensis on engorged females of Rhipicephalus sanguineus (Acari: Ixodide) host–pathogen interaction. Rev Iberoam Micol 8:75–78Google Scholar
  27. Chandler D, Davidson G, Pell JK, Shaw K, Sunderland KD (2000) Fungal biocontrol of the Acari. Biocontrol Sci Technol 10:357–384. doi: 10.1080/09583150050114972 Google Scholar
  28. Correia ACB, Fiorin AC, Monteiro AC (1998) Effects of Metarhizium anisopliae on the tick Boophilus microplus (Acari: Ixodidae) in stabled cattle. J Invertebr Pathol 71:189–191. doi: 10.1006/jipa.1997.4719 Google Scholar
  29. Cumming GS, Van Vuuren DP (2006) Will climate change affect ectoparasite species ranges? Glob Ecol Biogeogr 15:486–497Google Scholar
  30. da Costa GL, Sarquis MIM, de Moraes AML, Bittencourt VREP (2002) Isolation of Beauveria bassiana and Metarhizium anisopliae var. anisopliae from Boophilus microplus tick (Canestrini, 1887), in Rio de Janeiro State, Brazil. Mycopathology 154:207–209. doi: 10.1023/A:1016388618842 Google Scholar
  31. de Castro ABA, Bittencourt VREP, Daemon E, Viegas EDC (1997) Eficácia do fungo Metarhizium anisopliae sobre o carrapato Boophilus microplus em teste de estábulo. Rev Univ Rural Ser Cienc Vida 19:73–82Google Scholar
  32. Dillon RJ, Charnley AK (1985) A technique for accelerating and synchronising germination of conidia of the entomopathogenic fungus Metarhizium anisopliae. Arch Microbiol 142:204–206. doi: 10.1007/BF00447069 Google Scholar
  33. Downing DT, Lindholm JS (1982) Skin surface lipids of the cow. Comp Biochem Physiol 73B:327–330Google Scholar
  34. Environmental Protection Agency (2002) Biopesticides registration action document. Metarhizium anisopliae strain F52 (PC Code 029056). http://www.epa.gov/oppbppd1/biopesticides/ingredients/fr_notices/frnotices_029056.htm. Accessed 14 June 2002
  35. Evans GO (1992) Principles of acarology. CAB International, WallingfordGoogle Scholar
  36. Evans HC, Prior C (1990) Entomopathogenic fungi. In: Rosen D (ed) Armored scale insects, their biology, natural enemies and control. World crop pests, vol 4B. Elsevier Science Publishers, Amsterdam, The Netherlands, pp 3–17Google Scholar
  37. Frazzon APG, Junior IDV, Masuda A, Shrank A, Vainstein MH (2000) In vitro assessment of Metarhizium anisopliae isolates to control the cattle tick Boophilus microplus. Vet Parasitol 94:117–125. doi: 10.1016/S0304-4017(00)00368-X PubMedGoogle Scholar
  38. Freimoser FM, Screen S, Bagga S, Hu G, St. Leger R (2003) Expressed sequence tag (EST) analysis of two subspecies of Metarhizium anisopliae reveals a plethora of secreted proteins with potential activity in insect host. Microbiology 149:239–247. doi: 10.1099/mic.0.25761-0 PubMedGoogle Scholar
  39. George JE, Pound JM, Davey RB (2004) Chemical control of ticks on cattle and resistance of these parasites to acaricides. Parasitology 129:S353–S366. doi: 10.1017/S0031182003004682 Google Scholar
  40. Gindin G, Samish M, Alekseev E, Glazer I (2001) The susceptibility of Boophilus annulatus (Ixodidae) ticks to entomopathogenic fungi. Biocontrol Sci Technol 11:111–118. doi: 10.1080/09583150020029790 Google Scholar
  41. Gindin G, Samish M, Zangi G, Mishoutchenko A, Glazer I (2002) The susceptibility of different species and stages of ticks to entomopathogenic fungi. Exp Appl Acarol 28:283–288. doi: 10.1023/A:1025379307255 PubMedGoogle Scholar
  42. Ginsberg HS, Lebrun RA, Heyer K, Zhioua E (2002) Potential nontarget effects of Metarhizium anisopliae (Deuteromycete) used for biological control of ticks (Acari: Ixodidae). Environ Entomol 31:1191–1196Google Scholar
  43. Goettel MS, Poprawski TJ, Vandenberg JD, Li Z, Roberts DW (1990) Safety to nontarget invertebrates of fungal biocontrol agents. In: Laird M, Lacey LA, Davidson EW (eds) Safety of microbial insecticides. CRC Press, Boca Raton, FL, USAGoogle Scholar
  44. Graf JF, Gogolewski R, Leach-Bing N, Sabatini GA, Molento MB, Bordin EL et al (2004) Tick control: an industry point of view. Parasitology 129:S427–S442. doi: 10.1017/S0031182004006079 PubMedGoogle Scholar
  45. Hassan AEM, Dillon RJ, Charnley AK (1989) Influence of accelerating germination of conidia on the pathogenicity of Metarhizium anisopliae for Manduca sexta. J Invertebr Pathol 54:277–279. doi: 10.1016/0022-2011(89)90040-2 Google Scholar
  46. Hedimbi M, Kaaya GP, Singh S, Chimwamurombe PM, Gindin G, Glazer I et al (2008) Protection of Metarhizium anisopliae conidia from ultraviolet radiation and their pathogenicity to ticks. Exp Appl Acarol 45 (this issue)Google Scholar
  47. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE et al (2007) A higher level phylogenetic classification of the fungi. Mycol Res 111:509–547. doi: 10.1016/j.mycres.2007.03.004 PubMedGoogle Scholar
  48. Hornbostel VL, Ostfeld RS, Zhioua E, Benjamin MA (2004) Sublethal effects of Metarhizium anisopliae (Deuteromycetes) on engorged larval, nymphal, and adult Ixodes scapularis (Acari: Ixodidae). J Med Entomol 41:922–929PubMedGoogle Scholar
  49. Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents—progress, problems and potential. CAB International, WallingfordGoogle Scholar
  50. Jenkinson DM (1992) The basis of the skin ecosystem. In: Noble WC (ed) The skin microflora and microbial disease. Cambridge University Press, Cambridge, UKGoogle Scholar
  51. Jenkins NE, Grzywacz D (2000) Quality control of fungal and viral biocontrol agents—assurance of product performance. Biocontrol Sci Technol 10:753–777. doi: 10.1080/09583150020011717 Google Scholar
  52. Jenkinson DM, Lloyd DH (1979) The topography of the skin surface of cattle and sheep. Br Vet J 135:376–379PubMedGoogle Scholar
  53. Jenkinson DM, Mabon RM (1973) The effect of temperature and humidity on the skin surface pH and the ionic composition of skin secretions in Ayrshire cattle. Br Vet J 129:282–295PubMedGoogle Scholar
  54. Jenkinson DM, Mabon RM (1975) The corticosterol content of cattle skin washing. Res Vet Sci 19:94–95PubMedGoogle Scholar
  55. Jenkinson DM, Lloyd DH, Mabon RM (1979) The antigenic composition and source of soluble proteins on the surface of the skin of sheep. J Comp Pathol 89:43–50. doi: 10.1016/0021-9975(79)90007-0 PubMedGoogle Scholar
  56. Jenkinson DM, Mabon RM, Mason W (1974a) Sweat proteins. Br J Dermatol 90:175–181. doi: 10.1111/j.1365-2133.1974.tb06382.x PubMedGoogle Scholar
  57. Jenkinson DM, Mabon RM, Mason W (1974b) The effect of temperature and humidity on the losses of nitrogenous substances from the skin of Ayrshire cattle. Res Vet Sci 17:75–80PubMedGoogle Scholar
  58. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129:S3–S14. doi: 10.1017/S0031182004005967 PubMedGoogle Scholar
  59. Jonsson NN (1997) Control of cattle ticks (Boophilus microplus) on Queensland dairy farms. Aust Vet J 75:802–807. doi: 10.1111/j.1751-0813.1997.tb15657.x PubMedGoogle Scholar
  60. Jonsson NN, Mayer DG, Matschoss AL, Green PE, Ansell J (1998) Production effects of cattle tick (Boophilus microplus) infestation of high yielding dairy cows. Vet Parasitol 78:65–77. doi: 10.1016/S0304-4017(98)00118-6 PubMedGoogle Scholar
  61. Kaaya GP, Hassan S (2000) Entomogenous fungi as promising biopesticides for tick control. Exp Appl Acarol 24:913–926. doi: 10.1023/A:1010722914299 Google Scholar
  62. Kaaya GP, Mwangi EN, Ouna EA (1996) Prospects for biological control of livestock ticks, Rhipicephalus appendiculatus and Amblyomma variegatum, using the entomogenous fungi Beauveria bassiana and Metarhizium anisopliae. J Invertebr Pathol 67:15–20. doi: 10.1006/jipa.1996.0003 PubMedGoogle Scholar
  63. Kalsbeek V, Frandsen F, Steenberg T (1995) Entomopathogenic fungi associated with Ixodes ricinus ticks. Exp Appl Acarol 19:45–51. doi: 10.1007/BF00051936 PubMedGoogle Scholar
  64. Kedra E, Bogus MI (2006) The influence of Conidiobolus coronatus on phagocytic activity of insect hemocytes. J Invertebr Pathol 91:50–52. doi: 10.1016/j.jip.2005.06.013 PubMedGoogle Scholar
  65. Kettle DS (1995) Ixodida—Ixodidae (hard ticks). In: Kettle DS (ed) Medical and veterinary entomology, 2nd edn. CAB International, Wallingford, UKGoogle Scholar
  66. Kirkland BH, Cho E, Keyhani NO (2004) Differential susceptibility of Amblyomma maculatum and Amblyomma americanum (Acari: Ixodidea) to the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae. Biol Control 31:414–421. doi: 10.1016/j.biocontrol.2004.07.007 Google Scholar
  67. Klompen JSH, WC Black IV, Keirans JE, Homsher PJ (1996) Evolution of ticks. Annu Rev Entomol 41:141–161. doi: 10.1146/annurev.en.41.010196.001041 PubMedGoogle Scholar
  68. Kooyman C, Bateman RP, Langewald J, Lomer CJ, Ouambama Z, Thomas MB (1997) Operational-scale application of entomopathogenic fungi for the control of Sahelian grasshoppers. Proc R Soc Lond B Biol Sci 264:541–546. doi: 10.1098/rspb.1997.0077 Google Scholar
  69. Langewalde J, Ouambama Z, Mamadou A, Mamadou A, Peveling R, Stol I et al (1999) Comparison of an organophosphate insecticide with a mycoinsecticide for the control of Oedaleus senegalensis (Orthoptera:Acrididae) and other Sahelian grasshoppers at an operational scale. Biocontrol Sci Technol 9:199–214. doi: 10.1080/09583159929785 Google Scholar
  70. Latif A (2003) Ticks and tickborne diseases in livestock in southern Africa. Newsletter on Integrated Control of Pathogenic Trypanosomes and their Vectors, vol 7, pp 19–20Google Scholar
  71. Latif A, Jongejan F (2002) The wide use of acaricides for the control of livestock diseases in Africa needs a reappraisal. Newsletter on Integrated Control of Pathogenic Trypanosomes and their Vectors, vol 6, pp 10–12Google Scholar
  72. Leemon DM, Jonsson NN (2008) Laboratory studies on Australian isolates of Metarhizium anisopliae as a biopesticide for the cattle tick Boophilus microplus. J Invertebr Pathol 97:40–49. doi: 10.1016/j.jip.2007.07.006 PubMedGoogle Scholar
  73. Li DP, Holdom DG (1995) Effects of nutrients on colony formation, growth, and sporulation of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes). J Invertebr Pathol 65:253–260. doi: 10.1006/jipa.1995.1039 Google Scholar
  74. Lloyd DH, Mabon RM, Jenkinson DM (1977) The antigenic constituents of cattle skin washing. J Comp Pathol 87:75–82. doi: 10.1016/0021-9975(77)90081-0 PubMedGoogle Scholar
  75. Lloyd DH, Dick WDB, Jenkinson DM (1979a) Structure of the epidermis in Ayshire bullocks. Res Vet Sci 26:172–179PubMedGoogle Scholar
  76. Lloyd DH, Dick WDB, Jenkinson DM (1979b) Location of the microflora in the skin of cattle. Br Vet J 135:519–526PubMedGoogle Scholar
  77. Lombardini G (1953) Biological and anatomical observations on Rhipicephalus sanguineus (Acarina: Ixodidae). Rev Appl Entomol Ser B 41:8Google Scholar
  78. Loosová G, Jindrák L, Kopáček P (2001) Mortality caused by experimental infection with the yeast Candida haemulonii in the adults of Ornithodorus moubata (Acarina: Argasidae). Folia Parasitol (Praha) 48:149–153Google Scholar
  79. Lui ZY, Milner RJ, McRae CF, Lutton GC (1993) The use of dodine in selective medium for the isolation of Metarhizium spp. from soil. J Invertebr Pathol 62:248–251. doi: 10.1006/jipa.1993.1107 Google Scholar
  80. Mabon RM, Jenkinson DM (1971) The excretion of 3-methoxy-4-hydroxy mandelic acid (VMA) by cattle skin. Res Vet Sci 12:289–292PubMedGoogle Scholar
  81. Marcandier S, Khachatourians GG (1987) Susceptibility of the migratory grasshopper, Melanoplus sanguinipes (Fab.) (Orthoptera: Acrididae), to Beauveria bassiana (Bals.) Vuillemin (Hyphomycete): influence of relative humidity. Can Entomol 119:901–907CrossRefGoogle Scholar
  82. McBride ME (1993) Physical factors affecting the skin flora and skin disease. In: Noble WC (ed) The skin microflora and microbial disease. Cambridge University Press, Cambridge, UK, pp 73–101Google Scholar
  83. McMaster JD, Jenkinson DM, Noble RC, Elder HY (1985) The lipid composition of bovine sebum and dermis. Br Vet J 141:34–41PubMedGoogle Scholar
  84. Mitra SK, Sikdar A, Das P (1998) Dermatophytes isolated from selected ruminants in India. Mycopathologia 142:13–16. doi: 10.1023/A:1006944605066 PubMedGoogle Scholar
  85. Monteiro SG, Bittencourt VREP, Daemon E, Faccini JLH (1998a) Pathogenicity under laboratory conditions of the fungi Beauveria bassiana and Metarhizium anisopliae on larvae of the tick Rhipicephalus sanguineus (Acari: Ixodidae). Rev Bras Parasitol Vet 7:113–116Google Scholar
  86. Monteiro SG, Carneiro ME, Bittencourt VREP, Daemon E (1998b) Effect of isolate 986 of the fungi Beauveria bassiana (Bals) Vuill on engorged females of Anocentor nitens Neumann, 1897 (Acari: Ixodidae). Arq Bras Med Vet Zootec 50:673–676Google Scholar
  87. Monteiro SG, Matimoto LR, da Silveira FS, Leal AM (2004) Isolation of fungi in Ixodids ticks naturally infected. Rev Fac Zootec Vet Agro Uruguaiana 10:65–71Google Scholar
  88. Monty DE, Garbareno MS (1978) Behavioural and physiologic responses of Holstein-Friesian cows to high environmental temperatures and artificial cooling in Arizona. Am J Vet Res 39:877–882PubMedGoogle Scholar
  89. Moore D, Morley-Davies J (1994) The effects of temperature and ultra-violet irradiation on conidia of Metarhizium flavoviride. In: Proceedings of the Brighton crop protection conference—pest and diseases, pp 1085–1090Google Scholar
  90. Moore D, Higgins PM, Lomer CJ (1996) Effects of simulated and natural light on the germination of conidia of Metarhizium flavoviride Gams and Rozsypal and interactions with temperature. Biocontrol Sci Technol 6:63–76. doi: 10.1080/09583159650039539 Google Scholar
  91. Moore D, Langewald J, Obognon F (1997) Effects of rehydration on the conidial viability of Metarhizium flavoviride mycopesticide formulations. Biocontrol Sci Technol 7:87–94. doi: 10.1080/09583159731072 Google Scholar
  92. Morley-Davies J, Moore D, Prior C (1996) Screening of Metarhizium and Beauveria spp. conidia with exposure to simulated sunlight and a range of temperatures. Mycol Res 100:31–38Google Scholar
  93. Nari A (1995) Strategies for the control of one-host ticks and relationship with tick-borne diseases in South America. Vet Parasitol 57:153–165. doi: 10.1016/0304-4017(94)03117-F PubMedGoogle Scholar
  94. Olwoch JM, Rautenbach CJ, Erasmus BFN, Engelbrecht FA, Jaarsveld AS (2003) Simulating tick distributions over sub-Saharan Africa: the use of observed and simulated climate surfaces. J Biogeogr 30:1221–1232. doi: 10.1046/j.1365-2699.2003.00913.x Google Scholar
  95. Onions AHS (1966) Scopulariopsis brevicaulis CMI descriptions of pathogenic fungi and bacteria, vol 100. Commonwealth Agricultural Bureaux, WallingfordGoogle Scholar
  96. Onofre SB, Miniuk CM, Barros NM, Azevedo JL (2001) Pathogenicity of four strains of entomopathogenic fungi against the bovine tick Boophilus microplus. J Vet Med 62:1478–1480Google Scholar
  97. Pegram RG, Oosterwijk GP (1990) The effect of Amblyomma variegatum on liveweight gain of cattle in Zambia. Med Vet Entomol 4:327–330. doi: 10.1111/j.1365-2915.1990.tb00448.x PubMedGoogle Scholar
  98. Polar P (2007) Studies on the use of entomopathogenic fungi for the control of cattle ticks. Ph.D. thesis, The University of the West Indies, TrinidadGoogle Scholar
  99. Polar P, Kairo MTK, Peterkin D, Moore D, Pegram R, John S (2005a) Assessment of fungal isolates for the development of a myco-acaricide for cattle tick control. Vector Borne Zoonotic Dis 5:276–284. doi: 10.1089/vbz.2005.5.276 PubMedGoogle Scholar
  100. Polar P, Aquino de Muro M, Kairo MTK, Moore D, Pegram R, John S et al (2005b) Thermal characteristics of Metarhizium anisopliae isolates important for the development of biological pesticides for the control of cattle ticks. Vet Parasitol 134:159–167. doi: 10.1016/j.vetpar.2005.07.010 PubMedGoogle Scholar
  101. Polar P, Kairo MTK, Moore D et al (2005c) Comparison of water, oils and emulsifiable adjuvant oils as formulating agents for Metarhizium anisopliae for use in control of Boophilus microplus. Mycopathology 160:151–157. doi: 10.1007/s11046-005-0120-4 Google Scholar
  102. Prior C, Carey M, Abraham YJ, Moore D, Bateman RP (1995) Development of a bioassay method for the selection of entomopathogenic fungi virulent to the desert locust, Schistocerca gregaria (Forskål). J Appl Entomol 119:567–573Google Scholar
  103. Prior C, Jollands P, Le Patourel G (1988) Infectivity of oil and water formulations of Beauveria bassiana (Deuteromycotina: Hyphomycetes) to cocoa weevil pest Pantorhytes plutus (Coleoptera: Curculionidae). J Invertebr Pathol 52:66–72. doi: 10.1016/0022-2011(88)90103-6 Google Scholar
  104. Revankar SG, Sutton DA, Sanche SE, Rao J, Zervos M, Dashti F et al (1999) Metarrhizium [sic] anisopliae as a cause of sinusitis in immunocompetent host. J Clin Microbiol 37:195–198PubMedGoogle Scholar
  105. Rijo-Camacho E (1996) Lucha biological contra la garrapata Boophilus microplus (Canestrini, 1887) con hongos entomopatogenos. Ph.D. thesis, Instituto de Investigaciones de Sanidad Vegetal, Cuidad de la Havana, CubaGoogle Scholar
  106. Rogers GD (1989) Control of the molds Aspergillius sydowi and Penicillium citrinum in laboratory colonies of the Lone-Star tick, Amblyomma americanum (Acari: Ixodidae). Exp Appl Acarol 6:257–261. doi: 10.1007/BF01193985 Google Scholar
  107. Rourke BC, Gibbs AG (1999) Effects of lipid phase transitions on cuticular permeability: model membrane and in situ structures. J Exp Biol 202:3255–3262PubMedGoogle Scholar
  108. Samish M, Rehacek J (1999) Pathogens and predators of ticks and their potential in biological control. Annu Rev Entomol 44:159–182. doi: 10.1146/annurev.ento.44.1.159 PubMedGoogle Scholar
  109. Samish M, Gindin G, Alekseev E, Glazer I (2001) Pathogenicity of entomopathogenic fungi to different developmental stages of Rhipicephalus sanguineus (Acari: Ixodidae). J Parasitol 87:1355–1339PubMedGoogle Scholar
  110. Samsinakova A, Kalalova S, Daniel M, Dusbabek F, Honzakova E, Cerny V (1974) Entomogenous fungi associated with the tick Ixodes ricinus. Folia Parasitol (Praha) 21:38–48Google Scholar
  111. Singh SP, Newton WM (1978) Acclimation of young calves to high temperatures: composition of blood and skin secretions. Am J Vet Res 39:799–801PubMedGoogle Scholar
  112. Smith JMB (1989) Opportunistic mycoses of man and other animals. CAB International, Wallingford, UKGoogle Scholar
  113. Smith ME, Ahmed SU (1976) The lipid composition of sebaceous glands: a comparison with skin surface lipid. Res Vet Sci 21:250–252PubMedGoogle Scholar
  114. Smith ME, Jenkinson DM (1975a) The mode of secretion of the sebaceous glands of cattle. Br Vet J 131:610–617PubMedGoogle Scholar
  115. Smith ME, Jenkinson DM (1975b) The effect of age, sex and season on sebum output of Ayrshire calves. J Agric Sci 84:57–60CrossRefGoogle Scholar
  116. Souza EJ, Reis RCS, Bittencourt VREP (1999) Evaluation of in vitro effect of the fungi Beauveria bassiana and Metarhizium anisopliae on eggs and larvae of Amblyomma cajennense. Rev Bras Parasitol Vet 8:127–131Google Scholar
  117. Steelman CD, Brown MA, Gbur EE, Tolley G (1997) The effects of hair density of beef cattle on Haematobia irritans horn fly populations. Med Vet Entomol 11:257–264. doi: 10.1111/j.1365-2915.1997.tb00404.x PubMedGoogle Scholar
  118. St. Leger R, Nelson JO, Screen S (1999) The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology 145:2691–2691PubMedGoogle Scholar
  119. St. Leger R, Screen S (2001) Prospects for strain improvement of fungal pathogens of insects and weeds. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents—progress, problems and potential. CAB International, Wallingford, UK, pp 219–238Google Scholar
  120. Thomas MB (1999) Ecological approaches and the development of “truly integrated” pest management. Proc Natl Acad Sci U S A 96:5944–5951. doi: 10.1073/pnas.96.11.5944 PubMedGoogle Scholar
  121. Thomas MB, Wood SN, Langewald J, Lomer CJ (1997) Persistence of Metarhizium flavoviride and consequences for biological control of grasshoppers and locust. Pestic Sci 49:47–55. doi:10.1002/(SICI)1096-9063(199701)49:1<47::AID-PS471>3.0.CO;2-OGoogle Scholar
  122. Thomas MB, Wood SN, Solorzano V (1999) Application of insect-pathogen models to biological control. In: Hawkins BA, Cornell HV (eds) Theoretical approaches to biological control. Cambridge University Press, Cambridge, UK, pp 368–384Google Scholar
  123. Valle ACF, Wanke B, Lazera MS, Monteiro PCF, Viegas ML (2001) Entomophthoramycosis by Conidiobolus coronatus. Report of a case successfully treated with the combination of itraconazole and fluconazole. Rev Inst Med Trop Sao Paulo 43:233–236PubMedGoogle Scholar
  124. Van der Geest LPS, Elliot SL, Breeuwer JAJ, Beerling EAM (2000) Diseases of mites. Exp Appl Acarol 24:497–560. doi: 10.1023/A:1026518418163 PubMedGoogle Scholar
  125. Weitkamp AW (1945) The acidic constituents of degras—a new method of structural elucidation. J Am Chem Soc 67:447–454. doi: 10.1021/ja01219a027 Google Scholar
  126. Whipps JM, Lumsden RD (2001) Commercial use of fungi as plant disease biological control agents: status and prospects. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents—progress, problems and potential. CAB International, Wallingford, UK, pp 9–22Google Scholar
  127. Wikel SK (1996) The immunology of host-ectoparasitic arthropod relationships. CAB International, Wallingford, UKGoogle Scholar
  128. Wille JJ, Kydonieus A (2003) Palmitoleic acid isomer (C16:1∆6) in human skin sebum is effective against gram-positive bacteria. Skin Pharmacol Appl Skin Physiol 16:176–187. doi: 10.1159/000069757 PubMedGoogle Scholar
  129. Wolff MS, Monty DE (1974) Physiological response to intense summer heat and its effect on the estrous cycle of non-lactating and lactating Holstein-Friesian cows in Arizona. Am J Vet Res 35:187–192PubMedGoogle Scholar
  130. Yoder JA, Hanson PE, Zettler LW, Benoit JB, Ghisays F, Piskin KA (2003) Internal and external mycoflora of the American dog tick, Dermacentor variablis (Acari: Ixodidae), and its ecological implications. Appl Environ Microbiol 69:4994–4996. doi: 10.1128/AEM.69.8.4994-4996.2003 PubMedGoogle Scholar
  131. Zhioua E, Browning M, Johnson PW, Ginsberg HS, LeBrun RA (1997) Pathogenicity of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycete) to Ixodes scapularis (Acari: Ixodidae). J Parasitol 83:815–818. doi: 10.2307/3284273 PubMedGoogle Scholar
  132. Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Technol 176:553–555. doi: 10.1080/09583150701309006 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Perry Polar
    • 1
  • Dave Moore
    • 2
  • Moses T. K. Kairo
    • 3
  • Adash Ramsubhag
    • 4
  1. 1.CABI, Caribbean and Latin AmericaCurepeTrinidad and Tobago
  2. 2.CABI Europe-UKEghamUK
  3. 3.Center for Biological ControlFlorida A&M UniversityTallahasseeUSA
  4. 4.Faculty of Science and AgricultureThe University of the West IndiesSt. AugustineTrinidad and Tobago

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