Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T11:48:27.526Z Has data issue: false hasContentIssue false

Biological control of ticks

Published online by Cambridge University Press:  19 April 2005

M. SAMISH
Affiliation:
Kimron Veterinary Institute, P.O. Box 12, Bet Dagan 50250, Israel
H. GINSBERG
Affiliation:
Patuxent Wildlife Research Center, US Geological Survey, University of Rhode Island, Woodward-PLS, Kingston RI 02881, USA
I. GLAZER
Affiliation:
Entomology & Nematology, ARO, Volcani Center, B.O. Box 6, Bet Dagan 50250, Israel

Abstract

Ticks have numerous natural enemies, but only a few species have been evaluated as tick biocontrol agents (BCAs). Some laboratory results suggest that several bacteria are pathogenic to ticks, but their mode of action and their potential value as biocontrol agents remain to be determined. The most promising entomopathogenic fungi appear to be Metarhizium anisopliae and Beauveria bassiana, strains of which are already commercially available for the control of some pests. Development of effective formulations is critical for tick management. Entomopathogenic nematodes that are pathogenic to ticks can potentially control ticks, but improved formulations and selection of novel nematode strains are needed. Parasitoid wasps of the genus Ixodiphagus do not typically control ticks under natural conditions, but inundative releases show potential value. Most predators of ticks are generalists, with a limited potential for tick management (one possible exception is oxpeckers in Africa). Biological control is likely to play a substantial role in future IPM programmes for ticks because of the diversity of taxa that show high potential as tick BCAs. Considerable research is required to select appropriate strains, develop them as BCAs, establish their effectiveness, and devise production strategies to bring them to practical use.

Type
Research Article
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ALEKSEEV, A. N., BURENKOVA, L. A., PODBORONOV, V. M. & CHUNIKHIN, S. P. ( 1995). Bacteriocidal qualities of ixodid tick (Acarina: Ixodidae) salivary cement plugs and their changes under the influence of a viral tick-borne pathogen. Journal of Medical Entomology 32, 578582.CrossRefGoogle Scholar
ALFEEV, N. I. ( 1946). The utilisation of Hunterellus hookeri How. for the control of the tick, Ixodes ricinus L. and Ixodes persulcatus. Review of Applied Entomology B34, 108109 (abstract).Google Scholar
BARCI, L. A. G. ( 1997). Biological control of the cattle tick Boophilus microplus (Acari, Ixodidae) in Brazil. Arquivos Instuto Biologico, Sao Paulo 64, 95101.Google Scholar
BARRE, N., MAULEON, H., GARRIS, G. I. & KERMARREC, A. ( 1991). Predators of the tick Amblyomma variegatum (Acari: Ixodidae) in Guadeloupe, French West Indies. Experimental and Applied Acarology 12, 163170.CrossRefGoogle Scholar
BENJAMIN, M. A., ZHIOUA, E. & OSTFELD, R. S. ( 2002). Laboratory and field evaluation of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) for controlling questing adult Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 39, 723728.CrossRefGoogle Scholar
BEZUIDENHOUT, J. D. & STUTTERHEIM, C. J. ( 1980). A critical evaluation of the role played by the red-billed oxpecker Buphagus erythrorhychus in the biological control of ticks. Onderstepoort Journal of Veterinary Research 47, 5175.Google Scholar
BITTENCOURT, V. R. E. P. ( 2000). Trials to control South American ticks with entomopathogenic fungi. Annals of the New York Academy of Science 916, 555558.CrossRefGoogle Scholar
BITTENCOURT, V. R. E. P., MASSARD, C. L. & LIMA, A. F. ( 1994 a). The action of Metarhizium anisopliae, at eggs and larvae of tick Boophilus microplus. Revisto da Universidade Rural Serie Ciencias da Vida 16, 4147.Google Scholar
BITTENCOURT, V. R. E. P., MASSARD, C. L. & LIMA, A. F. ( 1994 b). The action of Metarhizium anisopliae, at free living stages of Boophilus microplus. Revista da Universidade Rural Serie Ciencias da Vida 16, 4955.Google Scholar
BITTENCOURT, V. R. E. P., SOUZA, E. J., PERALVA, S. L. F. S. & REIS, R. C. S. ( 1999). Efficacy of the fungus Metarhizium anisopliae (Metschnikoff, 1887) Sorokin,1883 in field test with bovines naturally infested with the tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Revista Brasileiro de Medicina Veterinaria 21, 7881.Google Scholar
BOICHEV, D. & RIZVANOV, K. ( 1960). Relation of Botrytis cinerea Pers. to ixodid ticks. Zoologicheskii Zhurnal Akademija Nauk USSR 39, 462.Google Scholar
BOWMAN, J. L., LOGAN, T. M. & HAIR, J. A. ( 1986). Host suitability of Ixodiphagus texanus Howard on five species of hard ticks. Journal of Agricultural Entomology 3, 19.Google Scholar
BROWN, R. S., REICHELDERFER, C. F. & ANDERSON, W. R. ( 1970). An endemic disease among laboratory populations of Dermacentor andersoni (=D. venustus) (Acarina: Ixodidae). Journal of Invertebrate Pathology 16, 142143.Google Scholar
BRUM, J. G. W., FACCINI, J. L. H. & DO AMARAL, M. M. ( 1991 a). Infection in engorged females of Boophilus microplus (Acari: Ixodidae). II. Histopathology and in vitro trials. Arquivos Brasileiro Medicina Vetrinaria Zootecnologia 43, 3537.Google Scholar
BRUM, J. G. W. & TEIXEIRA, M. O. ( 1992). Acaricidal activity of Cedea lapagei on engorged females of Boophilus microplus exposed to the environment. Arquivos Brasileiro de Medicina Veterinaria i Zoologia 44, 543544.Google Scholar
BRUM, J. G. W., TEIXEIRA, M. O. & DA SILVA, E. G. ( 1991 b). Infection in engorged females of Boophilus microplus (Acari: Ixodidae). I. Etiology and seasonal incidence. Arquivos Brasileiro de Medicina Veterinaria i Zoologia 43, 2530.Google Scholar
butt, t. m., jackson, c. w. & magan, n. (ed.) ( 2001). Fungi as Biocontrol Agents – Progress, Problems and Potential. Oxford, UK, CABI.CrossRef
CAMACHO, E. R., NAVARO, G., RODRIGUEZ, R. M. & MURILLO, E. Y. ( 1998). Effectiveness of Verticillium lecanii against the parasitic stage of the tick Boophilus microplus (Acari: Metastigmata: Ixodidae). Revista Colombiana Entomologia 24, 6769.Google Scholar
CASTINEIRAS, A., JIMENO, G., LOPEZ, M. & SOSA, L. M. ( 1987). Effect of Beauveria bassiana, Metarhizium anisopliae (Fungi, Imperfecti) and Pheidole megacephala (Hymenopthera, Formicidae) on eggs of Boophilus microplus (Acarina: Ixodidae). Revista Salud Animal 9, 288293.Google Scholar
CASTRO, A. B. A., BITTENCOURT, V. R. E. P., DAEMON, E. & VIEGAS, E. C. ( 1997). Efficacy of the fungus Metarhizium anisopliae (isolate 959) on the tick Boophilus microplus in a stall test. Revista Universidade Rural, Serie Ciencias da Vida 19, 7382.Google Scholar
CERAUL, S. M., SONENSHINE, D. E. & HYNES, W. L. ( 2002). Resistance of the tick Dermacentor variabilis (Acari: Ixodidae) following challenge with the bacterium Escherichi coli (Enterobacteriales: Enterobacteriaceae). Journal of Medical Entomology 39, 376383.CrossRefGoogle Scholar
CHANDLER, D., DAVIDSON, G., PELL, J. K., BALL, B. V., SHAW, K. & SUNDERLAND, K. D. ( 2000). Fungal biocontrol of Acari. Biocontrol Science and Technology 10, 357384.CrossRefGoogle Scholar
CHEREPANOVA, N. P. ( 1964). Fungi which are found on ticks. Botanicheskii Zhurnal 49, 696699.Google Scholar
COBB, S. ( 1942). Tick parasites on Cape Cod. Science 95, 503.CrossRefGoogle Scholar
COLE, M. M. ( 1965). Biological control of ticks by the use of hymenopterous parasites – a review. World Health Organization Publication, WHO/ebl/43.65, 112.Google Scholar
COOLEY, R. A. & KOHLS, G. M. ( 1934). A summary on tick parasites. Proceedings of the 5th Pacific Science Congress, Canada 1933. The University of Toronto Press 5, 33753381.Google Scholar
COPPING, L. G. ( 2001). The Bio-Pesticide Manual (2nd edition). British Crop Protection Council Publication, Surrey.
CORREIA, A. C. B., FIORIN, A. C., MONTEIRO, A. C. & VERISSIMO C. J. ( 1998). Effects of Metarhizium anisopliae on the tick Boophilus microplus (Acari: Ixodidae) in stabled cattle. Journal of Invertebrate Pathology 71, 189191.CrossRefGoogle Scholar
COUTO, J. T. ( 1994). Operation oxpecker. The Farmers December, pp. 1011.Google Scholar
DA COSTA, G. L., SARQUIS, M. I. M., DE MORAES, A. M. L. & BITTENCOURT, V. R. E. P. ( 2001). Isolation of Beauveria bassiana and Metarhizium anisopliae var anisopliae from Boophilus microplus tick (Canestrini, 1887), in Rio de Janeiro State, Brazil. Micropathologia 154, 207209.Google Scholar
DAVIS, A. J. ( 1986). Bibliography of the Ixodiphagini (Hymenoptera, Chalcidoidea, Encyrtidae), parasites of ticks (Acari, Ixodidae), with notes on their biology. Tijdschrift voor Entomologie 129, 181190.Google Scholar
DAVISON, E. ( 1963). Introduction of oxpeckers (Buphagus africanus and B. erythrorhynus) into McIlwaine National Park. Ostrich 34, 172173.Google Scholar
DE BACH, P. & ROSEN, D. ( 1991). Biological Control by Natural Enemies, 2nd Edn. New York, Cambridge University Press.
DOUBE, B. M. & HEATH, A. C. G. ( 1975). Observations on the biology and seasonal abundance of an encyrtid wasp, a parasite of ticks in Queensland. Journal of Medical Entomology 12, 443447.CrossRefGoogle Scholar
DREYER, K., FOURIE, L. J. & KOK, D. J. ( 1997). Predation of livestock ticks by chickens as a tick-control method in a resource-poor urban environment. Ondersterpoort Journal of Veterinary Research 64, 273276.Google Scholar
DUBOIS, N. R. & DEAN, D. H. ( 1995). Synergism between CryIA insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores, and vegetative cells against Lymantria dispar (Lepidoptera: Lymanntridae) larvae. Environmental Entomology 24, 17411747.CrossRefGoogle Scholar
EL-SADAWY, H. A. E. & HABEEB, S. M. ( 1998). Testing some entomopathogenic nematodes for the biocontrol of Hyalomma dromedrii Koch (Acarina: Ixodidae). Journal of the Union of Arab Biologists, Cairo 10A, Zoology 111.Google Scholar
ESTRADA PENA, A., GONZALEZ, J. & CASASOLAS, A. ( 1990). The activity of Aspergillus ochraceus (Fungi) on replete females of Rhipicephalus sanguineus (Acari: Ixodidae) in natural and experimental conditions. Folia Parasitologica 37, 331336.Google Scholar
FLEXNER, J. L. & BELNAVIS, D. L. ( 2000). Microbial insecticides. In Biological and Biotechnological Control of Insect Pests (ed. Rechcigl, J. E. & Rechcigl, N. A.), pp. 3562. Boca Raton, Florida, USA, Lewis Publishers.
GAHAN, A. B. ( 1934). On the identities of chalcidoid tick parasites (Hymenoptera). Washington Entomological Society Proceedings 36, 8788.Google Scholar
gaugler, r. (ed.)( 2002). Entomopathogenic Nematology. Oxford, UK, CABI.CrossRef
GEORGIS, R. & MANWEILER, S. A. ( 1994). Entomopathogenic nematodes: a developing biological control technology. Agricultural Zoological Review 6, 6394.Google Scholar
GILL, S. S., COWLES, E. A. & PIETRANTONIO, P. V. ( 1992). The mode of action of Bacillus thuringiensis endotoxins. Annual Review of Entomology 37, 615636.CrossRefGoogle Scholar
GINDIN, G., SAMISH, M., ALEKSEEV, E. & GLAZER, I. ( 2001). The susceptibility of Boophilus annulatus (Ixodidae) ticks to entomopathogenic fungi. Biocontrol Science and Technology 11, 111118.CrossRefGoogle Scholar
GINDIN, G., SAMISH, M., ZANGI, G., MISHOUTCHENKO, A. & GLAZER, I. ( 2003). The susceptibility of different species and stages of ticks to entomopathogenic fungi. Experimental and Applied Acarology 28, 283288.CrossRefGoogle Scholar
GINSBERG, H. S., LEBRUN, R. A., HEYER, K. & ZHIOUA, E. ( 2002). Potential nontarget effects of Metarhizium anisopliae (Deuteromycetes) used for biological control of ticks (Acari: Ixodidae). Environmental Entomology 31, 11911196.CrossRefGoogle Scholar
GINSBERG, H. S. & ZHIOUA, E. ( 1999). Influence of deer abundance on the abundance of questing adult Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 36, 376381.CrossRefGoogle Scholar
GLAZER, I. ( 2001). Survival biology. In Entomopathogenic Nematology (ed. Gaugler, R.), pp. 169187. Oxford, UK, CABI.
GLAZER, I., ALEKSEEV, E. & SAMISH, M. ( 2001). Factors affecting the virulence of entomopathogenic nematodes to engorged female Boophilus annulatus. Journal of Parasitology 87, 808812.CrossRefGoogle Scholar
GORSHKOVA, G. J. ( 1966). Reduction of fecundity of ixodid ticks females by fungal infection. Vestnik Leningradskogo Universiteta Seria Biologia 21, 1316.Google Scholar
GRAF, J. F. ( 1979). The biology of an encyrtid wasp parasitizing ticks on the Ivory Coast. In Recent Advances in Acarology, Volume I (ed. Rodriguez, J. G.), pp. 463468. New York, Academic Press.CrossRef
GROBLER, J. H. ( 1976). The introduction of oxpeckers into the Rhodes Matopos National Park. Honeyguide 87, 2325.Google Scholar
GROBLER, J. H. ( 1979). The re-introduction of oxpeckers Buphagus africanus and B. erythrorhynchus to Rhodes Matopos National Park, Rhodesia. Biological Conservation 15, 151158.Google Scholar
GUANGFU, T. ( 1984). Experiment of infection and killing of Hyalomma detritum with fungi. Journal of Veterinary Sciences (China) 7, 1113.Google Scholar
GUERRA, R. M. S. N. C., TEIXEIRA FILHO, W. L., COSTA, G. L. & BITTENCOURT, V. R. E. P. ( 2001). Fungus isolated from Rhipicephabus sanguineus (Acari: Ixodidae), Cochliomya macellaria (Diptera: Muscidae) and Musca domestica (Diptera: Muscidea), naturally infected on Seropedica, Rio de Janeiro. Ciencia Animal 11, 133136.Google Scholar
HAJEK, A. E. & ST. LEGER, R. J. ( 1994). Interaction between fungal pathogens and insect hosts. Annual Review of Entomology 39, 293322.CrossRefGoogle Scholar
HASSAN, S. M., DIPEOLU, O. O., AMOO, A. O. & ODHIAMBO, T. R. ( 1991). Predation on livestock ticks by chickens. Veterinary Parasitology 38, 199204.CrossRefGoogle Scholar
HASSAN, S. M., DIPEOLU, O. O. & MUNYINYI, D. M. ( 1992). Influence of exposure period and management methods on the effectiveness of chickens as predators of ticks infesting cattle. Veterinary Parasitology 43, 301309.CrossRefGoogle Scholar
HASSANAIN, M. A., DERBALA, A. A., ABDEL-BARRY, N. A., EL-SHERIF, M. A. & EL-SADAWY, H. A. E. ( 1999). Biological control of ticks (Argasidae) by entomopathogenic nematodes. Egyptian Journal of Biological Pest Control 7, 4146.Google Scholar
HASSANAIN, M. A., EL GARHY, M. F., ABDEL-GHAFFAR, F. A., EL-SHARABY, A. & MEGEED, K. N. A. ( 1997). Biological control studies of soft and hard ticks in Egypt, I. The effect of Bacillus thuringiensis varieties on soft and hard ticks (Ixodidae). Parasitology Research 83, 209213.CrossRefGoogle Scholar
HENDRY, D. A. & RECHAV, Y. ( 1981). Acaricidal bacteria infecting laboratory colonies of the tick Boophilus decoloratus (Acarina: Ixodidae). Journal of Invertebrate Pathology 38, 149151.CrossRefGoogle Scholar
HILL, D. E. ( 1998). Entomopathogenic nematodes as control agents of developmental stages of the black-legged tick, Ixodes scapularis. Journal of Parasitology 84, 11241127.CrossRefGoogle Scholar
HOOGSTRAAL, H. ( 1977). Pathogens of Acarina (ticks). In Pathogens of Medically Important Arthropods (ed. Roberts, D. W. & Strand, M. A.), pp. 337342. No. 55. Geneva, WHO.
HOWARD, L. O. ( 1907). A chalcidid parasite of a tick. Entomological News 18, 375378.Google Scholar
HOWARD, L. O. ( 1908). Another chalcidoid parasite of a tick. The Canadian Entomologist 40, 239241.CrossRefGoogle Scholar
HU, R. & HYLAND, K. E. ( 1997). Prevalence and seasonal activity of the wasp parasitoid, Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in its tick host, Ixodes scapularis (Acari: Ixodidae). Systematic and Applied Acarology 2, 95100.CrossRefGoogle Scholar
HU, R. & HYLAND, K. E. ( 1998). Effects of the feeding process of Ixodes scapularis (Acari: Ixodidae) on embryonic development of its parasitoid, Ixodiphagus hookeri (Hymenoptera: Encyrtidae). Journal of Medical Entomology 35, 10501053.CrossRefGoogle Scholar
HU, R., HYLAND, K. E. & MATHER, T. N. ( 1993). Occurrence and distribution in Rhode Island of Hunterellus hookeri (Hymenoptera: Encyrtidae), a wasp parasitoid of Ixodes dammini. Journal of Medical Entomology 30, 277280.CrossRefGoogle Scholar
HU, R., HYLAND, K. E. & OLIVER, J. H. ( 1998). A review on the use of Ixodiphagus wasps (Hymedoptera: Encyrtidae) as natural enemies for the control of ticks (Acari: Ixodidae). Systematic and Applied Acarology 3, 1928.CrossRefGoogle Scholar
JENKINS, D. W. ( 1964). Pathogens, parasites and predators of medically important arthropods. Bulletin of the World Health Organization, Supplement No. 30. pp. 1150.Google Scholar
JOHNS, R., SONENSHINE, D. E. & HYNES, W. L. ( 1998). Control of bacterial infections in the hard tick Dermacentor variabilis (Acari: Ixodidae): evidence for the existence of antimicrobial proteins in tick hemolymph. Journal of Medical Entomology 35, 458464.CrossRefGoogle Scholar
KAAYA, G. P. ( 2000). Laboratory and field evaluation of entomogenous fungi for tick control. Annals of the New York Academy of Science 916, 559564.CrossRefGoogle Scholar
KAAYA, G. P. ( 2003). Prospects for innovative methods of tick control in Africa. Insect Science and Application 23, 5967.CrossRefGoogle Scholar
KAAYA, G. P. & HASSAN, S. ( 2000). Entomogenous fungi as promising biopesticides for tick control. Experimental and Applied Acarology 24, 913926.CrossRefGoogle Scholar
KAAYA, G. P. & MWANGI, E. N. ( 1995). Control of livestock ticks in Africa: possibilities of biological control using the entomogenous fungi Beauveria bassiana and Metarhizium anisopliae. Proceedings and Abstracts, Krugers National Park, South Africa 1995, 516.Google Scholar
KAAYA, G. P., MWANGI, E. N. & OUNA, E. A. ( 1996). Prospects for biological control of livestock ticks, Rhipicephalus appendiculatus and Amblyomma variegatum, using the entomogenous fungi Beauveria bassiana and Metarhizium anisopliae. Journal of Invertebrate Pathology 67, 1520.CrossRefGoogle Scholar
KAAYA, G. P., SAMISH, M. & GLAZER, I. ( 2000). Laboratory evaluation of pathogenicity of entomopathogenic nematodes to African tick species. Annals of the New York Academy of Science 916, 303308.Google Scholar
KAISER, M. N. & HOOGSTRAAL, H. ( 1958). Hunterellus theileri Fiedler (Encyrtidae, Chalcidoidea) parasitizing an African Hyalomma tick on a migrant bird in Egypt. Journal of Parasitology 44, 392.CrossRefGoogle Scholar
KALSBEEK, V., FRANDSEN, F. & STEENBERG, T. ( 1995). Entomopathogenic fungi associated with Ixodes ricinus ticks. Experimental and Applied Acarology 19, 4551.CrossRefGoogle Scholar
KNIPLING, E. F. & STEELMAN, C. D. ( 2000). Feasibility of controlling Ixodes scapularis ticks (Acari: Ixodidae), the vector of Lyme Disease, by parasitoid augmentation. Journal of Medical Entomology 37, 645652.CrossRefGoogle Scholar
KNULLE, W. & RUDOLPH, D. ( 1982). Humidity relationships and water balance of ticks. In Physiology of Ticks (ed. Obenchain, F. D. & Galun, R.), pp. 4370. Oxford, Pergamon Press.CrossRef
KOCAN, K. M., BLOUIN, E. F., PIDHERNEY, M. S., CLAYPOOL, P. L., SAMISH, M. & GLAZER, I. ( 1998 a). Entomopathogenic nematodes as a potential biological control method for ticks. Annals of the New York Academy of Science 849, 355356.Google Scholar
KOCAN, K. M., PIDHERNEY, M. S., BLOUIN, E. F., CLAYPOOL, P. L., SAMISH, M. & GLAZER, I. ( 1998 b). Interaction of entomopathogenic nematodes (Steinernematidae) with selected species of ixodid ticks (Acari: Ixodidae). Journal of Medical Entomology 35, 514520.Google Scholar
KOK, O. B. & PETNEY, T. N. ( 1993). Small and medium sized, mammals as predators of ticks (Ixodoidea) in South Africa. Experimental and Applied Acarology 17, 733740.Google Scholar
KOLOMYETZ, U. S. ( 1950). Aspergilus fumigatus as a parasite of ticks. Priroda 39, 6465.Google Scholar
KRYLOV, B. ( 1972). Some problems in the study of fungal diseases of the bed bugs Cimex lectularius and ticks Argas persicus. Microbiol met borby s ectoparazit ptic Frunze, Ilim, 5355.Google Scholar
LARROUSSE, F., KING, A. G. & WOLBACH, S. B. ( 1928). The overwintering in Massachusetts of Ixodiohagus caucurtei. Science 67, 351353.CrossRefGoogle Scholar
LIPA, J. J. ( 1971). Microbial control of mites and ticks. In Microbial Control of Insects and Mites (ed. Burges, H. D. & Hussey, N. W.), pp. 357373. London, New York, Academic Press.
MANI, M. S. ( 1941). Studies on Indian parasitic Hymenoptera. I. Indian Journal of Entomology 3, 2536.Google Scholar
MARTIN, P. A. W. & SCHMIDTMANN, E. T. ( 1998). Isolation of aerobic microbes from Ixodes scapularis (Acari: Ixodidae), the vector of Lyme disease in the eastern United States. Journal of Economic Entomology 91, 864868.CrossRefGoogle Scholar
MASSON, C. A. & NORVAL, R. A. I. ( 1980). The ticks of Zimbabwe. I. The genus Boophilus. Zimbabwe Veterinary Journal 11, 3643.Google Scholar
MATHER, T. N., PIESMAN, J. & SPIELMAN, A. ( 1987). Absence of spirochaetes (Borrelia burgdorferi) and piroplasms (Babesia microti) in deer ticks (Ixodes dammini) parasitized by chalcid wasps (Hunterellus hookeri). Medical and Veterinary Entomology 1, 38.CrossRefGoogle Scholar
MAULEON, H., BARRE, N. & PANOMA, S. ( 1993). Pathogenicity of 17 isolates of entomophagous nematodes (Steinernematidae and Heterorhabditidae) for the ticks Amblyomma variegatum (Fabricius), Boophilus microplus (Canestrini) and Boophilus annulatus (Say). Experimental and Applied Acarology 17, 831838.CrossRefGoogle Scholar
MONTEIRO, S. G. M., BITTENCOURT, V. R. E. P., DAEMON, E. & FACCINI, J. L. H. ( 1998 a). Effect of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana on eggs of Rhipicephalus sanguineus (Acari: Ixodidae). Ciencia Rural, Santa Maria 28, 461466.Google Scholar
MONTEIRO, S. G. M., BITTENCOURT, V. R. E. P., DAEMON, E. & FACCINI, J. L. H. ( 1998 b). Pathogenicity under laboratory conditions of the fungi Beauveria bassiana and Metarhizium anisopliae on larvae of the tick Rhipicephalus sanguineus (Acari: Ixodidae). Revista Brasileira de Parasitologia Veterinaria 7, 113116.Google Scholar
MOORING, M. S. & MUNDY, P. J. ( 1996). Factors influencing host selection by Yellow-billed oxpeckers at Matoba national park, Zimbabwe. African Journal of Ecology 34, 177188.CrossRefGoogle Scholar
MUNDY, P. J. & COOK, A. W. ( 1975). Observation of the yellow-billed oxpecker Buphagus africanus in northern Nigeria. Ibis 117, 504506.CrossRefGoogle Scholar
MWANGI, E. N. ( 1991). The role of predators, parasitoids and pathogens in regulating natural populations of the non-parasitic stages of Rhipicephalus appendiculatus, Neumann and other livestock ticks, and related aspects of the tick's ecology. PhD thesis. Kenyatta University, Nairobi, Kenya.
MWANGI, E. N., DIPEOLU, O. O., NEWSON, R. M., KAAYA, G. P. & HASSAN, S. M. ( 1991 a). Predators, parasitoids and pathogens of ticks: a review. Biocontrol Science and Technology 1, 147156.Google Scholar
MWANGI, E. N., HASSAN, S. M., KAAYA, G. P. & ESSUMAN, S. ( 1997). The impact of Ixodiphagus hookeri, a tick parasitoid, on Amblyomma variegatum (Acari: Ixodidae) in a field trial in Kenya. Experimental and Applied Acarology 21, 117126.CrossRefGoogle Scholar
MWANGI, E. N. & KAAYA, G. P. ( 1997). Prospects of using tick parasitoids (Insecta) for tick management in Africa. International Journal of Acarology 23, 215219.CrossRefGoogle Scholar
MWANGI, E. N., KAAYA, G. P. & ESSUMEN, S. ( 1995). Experimental infections of the tick Rhipicephalus appendiculatus with entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae, and natural infections of some ticks with bacteria and fungi. Journal African Zoology 109, 151160.Google Scholar
MWANGI, E. N., NEWSON, R. M. & KAAYA, G. P. ( 1991 b). Predation of free-living engorged female Rhipicephalus appendiculatus. Experimental and Applied Acarology 12, 153162.Google Scholar
NAVON, A. ( 2000). Entomopathogenic bacteria: from laboratory to field application. In Bacillus thuringiensis Application in Agriculture (ed. Charles, J. F., Delecluse, A. & Nielsen-Le Roux, C.), pp. 455365. Dordrecht, Kluwer Academic Publishers.
NODA, H., MUNDERLOH, U. G. & KURTTI, T. J. ( 1997). Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Applied and Environmental Microbiology 63, 39263932.Google Scholar
NORVAL, R. A. I. & LIGHTFOOT, C. J. ( 1982). Tick problems in wildlife in Zimbabwe. Factors influencing the occurrence and abundance of Rhipicephalus appendiculatus. Zimbabwe Veterinary Journal 13, 1120.Google Scholar
OLIVER, J. H. Jr. ( 1964). A wasp parasite of the possum tick, Ixodes tasmani, in Australia. The Pan-Pacific Entomologist 40, 227230.Google Scholar
PAIAO, J. C. V., MONTEIRO, A. C. & KRONKA, S. N. ( 2001). Susceptibility of the cattle tick Boophilus microplus (Acari: Ixodidae) to isolates of the fungus Beauveria bassiana. World Journal of Microbiology and Biochemistry 17, 245251.CrossRefGoogle Scholar
PETNEY, T. N. & KOK, O. B. ( 1993). Birds as predators of ticks (Ixodoidea) in South Africa. Experimental and Applied Acarology 17, 393403.CrossRefGoogle Scholar
PETRISCHEVA, P. A. & ZHMAYEVA, Z. M. ( 1949). Natural enemies of field ticks. Zoologichesku Zhurnal 28, 479481.Google Scholar
POINAR, G. O. Jr. ( 1973). Entomogenous Nematodes. A Manual and Host List of Insect-Nematode Associations. Leiden, Belgium, E.J. Brill.
RAMAMOORTHY, R. & SCHOLL-MEEKER, D. ( 2001). Borrelia burgdorferi proteins whose expression is similarly affected by culture temperature and pH. Infection and Immunity 69, 27392742.CrossRefGoogle Scholar
REIS, R. C. S., MELO, D. R., SOUZA, E. J. & BITTENCOURT, V. R. E. P. ( 2001). In vitro action of the fungi Beauveria bassiana Vuill and Metarhizium anisopbiae Sorok on nymphs and adults of Amblyomma cajenense (Acari: Ixodidae). Arquivos Brasileiro de Medicina Veterinaria i Zootecnologia 53, 544547.CrossRefGoogle Scholar
ROBERTSON, A. & JARVIS, A. M. ( 2000). Oxpeckers in north-eastern Namibia: recent population trends and the possible negative impacts of drought and fire. Biological Conservation 92, 241247.CrossRefGoogle Scholar
SAMISH, M. & ALEKSEEV, E. A. ( 2001). Arthropods as predators of ticks (Ixodoidea). Journal of Medical Entomology 38, 111.CrossRefGoogle Scholar
SAMISH, M., ALEKSEEV, E. A. & GLAZER, I. ( 1995). The development of entomopathogenic nematodes in the tick B. annulatus. In The Second International Conference on Tick Borne Pathogens at the Host Vector Interface: A Global Perspective (ed. Coons, L. & Rothschild, M.), pp. 24. Krugel National Park, South Africa: Proceedings and Abstracts. S.I.: The conference, 1998.
SAMISH, M., ALEKSEEV, E. A. & GLAZER, I. ( 1998). The effect of soil composition on anti-tick activity of entomopathogenic nematodes. Annals of the New York Academy of Science 849, 402403.CrossRefGoogle Scholar
SAMISH, M., ALEKSEEV, E. A. & GLAZER, I. ( 1999 a). Efficacy of entomopathogenic nematode strains against engorged Boophilus annulatus females (Acari: Ixodidae) under simulated field conditions. Journal of Medical Entomology 36, 727732.Google Scholar
SAMISH, M., ALEKSEEV, E. A. & GLAZER, I. ( 1999 b). Interaction between ticks (Acari: Ixodidae) and pathogenic nematodes (Nematoda): susceptibility of tick species at various developmental stages. Journal of Medical Entomology 36, 733740.Google Scholar
SAMISH, M., ALEKSEEV, E. A. & GLAZER, I. ( 2000 a). Biocontrol of ticks by entomopathogenic nematodes. Annals of the New York Academy of Science 916, 589594.Google Scholar
SAMISH, M., ALEKSEEV, E. A. & GLAZER, I. ( 2000 b). Mortality rate of adult ticks due to infection by entomopathogenic nematodes. Journal of Parasitology 86, 679684.Google Scholar
SAMISH, M. & GLAZER, I. ( 1992). Infectivity of entomopathogenic nematodes (Stainernematidae and Heterorhabditidae) to female ticks of Boophilus annulatus (Arachenida, Ixodidae). Journal of Medical Entomology 29, 614618.CrossRefGoogle Scholar
SAMISH, M., GINDIN, G., ALEKSEEV, E. & GLAZER, I. ( 2001). Pathogenicity of entomopathogenic fungi to different developmental stages of Rhipicephalus sanguineus. Journal of Parasitology 87, 13551359.CrossRefGoogle Scholar
SAMISH, M. & GLAZER, I. ( 2001). Entomopathogenic nematodes for the biocontrol of ticks. Trends in Parasitology 17, 368371.CrossRefGoogle Scholar
SAMISH, M. & REHACEK, J. ( 1999). Pathogens and predators of ticks and their potential in biological control. Annual Review of Entomology 44, 159182.CrossRefGoogle Scholar
SAMSINAKOVA, A. ( 1957). Beauveria globulifera (SPEG) Pic. as a parasite of the tick Ixodes ricinus L. Zoologicke Listi 20, 329330.Google Scholar
SAMSINAKOVA, A., KALALOVA, S., DANIEL, M., DUSBABEK, F., HOUZAKOVA, E. & CERNY, V. ( 1974). Entomogenous fungi associated with the tick Ixodes ricinus. Folia Prarasitologica (Praha) 21, 3948.Google Scholar
SAMUEL, W. M. & WELCH, D. A. ( 1991). Winter ticks on moose and other ungulates: factors influencing their population size. Alces 27, 169182.Google Scholar
SEBESTA, K., FARKAS, J., HORSKA, K. & VANKOVA, J. ( 1981). Thuringiensin, the beta-exotoxin of Bacillus thuringiensis. In Microbial Control of Pests and Plant Diseases (1970–1980) ( ed. Burges H. D.), pp. 249281. New York, Academic Press.
SEWIFY, G. H. & HABIB, S. M. ( 2001). Biological control of the tick fowl Argas persicargas persicus by the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopbiae. Journal of Pest Science 74, 121123.Google Scholar
SHELTON, A. M. & ROUSH, R. T. ( 2000). Resistance to insect pathogens and strategies to manage resistance. In Field Manual of Techniques in Invertebrate Pathology (ed. Lacy, L. A. & Kaaya, H. K.), pp. 829845. Dordrecht, Kluwer Academic Publishers.CrossRef
SMITH, C. N. & COLE, M. M. ( 1943). Studies of parasites of the American dog tick. Journal of Economic Entomology 36, 469472.Google Scholar
SONENSHINE, D. E. ( 1991). Biology of Ticks. Vol. 1. Oxford, Oxford University Press.
STAFFORD, K. C. III, DENICOLA, A. J. & KILPATRICK, H. J. ( 2003). Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with reduction of white-tailed deer. Journal of Medical Entomology 40, 642652.CrossRefGoogle Scholar
STAFFORD, K. C. III, DENICOLA, A. J. & MAGNARELLI, L. A. ( 1996). Presence of Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in two Connecticut populations of Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 33, 183188.CrossRefGoogle Scholar
STAFFORD, K. C. & KITRON, U. ( 2002). Environmental management for Lyme Borreliosis control. In Lyme Borreliosis Biology, Epidemiology and Control. ( ed. Gray, J. S., Kahl, O., Lane, R. S. & Stanek, G.), pp. 301334. Oxford, UK, CABI.CrossRef
STEINHAUS, E. A. & MARSH, G. A. ( 1962). Report of diagnoses of diseased insects 1951–1961. Hilgardia 33, 349390.CrossRefGoogle Scholar
STUTTERHEIM, C. & BROOKE, R. ( 1981). Past and present ecological distribution of the yellow billed oxpecker in South Africa. African Journal of Zoology 16, 4449.Google Scholar
STUTTERHEIM, C. J. & STUTTERHEIM, I. M. ( 1980). Evidence of an increase in a red-billed oxpecker population in the Kruger National Park. South African Journal of Zoology 15, 284.CrossRefGoogle Scholar
STUTTERHEIM, I. M., BEZUIDENHOUT, J. D. & ELLIOTT, E. G. R. ( 1988). Comparative feeding behavior and food preferences of oxpeckers (Buphagus erythrorhynchus and B. africanus) in captivity. Onderstepoort Journal of Veterinary Research 55, 173179.Google Scholar
SYMONDSON, W. O. C. SUNDERLAND, K. D. & GREENSTONE, M. H. ( 2002). Can generalist predators be effective biocontrol agents? Annual Revue of Entomology 47, 561594.Google Scholar
TAKASU, K., TAKANO, S.-I., SASAKI, M., YAGI, S. & NAKAMURA, S. ( 2003). Host recognition by the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae). Environmental Entomology 32, 614617.CrossRefGoogle Scholar
TRJAPITZIN, V. A. ( 1985). Natural enemies of Ixodes persulcatus. In Taiga Tick, Ixodes persulcatus Schulze (Acarina, Ixodidae) – Morphology, Systematics, Ecology, Medical Importance (ed. Filippova, N. A.), pp. 334347. Leningrad, Russia Nauka Publishers.
VAN DRIESCHE, R. G. & BELLOWS, T. S. J. R. ( 1996). Biological Control. New York, Chapman & Hall.CrossRef
VAN SOMEREN, V. D. ( 1951). The red billed oxpecker and its relation to stock in Kenya. East African Agricultural Journal 17, 111.CrossRefGoogle Scholar
VERISSIMO, C. J. ( 1995). Natural enemies of the cattle parasitic tick. Agropecuaria Catarinense 8, 3537.Google Scholar
WEEKS, P. ( 1999). Interaction between Red-billed oxpeckers, Buphagus erythrorhynchus and domestic cattle, Bos taurus, in Zimbabwe. Animal Behaviour 58, 12531259.CrossRefGoogle Scholar
WYSOKI, M. ( 1998). Problems and trends of agricultural entomology at the end of the 2nd millennium. Bollettino del Laboratorio di Entomologia Agria ‘Fillipo Silvestri’ 54, 89143.Google Scholar
ZANGI, G. ( 2003). Tick Control by Means of Entomopathogenic Nematodes and Fungi. MSc thesis. The Hebrew University of Jerusalem, Israel.
ZHIOUA, E., BROWNING, M., JOHNSON, P. W., GINSBERG, H. S. & LEBRUN, R. A. ( 1997). Pathogenicity of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) to Ixodes scapularis (Acari: Ixodidae). Journal of Parasitology 83, 815818.CrossRefGoogle Scholar
ZHIOUA, E., GINSBERG, H. S., HUMBER, R. A. & LEBRUN, R. A. ( 1999 a). Preliminary survey for entomopathogenic fungi associated with Ixodes scapularis (Acari: Ixodidae) in southern New York and New England, USA. Journal of Medical Entomology 36, 635637.Google Scholar
ZHIOUA, E., HEYER, K., BROWNING, M., GINSBERG, H. S. & LEBRUN, R. A. ( 1999 b). Pathogenicity of Bacillus thuringiensis variety kurstaki to Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 36, 900902.Google Scholar
ZHIOUA, E., LEBRUN, R. A., GINSBERG, H. S. & AESCHLIMANN, A. ( 1995). Pathogenicity of Steinernema carpocapsae and S. glaseri (Nematoda: Steinernematidae) to Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 32, 900905.Google Scholar