Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T06:40:05.544Z Has data issue: false hasContentIssue false
  • English
  • Français

Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors

Published online by Cambridge University Press:  19 April 2005

S. E. RANDOLPH
S. E. RANDOLPH
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

The population ecology of ticks is fundamental to the spatial and temporal variation in the risk of infection by tick-borne pathogens. Tick population dynamics can only be fully understood by quantifying the rates of the demographic processes, which are influenced by both abiotic (climatic) factors acting on the free-living tick stages and biotic (host) responses to the tick as a parasite. Within the framework of a population model, I review methods and results of attempts to quantify (1) rates of tick development and the probability of diapause, (2) the probability of questing for hosts by unfed ticks, (3) the probability of ticks attaching to a host, and (4) tick mortality rates. Biologically, these processes involve the physiological and behavioural response of ticks to temperature, moisture stress and day length that result in specific patterns of seasonal population dynamics and host relationships. Temperate and tropical patterns will be illustrated with reference mostly to Ixodes ricinus and Rhipicephalus appendiculatus, respectively.

Keywords

Ticksecologyepidemiologydemographic processespopulation models
Type
Research Article
Information
Parasitology , Volume 129 , Issue S1 , October 2004 , pp. S37 - S65
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., DUBININA, H. V., RIJPKEMA, S. G. T. & SCHOULS, L. M. ( 1999). Sexual transmission of Borrelia garinii by male Ixodes persulcatus ticks (Acari, Ixodidae). Experimental and Applied Acarology 23, 165–169.CrossRefGoogle Scholar
ALLAN, B. F., KEESING, F. & OSTFELD, R. S. ( 2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267–272.CrossRefGoogle Scholar
ANDERSON, J. F. ( 1991). Epizootiology of Lyme borreliosis. Scandinavian Journal of Infectious Diseases Supplement 77, 23–34.Google Scholar
ANDERSON, R. M. & GORDON, D. M. ( 1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.CrossRefGoogle Scholar
ANDERSON, R. M. & MAY, R. M. ( 1978). Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–249.Google Scholar
APPERSON, C. S., LEVINE, J. F., EVANS, T. L., BRASWELL, A. & HELLER, J. ( 1993). Relative utilization of reptiles and rodents as hosts by immature Ixodes scapularis (Acari: Ixodidae) in the coastal plain of North Carolina, USA. Experimental and Applied Acarology 17, 719–731.Google Scholar
BEGON, M., HARPER, J. L. & TOWNSEND, C. R. ( 1996). Ecology (3rd edn.). Oxford, Blackwell Scientific Publications.
BELOZEROV, V. N. ( 1967). [Larval diapause in the tick Ixodes ricinus L and its dependence on external conditions. IV. Interactions between exogenous and endogenous factors in the regulation of the larval diapause.] (In Russian). Entomological Review 46, 447–451.Google Scholar
BELOZEROV, V. N. ( 1970). [Nymphal diapause in the tick Ixodes ricinus L. (Ixodidae). III. Photoperiodic reaction in unfed nymphs.] (In Russian.) Parazitologiya 4, 139–145.Google Scholar
BELOZEROV, V. N. ( 1982). Diapause and biological rhythms in ticks. In Physiology of Ticks ( ed. Obenchain, F. D. & Galun, R.), pp. 469–500. Oxford, Pergamon Press.CrossRef
BELOZEROV, V. N. ( 1998 a). Role of two-step photoperiodic reaction in the control of development and diapause in the nymphs of Ixodes persulcatus. Russian Journal of Zoology 2, 414–418.Google Scholar
BELOZEROV, V. N. ( 1998 b). Dynamics of gas exchange during development of Ixodid ticks: III. Dynamics of gas exchange in nymphs of the Ixodid ticks Hyalomma anatolicum Koch (Acari, Ixodidae) during active development and developmental diapause. Entomological Review 78, 197–205.Google Scholar
BELOZEROV, V. N. & NAUMOV, R. L. ( 2001). Photoperiodic control of nymphal diapause in the North American tick, Ixodes (Ixodes) scapularis Say (Acari: Ixodidae). In IVth European Workshop of Invertebrate Ecophysiology ( ed. Kipyatkov, V. E.), p. 69. St Petersburg, Russia.
BERKVENS, D. L., PEGRAM, R. G. & BRANDT, J. R. A. ( 1995). A study of the diapausing behaviour of Rhipicephalus appendiculatus and R. zambesiensis under quasi-natural conditions in Zambia. Medical and Veterinary Entomology 9, 307–315.Google Scholar
BERTRAND, M. R. & WILSON, M. L. ( 1997). Microhabitat-independent regional differences in survival of unfed Ixodes scapularis nymphs (Acari: Ixodidae) in Connecticut. Journal of Medical Entomology 34, 167–172.CrossRefGoogle Scholar
BRANAGAN, D. ( 1973). Observations on the development and survival of the Ixodid tick Rhipicephalus appendiculatus Neumann, 1901 under quasi-natural conditions in Kenya. Tropical Animal Health and Production 5, 153–165.CrossRefGoogle Scholar
CAMPBELL, J. A. ( 1948). The life history and development of the sheep tick Ixodes ricinus Linaeus in Scotland, under natural and controlled conditions. PhD thesis, University of Edinburgh.
CERNY, M., DANIEL, M. & ROSICKY, B. ( 1974). Some features of the developmental cycle of the tick Ixodes ricinus (L.) (Acarina: Ixodidae). Folia Parasitologica 21, 85–87.Google Scholar
CHIERA, J. W., NEWSON, R. M. & CUNNINGHAM, M. P. ( 1985). Cumulative effects of host resistance on Rhipicephalus appendiculatus Neumann (Acarina: Ixodidae) in the laboratory. Parasitology 90, 401–408.CrossRefGoogle Scholar
CHMELA, J. ( 1969). On the developmental cycle of the common tick (Ixodes ricinus L.) in the north-Moravian natural focus of tick-borne encephalitis. Folia Parasitologica 16, 313–319.Google Scholar
CLARK, D. D. ( 1995). Lower temperature limits for activity of several ixodid ticks (Acari: Ixodidae): effects of body size and rate of temperature change. Journal of Medical Entomology 32, 449–452.CrossRefGoogle Scholar
clayton, d. h. & moore, j. (ed.) ( 1997). Host–Parasite Evolution. Oxford, Oxford University Press.
CRAINE, N. G., RANDOLPH, S. E. & NUTTALL, P. A. ( 1995). Seasonal variation in the role of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochaete, in a British woodland. Folia Parasitologica 42, 73–80.Google Scholar
CROFTON, H. D. ( 1971 a). A quantitative approach to parasitism. Parasitology 62, 179–193.Google Scholar
CROFTON, H. D. ( 1971 b). A model of host–parasite relationships. Parasitology 63, 343–364.Google Scholar
CUMMING, G. S. ( 1996). The evolutionary ecology of African ticks. DPhil thesis, University of Oxford.
CUMMING, G. S. ( 1998). Host preference in African ticks (Acari: Ixodidae): a quantitative data set. Bulletin of Entomological Research 88, 379–406.CrossRefGoogle Scholar
CUMMING, G. S. ( 1999). Host distributions do not limit the species ranges of most African ticks (Acari: Ixodida). Bulletin of Entomological Research 89, 303–327.CrossRefGoogle Scholar
CUMMING, G. S. ( 2002). Comparing climate and vegetation as limiting factors for species ranges of African ticks. Ecology 83, 255–268.CrossRefGoogle Scholar
DANIEL, M., CERNY, V., DUSBABEK, F., HONZAKOVA, E. & OLEJNICEK, J. ( 1976). Influence of microclimate on the life cycle of the common tick Ixodes ricinus (L.) in thermophilic oak forest. Folia Parasitologica 23, 327–342.Google Scholar
DANIEL, M., CERNY, V., DUSBABEK, F., HONZAKOVA, E. & OLEJNICEK, J. ( 1977). Influence of microclimate on the life cycle of the common tick Ixodes ricinus (L.) in an open area in comparison with forest habitats. Folia Parasitologica 24, 149–160.Google Scholar
DANIEL, M. & KOLAR, J. ( 1990). Using satellite data to forecast the occurrence of the common tick Ixodes ricinus (L.). Journal of Hygiene, Epidemiology, Microbiology and Immunology 45, 243–252.Google Scholar
DANIEL, M., KOLAR, J., ZEMAN, P., PAVELKA, K. & SADLO, J. ( 1998). Predictive map of Ixodes ricinus high-incidence habitats and a tick-borne encephalitis risk assessment using satellite data. Experimental and Applied Acarology 22, 417–433.CrossRefGoogle Scholar
DANIELOVÁ, V. ( 2002). Natural foci of tick-borne encephalitis and prerequisites for their existence. International Journal of Medical Microbiology 291, S183–S186.CrossRefGoogle Scholar
DANIELOVÁ, V. & HOLUBOVÁ, J. ( 1991). Transovarial transmission rate of tick-borne encephalitis virus in Ixodes ricinus ticks. In Modern Acarology ( ed. Dusbabek, F. & Bukva, V.), pp. 7–10. The Hague, Academia, Prague and SPB Academic Publishing.
DANIELOVÁ, V., HOLUBOVA, J., PEJCOCH, M. & DANIEL, M. ( 2002). Potential significance of transovarial transmission in the circulation of tick-borne encephalitis virus. Folia Parasitologica 49, 323–325.CrossRefGoogle Scholar
DANIELS, T. J., FALCO, R. C., CURRAN, K. L. & FISH, D. ( 1996). Timing of Ixodes scapularis (Acari: Ixodidae) oviposition and larval activity in southern New York. Journal of Medical Entomology 33, 140–147.CrossRefGoogle Scholar
DANIELS, T. J., FALCO, R. C. & FISH, D. ( 2000). Estimating population size and drag sampling efficiency for the blacklegged tick (Acari: Ixodidae). Journal of Medical Entomology 37, 357–363.CrossRefGoogle Scholar
DANIELS, T. J. & FISH, D. ( 1995). Effect of deer exclusion on the abundance of immature Ixodes scapularis (Acari: Ixodidae) parasitizing small and medium-sized mammals. Journal of Medical Entomology 32, 5–11.CrossRefGoogle Scholar
DISTER, S. W., FISH, D., BROS, S. M., FRANK, D. H. & WOOD, B. L. ( 1997). Landscape characterization of peridomestic risk for Lyme disease using satellite imagery. American Journal of Tropical Medicine and Hygiene 57, 687–692.CrossRefGoogle Scholar
DIZIJ, A. & KURTENBACH, K. ( 1995). Clethrionomys glareolus, but not Apodemus flavicollis, acquires resistance to Ixodes ricinus L., the main European vector of Borrelia burgdorferi. Parasite Immunology 17, 177–183.Google Scholar
EISEN, L., EISEN, R. J. & LANE, R. S. ( 2002). Seasonal activity patterns of Ixodes pacificus nymphs in relation to climatic conditions. Medical and Veterinary Entomology 16, 235–244.CrossRefGoogle Scholar
ESTRADA-PEÑA, A. ( 1998). Geostatistics and remote sensing as predictive tools of tick distribution: a cokriging system to estimate Ixodes scapularis (Acari: Ixodidae) habitat suitability in the United States and Canada from Advanced Very High Resolution Radiometer satellite imagery. Journal of Medical Entomology 35, 989–995.CrossRefGoogle Scholar
ESTRADA-PEÑA, A. ( 1999). Geostatistics as predictive tools to estimate Ixodes ricinus (Acari: Ixodidae) habitat suitability in the western Paleartic from AVHRR satellite imagery. Experimental and Applied Acarology 23, 337–349.CrossRefGoogle Scholar
FALCO, R. C., DANIELS, T. J. & FISH, D. ( 1995). Increase in abundance of immature Ixodes scapularis (Acari: Ixodidae) in an emergent Lyme disease endemic area. Journal of Medical Entomology 32, 522–526.CrossRefGoogle Scholar
FIELDEN, L. J. & LIGHTON, J. R. B. ( 1996). Effects of water stress and relative humidity on ventilation in the tick Dermacentor andersoni (Acari: Ixodidae). Physiological Zoology 69, 599–617.CrossRefGoogle Scholar
FILIPPOVA, N. A. (ed.) ( 1985). [Taiga Tick Ixodes persulcatus Schulze (Acarina, Ixodidae).] (In Russian). Leningrad: Nauka.
FIVAZ, B. H. & NORVAL, R. A. I. ( 1990). Immunity of the ox to the brown ear tick Rhipicephalus appendiculatus. Experimental and Applied Acarology 8, 51–63.CrossRefGoogle Scholar
FOURIE, L. J., BELOZEROV, V. N. & NEEDHAM, G. R. ( 2001). Ixodes rubicundus nymphs are short-day diapause-induced ticks with thermolabile sensitivity and desiccation resistance. Medical and Veterinary Entomology 15, 335–341.CrossRefGoogle Scholar
GAEDE, K. & KNÜLLE, W. ( 1997). On the mechanism of water vapour sorption from unsaturated atmospheres by ticks. Journal of Experimental Biology 200, 1491–1498.Google Scholar
GIGON, F. ( 1985). Biologie d'Ixodes ricinus L. sur le Plateau Suisse – une contribution a l'écologie de ce vecteur. MS thesis, Université de Neuchâtel, Switzerland.
GILOT, B., BONNEFILLE, M., DEGEILH, B., BEAUCOURNU, J.-C., PICHOT, J. & GUIGUEN, C. ( 1994). La colonisation des massifs forestiers par Ixodes ricinus (Linne, 1758) en France: utilisation du chevreuil, Capreolus capreolus (L. 1758) comme marqueur biologique. Parasite 1, 81–86.Google Scholar
GLASS, G. E., SCHWARZ, B. S., MORGAN III, J. M., JOHNSON, D. T., NOY, P. M. & ISRAEL, E. ( 1995). Environmental risk factor for Lyme disease identified with geographic information systems. American Journal of Public Health 85, 944–948.CrossRefGoogle Scholar
GRAY, J. S. ( 1981). The fecundity of Ixodes ricinus (L.) (Acarina: Ixodidae) and the mortality of its developmental stages under field conditions. Bulletin of Entomological Research 71, 533–542.Google Scholar
GRAY, J. S. ( 1982). The development and questing activity of Ixodes ricinus (L.) (Acari: Ixodidae) under field conditions in Ireland. Bulletin of Entomological Research 72, 263–270.Google Scholar
GRAY, J. S. ( 1985). Studies on the larval activity of the tick Ixodes ricinus L. in Co. Wicklow, Ireland. Experimental and Applied Acarology 1, 307–316.CrossRefGoogle Scholar
GRAY, J. S., KAHL, O., JANETZKI, C. & STEIN, J. ( 1992). Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. Journal of Medical Entomology 29, 915–920.CrossRefGoogle Scholar
GRAY, J. S., VON STEDINGK, L. V. & GURTELSCHMID, M. E. A. ( 2002). Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. Journal of Clinical Microbiology 40, 1259–1263.CrossRefGoogle Scholar
GUERRA, M., WALKER, E., JONES, C. J., PASKEWITZ, S., CORTINAS, M. R., SANCIL, A., BECK, L., BOBO, M. & KITRON, U. ( 2002). Predicting the risk of Lyme disease: habitat suitability for Ixodes scapularis in the north central United States. Emerging Infectious Diseases 8, 289–297.CrossRefGoogle Scholar
HASIBEDER, G. & DYE, C. M. ( 1988). Population dynamics of mosquito-borne disease: persistence in a completely heterogeneous environment. Theoretical Population Biology 33, 31–53.CrossRefGoogle Scholar
HOODLESS, A. N., KURTENBACH, K., NUTTALL, P. A. & RANDOLPH, S. E. ( 2002). The impact of ticks on pheasant territoriality. Oikos 96, 245–250.CrossRefGoogle Scholar
HOOGSTRAAL, H. ( 1981). Changing patterns of tick-borne diseases in modern society. Annual Review of Entomology 26, 75–99.CrossRefGoogle Scholar
HUDSON, P. J., RIZZOLI, A., ROSA, R., CHEMINI, C., JONES, L. D. & GOULD, E. A. ( 2001). Tick-borne encephalitis virus in northern Italy: molecular analysis, relationships with density and seasonal dynamics of Ixodes ricinus. Medical and Veterinary Entomology 15, 304–313.CrossRefGoogle Scholar
HUGH-JONES, M., BARRE, N., NELSON, G., WEHNES, K., WARNER, J., GARVIN, J. & GARRIS, G. ( 1992). Landsat-TM identification of Amblyomma variegatun (Acari: Ixodidae) habitats in Guadeloupe. Remote Sensing of the Environment 40, 43–55.CrossRefGoogle Scholar
HUGHES, V. L. & RANDOLPH, S. E. ( 2001 a). Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. Journal of Parasitology 87, 49–54.Google Scholar
HUGHES, V. L. & RANDOLPH, S. E. ( 2001 b). Testosterone increases the transmission potential of tick-borne parasites. Parasitology 123, 365–371.Google Scholar
HUTCHINSON, M. F., NIX, H. A., McMAHON, J. P. & ORD, K. D. ( 1995). Africa. A topographic and climate database. In Centre for Resources and Environmental Studies, Canberra, The Australian National University.
JENSEN, P. M. & FRANDSEN, F. ( 2000). Temporal risk assessment for Lyme borreliosis in Denmark. Scandinavian Journal of Infectious Diseases 35, 539–544.Google Scholar
JENSEN, P. M., HANSEN, H. & FRANDSEN, F. ( 2000). Spatial risk assessment for Lyme borreliosis in Denmark. Scandinavian Journal of Infectious Diseases 35, 545–550.Google Scholar
JONGEJAN, F., PEGRAM, R. G., ZIVKOVIC, D., HENSEN, E. J., MWASE, E. T., THIELEMANS, M. J. C., COSSE, A., NIEWOLD, T. A., SAID, A. E. & UILENBERG, G. ( 1989). Monitoring of naturally acquired and artificially induced immunity to Amblyomma variegatum and Rhipicephalus appendiculatus ticks under field and laboratory conditions. Experimental and Applied Acarology 7, 181–189.CrossRefGoogle Scholar
KAISER, M. N., SUTHERST, R. W. & BOURNE, A. S. ( 1982). Relationship between ticks and zebu cattle in southern Uganda. Tropical Animal Health Production 14, 63–74.CrossRefGoogle Scholar
KAISER, M. N., SUTHERST, R. W. & BOURNE, A. S. ( 1991). Tick (Acarina: Ixodidae) infestations on zebu cattle in northern Uganda. Bulletin of Entomological Research 81, 257–262.CrossRefGoogle Scholar
KAISER, M. N., SUTHERST, R. W., BOURNE, A. S., GORISSEN, L. & FLOYD, R. B. ( 1988). Population dynamics of ticks on Ankole cattle in five ecological zones in Burundi and strategies for their control. Preventive Veterinary Medicine 6, 199–222.CrossRefGoogle Scholar
KEMP, D. H. ( 1968). Physiological studies on hard ticks Ixodidae. PhD thesis, University of Edinburgh.
KITRON, U., JONES, C. J., BOUSEMAN, J. K., NELSON, J. A. & BAUMGARTNER, D. L. ( 1992). Spatial analysis of the distribution of Ixodes dammini (Acari: Ixodidae) on white-tailed deer in Ogle county, Illinois. Journal of Medical Entomology 29, 259–266.CrossRefGoogle Scholar
KITRON, U. & KAZMIERCZAK, J. J. ( 1997). Spatial analysis of the distribution of Lyme disease in Wisconsin. American Journal of Epidemiology 145, 558–566.CrossRefGoogle Scholar
KLOMPEN, J. S. H., BLACK, W. C., KEIRANS, J. E. & OLIVER, J. H. ( 1996). Evolution of ticks. Annual Review of Entomology 41, 141–161.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. 43–70. Oxford, Pergamon Press.CrossRef
KORENBERG, E. I. ( 2000). Seasonal population dynamics of Ixodes ticks and tick-borne encephalitis virus. Experimental and Applied Acarology 24, 665–681.CrossRefGoogle Scholar
KORENBERG, E. I. & KOVALEVSKII, Y. V. ( 1994). A model for relationships among the tick-borne encephalitis virus, its main vectors, and hosts. Advances in Disease Vector Research 10, 65–92.CrossRefGoogle Scholar
KURTENBACH, K., PEACEY, M. F., RIJPKEMA, S. G. T., HOODLESS, A. N., NUTTALL, P. A. & RANDOLPH, S. E. ( 1998). Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Applied and Environmental Microbiology 64, 1169–1174.Google Scholar
LABUDA, M., AUSTYN, J. M., ZUFFOVA, E., KOZUCH, O., FUCHSBERGER, N., LYSY, J. & NUTTALL, P. A. ( 1996). Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology 219, 357–366.CrossRefGoogle Scholar
LABUDA, M., JONES, L. D., WILLIAMS, T., DANIELOVA, V. & NUTTALL, P. A. ( 1993 a). Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. Journal of Medical Entomology 30, 295–299.Google Scholar
LABUDA, M., KOZUCH, O., ZUFFOVA, E., ELECKOVA, E., HAILS, R. S. & NUTTALL, P. A. ( 1997). Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235, 138–143.CrossRefGoogle Scholar
LABUDA, M., NUTTALL, P. A., KOZUCH, O., ELECKOVA, E., WILLIAMS, T., ZUFFOVA, E. & SABO, A. ( 1993 b). Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49, 802–805.Google Scholar
LANE, R. S. & QUISTAD, G. B. ( 1998). Borreliacidal factor in the blood of the Western Fence Lizard (Sceloporus occidentalis). Journal of Parasitology 84, 29–34.CrossRefGoogle Scholar
LEES, A. D. & MILNE, A. ( 1951). The seasonal and diurnal activities of individual sheep ticks (Ixodes ricinus). Parasitology 41, 180–209.CrossRefGoogle Scholar
LIGHTON, J. R. B. & FIELDEN, L. J. ( 1995). Mass scaling of standard metabolism in ticks – a valid case of low metabolic rates in sit-and-wait strategists. Physiological Zoology 68, 43–62.CrossRefGoogle Scholar
LOGIUDICE, K., OSTFELD, R. S., SCHMIDT, K. A. & KEESING, F. ( 2003). The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, USA 100, 567–571.CrossRefGoogle Scholar
LOYE, J. E. & LANE, R. S. ( 1988). Questing behavior of Ixodes pacificus (Acari: Ixodidae) in relation to meteorological and seasonal factors. Journal of Medical Entomology 25, 391–398.CrossRefGoogle Scholar
MACLEOD, J. ( 1935). Ixodes ricinus in relation to its physical environment. II. The factors governing survival and activity. Parasitology 27, 123–144.Google Scholar
MACLEOD, J. ( 1936). Ixodes ricinus in relation to its physical environment. IV. An analysis of the ecological complexes controlling distribution and activities. Parasitology 28, 295–319.CrossRefGoogle Scholar
MACLEOD, J. ( 1970). Tick infestation patterns in the Southern Province of Zambia. Bulletin of Entomological Research 60, 253–274.CrossRefGoogle Scholar
MADDER, M., SPEYBROECK, N., BRANDT, J. & BERKVENS, D. ( 1999). Diapause induction in adults of three Rhipicephalus appendiculatus stocks. Experimental and Applied Acarology 23, 961–968.CrossRefGoogle Scholar
MATUSCHKA, F.-R., FISCHER, P., HEILER, M., RICHTER, D. & SPIELMAN, A. ( 1992). Capacity of European animals as reservoir hosts for the Lyme disease spirochete. Journal of Infectious Diseases 165, 479–483.CrossRefGoogle Scholar
MATUSCHKA, F.-R., SCHINKEL, T. W., KLUG, B., SPIELMAN, A. & RICHTER, D. ( 2000). Relative importance of European rabbits for Lyme disease spirochaetes. Parasitology 121, 297–302.CrossRefGoogle Scholar
MILNE, A. ( 1949). The ecology of the sheep tick, Ixodes ricinus L. Host relationships of the tick. Part 2. Observations on hill and moorland grazings in northern England. Parasitology 39, 173–194.Google Scholar
MOORE, S. L. & WILSON, K. ( 2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018.CrossRefGoogle Scholar
MORAN, M. C., NIGARURA, G. & PEGRAM, R. G. ( 1996). An assessment of host resistance to ticks on cross-bred cattle in Burundi. Medical and Veterinary Entomology 10, 12–18.CrossRefGoogle Scholar
NEEDHAM, G. R. & TEEL, P. D. ( 1991). Off-host physiological ecology of ixodid ticks. Annual Review of Entomology 36, 659–681.CrossRefGoogle Scholar
NEWSON, R. M. ( 1978). The life cycle of Rhipicephalus appendiculatus on the Kenyan coast. In Tick-borne Diseases and their Vectors ( ed. Wilde, J. K. H.), pp. 46–50. Edinburgh, CTVM, University of Edinburgh.
NICHOLSON, M. C. & MATHER, T. N. ( 1996). Methods for evaluating Lyme disease risks using geographical information systems and geospatial analysis. Journal of Medical Entomology 33, 711–720.CrossRefGoogle Scholar
NORVAL, R. A. I., LAWRENCE, J. A., YOUNG, A. S., PERRY, B. D., DOLAN, T. T. & SCOTT, J. ( 1991). Theileria parva: influence of vector, parasite and host relationships on the epidemiology of theileriosis in southern Africa. Parasitology 102, 347–356.CrossRefGoogle Scholar
NUTTALL, P. A. & LABUDA, M. ( 1994). Tick-borne encephalitides. In Ecological Dynamics of Tick-borne Zoonoses ( ed. Sonenshine, D. E. & Mather, T. N.), pp. 351–391. New York, Oxford, Oxford University Press.
OCHANDA, H., YOUNG, A. S., WELLS, C., MEDLEY, G. F. & PERRY, B. D. ( 1996). Comparison of the transmission of Theileria parva between different instars of Rhipicephalus appendiculatus. Parasitology 113, 243–253.CrossRefGoogle Scholar
OGDEN, N. H., HAILS, R. S. & NUTTALL, P. A. ( 1998). Interstadial variation in the attachment sites of Ixodes ricinus ticks on sheep. Experimental and Applied Acarology 22, 227–232.CrossRefGoogle Scholar
OGDEN, N. H., RANDOLPH, S. E. & NUTTALL, P. A. ( 1997). Natural Lyme disease cycle maintained via sheep by co-feeding ticks. Parasitology 115, 591–599.CrossRefGoogle Scholar
PACALA, S. W. & DOBSON, A. P. ( 1988). The relation between the number of parasites/host and host age: population dynamics causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle Scholar
PADGETT, K. A. & LANE, R. S. ( 2001). Life cycle of Ixodes pacificus (Acari: Ixodidae): timing of development processes under field and laboratory conditions. Journal of Medical Entomology 38, 684–693.CrossRefGoogle Scholar
PEGRAM, R. G. & BANDA, D. S. ( 1990). Ecology and phenology of cattle ticks in Zambia: development and survival of free-living stages. Experimental and Applied Acarology 8, 291–293.CrossRefGoogle Scholar
PERRET, J.-L., GUERIN, P. M., DIEHL, P.-A., VLIMANT, M. & GERN, L. ( 2003). Darkness favours mobility and saturation deficit limits questing duration in Ixodes ricinus, the tick vector of Lyme disease in Europe. Journal of Experimental Biology 206, 1809–1815.CrossRefGoogle Scholar
PERRET, J.-L., GUIGOZ, E., RAIS, O. & GERN, L. ( 2000). Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borrelosis-endemic area (Switzerland). Parasitology Research 86, 554–557.CrossRefGoogle Scholar
PETERS, A. ( 2000). Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proceedings of the Royal Society of London, B 267, 883–889.CrossRefGoogle Scholar
PIESMAN, J. ( 2002). Ecology of Borrelia burgdorferi sensu lato in North America. In Lyme Borreliosis Biology, Epidemiology and Control ( ed. Gray, J. S., Kahl, O., Lane, R. S. & Stanek, G.), pp. 223–250. Wallingford, CABI.CrossRef
RAND, P. W., LUBELCZYK, C., LAVIGNE, G. R., ELIAS, S., HOLMAN, M. S., LACOMBE, E. H. & SMITH, R. P. J. ( 2003). Deer density and the abundance of Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 40, 179–184.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 1975). Patterns of distribution of the tick Ixodes trianguliceps Birula on its hosts. Journal of Animal Ecology 44, 451–474.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 1977). Changing spatial relationships in a population of Apodemus sylvaticus with the onset of breeding. Journal of Animal Ecology 46, 653–676.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 1979). Population regulation in ticks: the role of acquired resistance in natural and unnatural hosts. Parasitology 79, 141–156.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 1993). Climate, satellite imagery and the seasonal abundance of the tick Rhipicephalus appendiculatus in southern Africa: a new perspective. Medical and Veterinary Entomologyy 7, 243–258.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 1994 a). Population dynamics and density-dependent seasonal mortality indices of the tick Rhipicephalus appendiculatus in east and southern Africa. Medical and Veterinary Entomology 8, 351–368.Google Scholar
RANDOLPH, S. E. ( 1994 b). Density-dependent acquired resistance to ticks in natural hosts, independent of concurrent infection with Babesia microti. Parasitology 108, 413–419.Google Scholar
RANDOLPH, S. E. ( 1995). Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Clethrionomys glareolus). Parasitology 110, 287–295.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 1997). Abiotic and biotic determinants of the seasonal dynamics of the tick Rhipicephalus appendiculatus in South Africa. Medical and Veterinary Entomology 11, 25–37.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 1998). Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitology Today 14, 186–192.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 2000). Ticks and tick-borne disease systems in space and from space. Advances in Parasitology 47, 217–243.CrossRefGoogle Scholar
RANDOLPH, S. E. ( 2001). The shifting landscape of tick-borne zoonoses: tick-borne encephalitis and Lyme borreliosis in Europe. Philosophical Transactions of the Royal Society, B 356, 1045–1056.CrossRefGoogle Scholar
RANDOLPH, S. E. & STEELE, G. M. ( 1985). An experimental evaluation of conventional control measures against the sheep tick Ixodes ricinus (L) (Acari: Ixodidae). II. The dynamics of the tick–host interaction. Bulletin of Entomological Research 75, 501–518.Google Scholar
RANDOLPH, S. E., GREEN, R. M., PEACEY, M. F. & ROGERS, D. J. ( 2000). Seasonal synchrony: the key to tick-borne encephalitis foci identified by satellite data. Parasitology 121, 15–23.CrossRefGoogle Scholar
RANDOLPH, S. E., GREEN, R. M., HOODLESS, A. N. & PEACEY, M. F. ( 2002). An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Internatioal Journal for Parasitology 32, 979–989.CrossRefGoogle Scholar
RANDOLPH, S. E., MIKLISOVÁ, D., LYSY, J., ROGERS, D. J. & LABUDA, M. ( 1999). Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177–186.CrossRefGoogle Scholar
RANDOLPH, S. E. & ROGERS, D. J. ( 1997). A generic population model for the African tick Rhipicephalus appendiculatus. Parasitology 115, 265–279.CrossRefGoogle Scholar
RANDOLPH, S. E. & STOREY, K. ( 1999). Impact of microclimate on immature tick-rodent interactions (Acari: Ixodidae): implications for parasite transmission. Journal of Medical Entomology 36, 741–748.CrossRefGoogle Scholar
RECHAV, Y. ( 1979). Migration and dispersal patterns of three African ticks (Acari: Ixodidae) under field conditions. Journal of Medical Entomology 16, 150–163.CrossRefGoogle Scholar
RECHAV, Y. ( 1981). Ecological factors affecting the seasonal activity of the brown ear tick Rhipicephalus appendiculatus. In Tick Biology and Control ( ed. Whitehead, G. B. & Gibson, J. D.), pp. 187–191. South Africa, Grahamstown University.
RECHAV, Y. ( 1982). Dynamics of tick populations (Acari: Ixodidae) in the Eastern Cape Province of South Africa. Journal of Medical Entomology 19, 679–700.CrossRefGoogle Scholar
RECHAV, Y. ( 1992). Naturally acquired resistance to ticks – a global view. Insect Science and its Application 13, 495–504.CrossRefGoogle Scholar
ROGERS, D. J. & RANDOLPH, S. E. ( 1993). Distribution of tsetse and ticks in Africa: past, present and future. Parasitology Today 9, 266–271.CrossRefGoogle Scholar
ROWSEWITT, C. N. ( 1986). Seasonal variation in activity rhythms of male voles: mediation by gonadal hormones. Physiology and Behaviour 37, 797–803.CrossRefGoogle Scholar
SHAW, D. J., GRENFELL, B. T. & DOBSON, A. P. ( 1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle Scholar
SHORT, N. J., FLOYD, R. B., NORVAL, R. A. I. & SUTHERST, R. W. ( 1989). Survival and behaviour of unfed stages of the ticks Rhipicephalus appendiculatus, Boophilus decoloratus and B. microplus under field conditions in Zimbabwe. Experimental and Applied Acarology 6, 215–236.Google Scholar
SHORT, N. J. & NORVAL, R. A. I. ( 1981). The seasonal activity of Rhipicephalus appendiculatus Neumann 1901 (Acarina: Ixodidae) in the high veld of Zimbabwe Rhodesia. Journal of Parasitology 67, 77–84.CrossRefGoogle Scholar
SONENSHINE, D. E. ( 1991). Biology of Ticks, vol. 1. Oxford, Oxford University Press.
SPIELMAN, A., WILSON, M. L., LEVINE, J. F. & PIESMAN, J. ( 1985). Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annual Review of Entomology 30, 439–460.CrossRefGoogle Scholar
STEELE, G. M. & RANDOLPH, S. E. ( 1985). An experimental evaluation of conventional control measures against the sheep tick Ixodes ricinus (L) (Acari: Ixodidae). I. A unimodal seasonal activity pattern. Bulletin of Entomological Research 75, 489–499.Google Scholar
STUBBS, M. ( 1977). Density dependence in the life-cycles of animals and its importance in K- and r-strategies. Journal of Animal Ecology 46, 677–688.CrossRefGoogle Scholar
SUTHERST, R. W., UTECH, K. B. W., KERR, J. D. & WHARTON, R. H. ( 1979). Density-dependent mortality of the tick Boophilus microplus, on cattle – further observations. Journal of Applied Ecology 16, 397–403.CrossRefGoogle Scholar
TALLEKLINT, L. & JAENSON, T. G. T. ( 1994). Transmission of Borrelia burgdorferi s.l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden. Journal of Medical Entomology 31, 880–886.Google Scholar
TALLEKLINT, L. & JAENSON, T. G. T. ( 1996). Relationship between Ixodes ricinus density and prevalence of infection with Borrelia-like spirochetes and density of infected ticks. Journal of Medical Entomology 33, 805–811.CrossRefGoogle Scholar
TALLEKLINT-EISEN, L. & LANE, R. S. ( 2000). Efficiency of drag sampling for estimating population sizes of Ixodes pacificus (Acari: Ixodidae) nymphs in leaf litter. Journal of Medical Entomology 37, 484–487.CrossRefGoogle Scholar
TATCHELL, R. J. & EASTON, E. ( 1986). Tick (Acari: Ixodidae) ecological studies in Tanzania. Bulletin of Entomological Research 76, 229–246.CrossRefGoogle Scholar
USPENSKY, I. ( 1995). Physiological age of Ixodid ticks: aspects of its determination and application. Journal of Medical Entomology 32, 751–764.CrossRefGoogle Scholar
UTECH, K. B. W., SEIFERT, G. W. & WHARTON, R. H. ( 1978). Breeding Australian Illawara shorthorn cattle for resistance to Boophilus microplus. I. Factors affecting resistance. Australian Journal of Agricultural Research 29, 411–422.CrossRefGoogle Scholar
VAN ES, R. P., HILLERTON, J. E. & GETTINBY, G. ( 1998). Lipid consumption in Ixodes ricinus (Acari: Ixodidae): temperature and potential longevity. Bulletin of Entomological Research 88, 567–573.CrossRefGoogle Scholar
VANDYK, J. K., BARTHOLOMEW, D. M., ROWLEY, W. A. & PLATT, K. B. ( 1996). Survival of Ixodes scapularis (Acari: Ixodidae) exposed to cold. Journal of Medical Entomology 33, 6–10.CrossRefGoogle Scholar
VARLEY, G. C., GRADWELL, G. R. & HASSELL, M. P. ( 1973). Insect Population Ecology: An Analytical Approach. Oxford, Blackwell Scientific Publications.
WALKER, A. R. ( 2001). Age structure of a population of Ixodes ricinus (Acari: Ixodidae) in relation to its seasonal questing. Bulletin of Entomological Research 91, 69–78.Google Scholar
WALKER, A. R., FLETCHER, J. D. & TODD, L. ( 1990). Resistance between stages of the tick Rhipicephalus appendiculatus (Acari: Ixodidae). Journal of Medical Entomology 27, 955–961.CrossRefGoogle Scholar
WILSON, M. L., ADLER, G. H. & SPEILMAN, A. ( 1985). Correlation between abundance of deer and that of the deer tick, Ixodes dammini (Acari: Ixodidae). Annals of the Entomological Society of America 78, 172–176.CrossRefGoogle Scholar
WOOLHOUSE, M. E. J., DYE, C., ETARD, J. F., SMITH, T., CHARLWOOD, J. D., GARNETT, G. P., HAGAN, P., HII, J. L. K., NDHLOVU, P. D., QUINNELL, R. J., WATTS, C. H., CHANDIWANA, S. K. & ANDERSON, R. M. ( 1997). Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338–342.CrossRefGoogle Scholar
WOOLHOUSE, M. E. J., ETARD, J.-F., DIETZ, K., NDHLOVU, P. D. & CHANDIWANA, S. K. ( 1998). Heterogeneities in schistosome transmission dynamics and control. Parasitology 117, 475–482.CrossRefGoogle Scholar
ZABICKA, J. ( 1994). [The tick-borne encephalitis in Poland.] (In Polish.) Przegl Epidemiology 48, 197–203.Google Scholar
ZEMAN, P. & JANUSKA, J. ( 1999). Epizootiologic background of dissimilar distribution of human cases of Lyme borreliosis and tick-borne encephalitis in a joint endenic area. Comparative Immunology, Microbiology and Infectious Diseases 22, 247–260.CrossRefGoogle Scholar