Hostname: page-component-89b8bd64d-5bvrz Total loading time: 0 Render date: 2026-05-12T12:56:34.199Z Has data issue: false hasContentIssue false
  • English
  • Français

Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics

Published online by Cambridge University Press:  13 November 2006

S. TELFER ,
M. BEGON ,
M. BENNETT ,
K. J. BOWN ,
S. BURTHE ,
X. LAMBIN ,
G. TELFORD  and
R. BIRTLES
S. TELFER
Affiliation:
School of Biological Sciences, University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
M. BEGON
Affiliation:
School of Biological Sciences, University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK
M. BENNETT
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
K. J. BOWN
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
S. BURTHE
Affiliation:
School of Biological Sciences, University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK
X. LAMBIN
Affiliation:
School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
G. TELFORD
Affiliation:
School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
R. BIRTLES
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Many zoonotic disease agents are transmitted between hosts by arthropod vectors, including fleas, but few empirical studies of host-vector-microparasite dynamics have investigated the relative importance of hosts and vectors. This study investigates the dynamics of 4 closely related Bartonella species and their flea vectors in cyclic populations of field voles (Microtus agrestis) over 3 years. The probability of flea infestation was positively related to field vole density 12 months previously in autumn, but negatively related to more recent host densities, suggesting a dilution effect. The 4 Bartonella species exhibited contrasting dynamics. Only B. grahamii, showed a distinct seasonal pattern. Infection probability increased with field vole density for B. doshiae, B. taylorii and BGA (a previously unidentified species) and with density of coexisting wood mice for B. doshiae and B. grahamii. However, only the infection probability of BGA in spring was related to flea prevalence. B. doshiae and BGA were most common in older animals, but the other 2 were most common in non-reproductive hosts. Generally, host density rather than vector abundance appears most important for the dynamics of flea-transmitted Bartonella spp., possibly reflecting the importance of flea exchange between hosts. However, even closely related species showed quite different dynamics, emphasising that other factors such as population age structure can impact on zoonotic risk.

Keywords

host-parasite dynamicspathogendensity dependenceflea-bornewildlife disease

Information

Type
Research Article
Information
Parasitology , Volume 134 , Issue 3 , March 2007 , pp. 413 - 425
Copyright
© 2006 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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Albright, J. W. and Albright, J. F. ( 1991). Rodent trypanosomes – their conflict with the immune-system of the host. Parasitology Today 7, 137–140.CrossRefGoogle Scholar
Anderson, B. E. and Neuman, M. A. ( 1997). Bartonella spp. as emerging human pathogens. Clinical Microbiology Review 10, 203–219.Google Scholar
Begon, M. ( 2007). Effects of host diversity on disease dynamics. In Ecology of Infectious Diseases: Effects of Ecosystems on Disease and of Disease on Ecosystems (ed. Ostfeld, R. S., Keesing, F. and Eviner, V.). Princeton University Press. (in the Press).
Begon, M., Bennett, M., Bowers, R. G., French, N. P., Hazel, S. M. and Turner, J. ( 2002). A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiology and Infection 129, 147–153.CrossRefGoogle Scholar
Birtles, R. J., Hazel, S. M., Bennett, M., Bown, K., Raoult, D. and Begon, M. ( 2001). Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiology and Infection 126, 323–329.CrossRefGoogle Scholar
Bown, K. J., Bennett, M. and Begon, M. ( 2004). Flea-borne Bartonella grahamii and Bartonella taylorii in bank voles. Emerging Infectious Disease 10, 684–687.CrossRefGoogle Scholar
Breitschwerdt, E. B. and Kordick, D. L. ( 2000). Bartonella infection in animals: Carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clinical Microbiology Review 13, 428–438.CrossRefGoogle Scholar
Burnham, K. P. and Anderson, D. R. ( 1998). Model Selection and Inference: A Practical Information-theoretic Approach. Springer, New York.CrossRef
Chang, C. C., Chomel, B. B., Kasten, R. W., Romano, V. and Tietze, N. ( 2001). Molecular evidence of Bartonella spp. in questing adult Ixodes pacificus ticks in California. Journal of Clinical Microbiology 39, 1221–1226.Google Scholar
Chomel, B. B., Kasten, R. W., Sykes, J. E., Boulouis, H. J. and Breitschwerdt, E. B. ( 2003). Clinical impact of persistent Bartonella bacteremia in humans and animals. Annals of the New York Academy of Science 990, 267–278.CrossRefGoogle Scholar
Cleaveland, S., Laurenson, M. K. and Taylor, L. H. ( 2001). Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society of London, B 356, 991–999.CrossRefGoogle Scholar
Dye, C. and Williams, B. G. ( 1995). Nonlinearities in the dynamics of indirectly transmitted infections (or, does having a vector make a difference?). In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 260–279. Cambridge University Press, Cambridge.CrossRef
Hawlena, H., Abramsky, Z. and Krasnov, B. R. ( 2005). Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146, 200–208.CrossRefGoogle Scholar
Hudson, P. and Dobson, A. ( 1995). Macroparasites: observed patterns. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 114–176. Cambridge University Press, Cambridge.CrossRef
Hudson, P. J., Norman, R., Laurenson, M. K., Newborn, D., Gaunt, M., Jones, L., Reid, H., Gould, E., Bowers, R. and Dobson, A. ( 1995). Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations. Parasitology 111, S49–S58.CrossRefGoogle Scholar
Kosoy, M., Mandel, E., Green, D., Marston, E. and Childs, J. ( 2004 a). Prospective studies of Bartonella of rodents. Part I. Demographic and temporal patterns in population dynamics. Vector-Borne Zoonotic Diseases 4, 285–295.Google Scholar
Kosoy, M., Mandel, E., Green, D., Marston, E., Jones, D. and Childs, J. ( 2004 b). Prospective studies of Bartonella of rodents. Part II. Diverse infections in a single rodent community. Vector-Borne Zoonotic Diseases 4, 296–305.Google Scholar
Kosoy, M. Y., Regnery, R. L., Kosaya, O. I., Jones, D., Marston, E. and Childs, J. ( 1998). Isolation of Bartonella spp. from embryos and neonates of naturally infected rodents. Journal of Wildlife Diseases 34, 305–309.Google Scholar
Kosoy, M. Y., Regnery, R. L., Tzianabos, T., Marston, E. L., Jones, D. C., Green, D., Maupin, G. O., Olson, J. G. and Childs, J. E. ( 1997). Distribution, diversity, and host specificity of Bartonella in rodents from the southeastern United States. Americal Journal of Tropical Medicine and Hygiene 57, 578–588.CrossRefGoogle Scholar
Kosoy, M. Y., Saito, E. K., Green, D., Marston, E., Jones, D. and Childs, J. ( 2000). Experimental evidence of host specificity of Bartonella infection in rodents. Comparative Immunology, Microbiology and Infectious Diseases 23, 221–238.CrossRefGoogle Scholar
Krampitz, H. E. ( 1962). Weitere Untersuchungen an Grahamella Brumpt 1911. Zeitschrift für Tropenmedizin und Parasitologie 13, 34–53.Google Scholar
Krasnov, B. R., Burdelova, N. V., Shenbrot, G. I. and Khokhlova, I. S. ( 2002 a). Annual cycles of four flea species in the central Negev desert. Medical Veterinary Entomology 16, 266–276.Google Scholar
Krasnov, B. R., Khokhlova, I. S., Burdelova, N. V., Mirzoyan, N. S. and Degen, A. A. ( 2004). Fitness consequences of host selection in ectoparasites: testing reproductive patterns predicted by isodar theory in fleas parasitizing rodents. Journal of Animal Ecology 73, 815–820.CrossRefGoogle Scholar
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. ( 2002 b). Time of survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. Journal of Vector Ecology 27, 70–81.Google Scholar
Krasnov, B. R., Khokhlova, I. S. and Shenbrot, G. I. ( 2002 c). The effect of host density on ectoparasite distribution: an example of a rodent parasitized by fleas. Ecology 83, 164–175.Google Scholar
Krasnov, B. R., Khokhlova, I. S. and Shenbrot, G. I. ( 2003). Density-dependent host selection in ectoparasites: an application of isodar theory to fleas parasitizing rodents. Oecologia 134, 365–372.CrossRefGoogle Scholar
Lambin, X., Petty, S. J. and Mackinnon, J. L. ( 2000). Cyclic dynamics in field vole populations and generalist predation. Journal of Animal Ecology 69, 106–118.CrossRefGoogle Scholar
Laurenson, M. K., Norman, R. A., Gilbert, L., Reid, H. W. and Hudson, P. J. ( 2003). Identifying disease reservoirs in complex systems: mountain hares as reservoirs of ticks and louping-ill virus, pathogens of red grouse. Journal of Animal Ecology 72, 177–185.CrossRefGoogle Scholar
Lindsay, L. R. and Galloway, T. D. ( 1997). Seasonal activity and temporal separation of four species of fleas (Insecta: Siphonaptera) infesting Richardson's ground squirrels, Spermophilus richardsonii (Rodentia: Sciuridae), in Manitoba, Canada. Canadian Journal of Zoology 75, 1310–1322.CrossRefGoogle Scholar
Littell, R. C., Milliken, G. A., Stroup, W. W. and Wolfinger, R. D. ( 1996). SAS System for Mixed Models. SAS Institute Inc., Cary, NC.
Mackinnon, J. L., Petty, S. J., Elston, D. A., Thomas, C. J., Sherratt, T. N. and Lambin, X. ( 2001). Scale invariant spatio-temporal patterns of field vole density. Journal of Animal Ecology 70, 101–111.CrossRefGoogle Scholar
Maggi, R. G., Duncan, A. W. and Breitschwerdt, E. B. ( 2005). Novel chemically modified liquid medium that will support the growth of seven Bartonella species. Journal of Clinical Microbiology 43, 2651–2655.CrossRefGoogle Scholar
Marshall, A. G. ( 1981). The Ecology of Ectoparasitic Insects. Academic Press, London.
Myllymaki, A., Paasikallio, A., Pankakoski, E. and Kanervo, V. ( 1971). Removal experiments on small quadrats as a means of rapid assessment of the abundance of small mammals. Annales Zoologici Fennici 8, 177–185.Google Scholar
Pappalardo, B. L., Correa, M. T., York, C. C., Peat, C. Y. and Breitschwerdt, E. B. ( 1997). Epidemiologic evaluation of the risk factors associated with exposure and seroreactivity to Bartonella vinsonii in dogs. American Journal of Veterinary Research 58, 467–471.Google 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., Chemini, C., Furlanello, C., Genchi, C., Hails, R., Hudson, P., Jones, L., Medley, G., Norman, R., Rizzoli, A., Smith, G. and Woolhouse, M. ( 2002). The ecology of tick-borne infections in wildlife reservoirs. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 119–138. Oxford University Press, Oxford.
Ribeiro P. J. Jr and Diggle, P. J. ( 2001). geoR: a package for geostatistical analysis. R-NEWS 1, 15–18.Google Scholar
Rust, M. K. and Dryden, M. W. ( 1997). The biology, ecology, and management of the cat flea. Annual Review of Entomology 42, 451–473.CrossRefGoogle Scholar
Sato, H., Ishita, K., Osanai, A., Yagisawa, M., Kamiya, H. and Ito, M. ( 2004). T cell dependent elimination of dividing Trypanosoma grosi from the bloodstream Mongolian jirds. Parasitology 128, 295–304.CrossRefGoogle Scholar
Smith, A., Telfer, S., Burthe, S., Bennett, M. and Begon, M. ( 2005). Trypanosomes, fleas and field voles: ecological dynamics of a host-vector-parasite interaction. Parasitology 131, 355–365.CrossRefGoogle Scholar
Telfer, S., Bown, K. J., Sekules, R., Begon, M., Hayden, T. and Birtles, R. ( 2005). Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130, 661–668.CrossRefGoogle Scholar
Venables, W. N. and Ripley, B. D. ( 2002). Modern Applied Statistics with S. Springer, New York.CrossRef