Hostname: page-component-7dd5485656-j7khd Total loading time: 0 Render date: 2025-10-28T09:43:23.066Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of spatial heterogenity on the aggregation of ticks on white-footed mice

Published online by Cambridge University Press:  12 March 2012

G. DEVEVEY  and
D. BRISSON
G. DEVEVEY*
Affiliation:
Department of Biology, 415 S. University Avenue, Philadelphia, PA 19104, USA
D. BRISSON*
Affiliation:
Department of Biology, 415 S. University Avenue, Philadelphia, PA 19104, USA
*
*Corresponding author: Tel: +1 215 746 1732. Fax: +1 215 573 9454. E-mail: dbrisson@sas.upenn.edu
Get access Rights & Permissions [Opens in a new window]

Summary

Parasites are often aggregated on a minority of the individuals in their host populations. Although host characteristics are commonly presumed to explain parasite aggregation on hosts, spatio-temporal aggregation of parasites during their host-seeking stages may have a dominant effect on the aggregation on hosts. We aimed to quantify, using mixed models, repeatability and autocorrelation analyses, the degree to which the aggregation of blacklegged ticks (Ixodes scapularis) on white-footed mice (Peromyscus leucopus) is influenced by spatio-temporal distributions of the host-seeking ticks and by heterogeneity among mice. Host-seeking ticks were spatially aggregated at both the larval and nymphal life-stages. However, this spatial aggregation accounted for little of the variation in larval and nymphal burdens observed on mice (3% and 0%, respectively). Conversely, mouse identity accounted for a substantial proportion of the variance in tick burdens. Mouse identity was a significant explanatory factor as the majority of ticks parasitized a consistent set of mice throughout the activity seasons. Of the characteristics associated with mouse identity investigated, only gender affected larval burdens, and body mass and home range sizes in males were correlated with nymphal burdens. These analyses suggest that aggregation of ticks on a minority of mice does not result from the distribution of host-seeking ticks but from characteristics of the hosts.

Keywords

burdenhost-seeking ticksindex of dispersionIxodes scapularisPennsylvaniaPeromyscus leucopusrepeatability

Information

Type
Research Article
Information
Parasitology , Volume 139 , Issue 7 , June 2012 , pp. 915 - 925
Copyright
Copyright © Cambridge University Press 2012

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

Behnke, J. M. and Wakelin, D. (1973). Survival of Trichuris muris in wild populations of its natural hosts. Parasitology 67, 157–164.CrossRefGoogle ScholarPubMed
Bize, P. and Roulin, A. (2009). Effects of common origin and common rearing environment on variance in ectoparasite load and phenotype of nestling Alpine Swifts. Evolutionary Biology 36, 301–310. doi: 10.1007/s11692-009-9063-x.CrossRefGoogle Scholar
Bohan, D. A. (2000). Spatial structuring and frequency distribution of the nematode Steinernema feltiae Filipjev. Parasitology 121, 417–425. doi: 10.1017/s0031182099006551.CrossRefGoogle ScholarPubMed
Bown, K. J., Lambin, X., Telford, G. R., Ogden, N. H., Telfer, S., Woldehiwet, Z. and Birtles, R. J. (2008). Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors for Anaplasma phagocytophilum and Babesia microti in Field Vole (Microtus agrestis) Populations. Applied and Environmental Microbiology 74, 7118–7125. doi: 10.1128/aem.00625-08.CrossRefGoogle ScholarPubMed
Boyer, N., Reale, D., Marmet, J., Pisanu, B. and Chapuis, J.-L. (2010). Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. Journal of Animal Ecology 79, 538–547. doi: 10.1111/j.1365-2656.2010.01659.x.CrossRefGoogle Scholar
Brown, E. D., Macdonald, D. W., Tew, T. E. and Todd, I. A. (1994). Apodemus sylvaticus infected with Heligmosomoides polygyrus (Nematoda) in an arable ecosystem – Epidemiology and effects of infection on the movements of male mice. Journal of Zoology 234, 623–640.CrossRefGoogle Scholar
Brunner, J. L., Cheney, L., Keesing, F., Killilea, M., Logiudice, K., Previtali, A. and Ostfeld, R. S. (2011). Molting success of Ixodes scapularis varies among individual blood meal hosts and species. Journal of Medical Entomology 48, 860–866. doi: 10.1603/me10256.CrossRefGoogle ScholarPubMed
Brunner, J. L. and Ostfeld, R. S. (2008). Multiple causes of variable tick burdens on small-mammal hosts. Ecology 89, 2259–2272. doi: 10.1890/07-0665.1.CrossRefGoogle ScholarPubMed
Clayton, D. H. and Moore, J. (1997). Host-Parasite Evolution: General Principles and Avian Models, Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Cotton, M. J. and Watts, C. H. S. (1967). Ecology of tick Ixodes trianguliceps Birula (Arachnida Acarina Ixodoidea). Parasitology 57, 525–531.CrossRefGoogle Scholar
Clutton-Brock, T. H. (1990). Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems, University of Chicago Press, Chicago, USA.Google Scholar
Daniels, T. J. and Fish, D. (1990). Spatial-distribution and dispersal of unfed larval Ixodes dammini (ACARI, Ixodidae) in Southern New-York. Environmental Entomology 19, 1029–1033.Google Scholar
Davidar, P., Wilson, M. and Ribeiro, J. M. C. (1989). Differential distribution of immature Ixodes dammini (ACARI, Ixodidae) on rodent hosts. Journal of Parasitology 75, 898–904. doi: 10.2307/3282868.CrossRefGoogle ScholarPubMed
Davies, J. B., Sandstroem, S., Shorrocks, A. and Wolff, E. N. (2007). Estimating the level and distribution of global household wealth. UNU-WIDER, 2007/77. doi: ISBN 978-92-9230-030-2.Google Scholar
Dingemanse, N. J., Both, C., Drent, P. J., Van Oers, K. and Van Noordwijk, A. J. (2002). Repeatability and heritability of exploratory behaviour in great tits from the wild. Animal Behaviour 64, 929–938. doi: 10.1006/anbe.2002.2006.Google Scholar
Dobson, A. D. M., Taylor, J. L. and Randolph, S. E. (2011). Tick (Ixodes ricinus) abundance and seasonality at recreational sites in the UK: Hazards in relation to fine-scale habitat types revealed by complementary sampling methods. Ticks and Tick-Borne Diseases 2, 67–74. doi: 10.1016/j.ttbdis.2011.03.002.CrossRefGoogle ScholarPubMed
Dubey, J. P., Bhatia, C. R., Lappin, M. R., Ferreira, L. R., Thorn, A. and Kwok, O. C. H. (2009). Seroprevalence of Toxoplasma gondii and Bartonella spp. antibodies in cats from Pennsylvania. Journal of Parasitology 95, 578–580. doi: 10.1645/ge-1933.1.CrossRefGoogle ScholarPubMed
Dzieweczynski, T. L. and Crovo, J. A. (2011). Shyness and boldness differences across contexts in juvenile three-spined stickleback Gasterosteus aculeatus from an anadromous population. Journal of Fish Biology 79, 776–788. doi: 10.1111/j.1095-8649.2011.03064.x.CrossRefGoogle ScholarPubMed
Ellis, G. B. and Turek, F. W. (1983). Testosterone and photoperio interact to regulate locomotor activity in male hamsters. Hormones and Behavior 17, 66–75. doi: 10.1016/0018-506x(83)90016-8.CrossRefGoogle ScholarPubMed
Ezenwa, V. O., Price, S. A., Altizer, S., Vitone, N. D. and Cook, K. C. (2006). Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla. Oikos 115, 526–536. doi: 10.1111/j.2006.0030-1299.15186.x.CrossRefGoogle Scholar
Falconer, D. S. and Mackay, T. F. C. (1996). Introduction to Quantitative Genetics, Longman, New-York, USA.Google Scholar
Fish, D. (1993). Population ecology of Ixodes dammini. In Ecology and Environmental Management of Lyme Disease (ed. Ginsberg, H. S.), pp. 25–42. Rutgers University Press, New Brunswick, NJ, USA.CrossRefGoogle Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622. doi: 10.1086/285346.Google Scholar
Gern, L., Cadenas, F. M. and Burri, C. (2008). Influence of some climatic factors on Ixodes ricinus ticks studied along altitudinal gradients in two geographic regions in Switzerland. International Journal of Medical Microbiology 298, 55–59. doi: 10.1016/j.ijmm.2008.01.005.CrossRefGoogle Scholar
Goodwin, B. J., Ostfeld, R. S. and Schauber, E. M. (2001). Spatiotemporal variation in a Lyme Disease host and vector: black-legged ticks on white-footed mice. Vector borne and Zoonotic Diseases 1, 129–138.Google Scholar
Grear, D. A., Perkins, S. E. and Hudson, P. J. (2009). Does elevated testosterone result in increased exposure and transmission of parasites? Ecology Letters 12, 528–537. doi: 10.1111/j.1461-0248.2009.01306.x.CrossRefGoogle ScholarPubMed
Hansen, F., Jeltsch, F., Tackmann, K., Staubach, C. and Thulke, H. H. (2004). Processes leading to a spatial aggregation of Echinococcus multilocularis in its natural intermediate host Microtus arvalis. International Journal for Parasitology 34, 37–44. doi: 10.1016/j.ipara.2003.10.003.Google ScholarPubMed
Harrison, A., Scantlebury, M. and Montgomery, W. I. (2010). Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119, 1099–1104. doi: 10.1111/j.1600-0706.2009.18072.x.CrossRefGoogle Scholar
Hillegass, M. A., Waterman, J. M. and Roth, J. D. (2008). The influence of sex and sociality on parasite loads in an African ground squirrel. Behavioral Ecology 19, 1006–1011. doi: 10.1093/beheco/arn070.CrossRefGoogle Scholar
Hughes, V. L. and Randolph, S. E. (2001). 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.CrossRefGoogle ScholarPubMed
Jones, C. G., Ostfeld, R. S., Richard, M. P., Schauber, E. M. and Wolff, J. O. (1998). Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279, 1023–1026. doi: 10.1126/science.279.5353.1023.CrossRefGoogle ScholarPubMed
Juran, J. M., Seder, L. A. and Gryna, F. M. (1962). The Quality Control Handbook, New-York, McGraw-Hill, New-York, USA.Google Scholar
Kiffner, C., Loedige, C., Alings, M., Vor, T. and Ruehe, F. (2011 a). Body-mass or sex-biased tick parasitism in roe deer (Capreolus capreolus)? A GAMLSS approach. Medical and Veterinary Entomology 25, 39–45. doi: 10.1111/j.1365-2915.2010.00929.x.CrossRefGoogle ScholarPubMed
Kiffner, C., Vor, T., Hagedorn, P., Niedrig, M. and Ruehe, F. (2011 b). Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany. Parasitology Research 108, 323–335. doi: 10.1007/s00436-010-2065-x.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Morand, S., Hawlena, H., Khokhlova, I. S. and Shenbrot, G. I. (2005). Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209–217. doi: 10.1007/s00442-005-0189-y.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Stanko, M. and Morand, S. (2007). Host community structure and infestation by ixodid ticks: repeatability, dilution effect and ecological specialization. Oecologia 154, 185–194. doi: 10.1007/s00442-007-0824-x.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Stanko, M. and Morand, S. (2010). Competition, facilitation or mediation via host? Patterns of infestation of small European mammals by two taxa of haematophagous arthropods. Ecological Entomology 35, 37–44. doi: 10.1111/j.1365-2311.2009.01153.x.Google Scholar
Lessells, C. M. and Boag, P. T. (1987). Unrepeatable repeatabilities – a common mistake. Auk 104, 116–121.CrossRefGoogle Scholar
Leung, B. (1998). Aggregated parasite distributions on hosts in a homogeneous environment: examining the Poisson null model. International Journal for Parasitology 28, 1709–1712. doi: 10.1016/s0020-7519(98)00128-3.CrossRefGoogle Scholar
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. and Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature, London 438, 355–359. doi: 10.1038/nature04153.CrossRefGoogle ScholarPubMed
Lynn, S. E., Houtman, A. M., Weathers, W. W., Ketterson, E. D. and Nolan, V. (2000). Testosterone increases activity but not daily energy expenditure in captive male dark-eyed juncos, Junco hyemalis. Animal Behaviour 60, 581–587. doi: 10.1006/anbe.2000.1510.CrossRefGoogle Scholar
Minerly, A. E., Russo, S. J., Kemen, L. M., Nazarian, A., Wu, H. B. K., Weierstall, K. M., Akhavan, A., Jenab, S. and Quinones-Jenab, V. (2008). Testosterone plays a limited role in cocaine-induced conditioned place preference and locomotor activity in male rats. Ethnicity & Disease 18, S2.Google Scholar
Morand, S., Krasnov, B. R. and Poulin, R. (2006). Micromammals and macroparasites, Springer-Verlag, Tokyo.CrossRefGoogle Scholar
Ostfeld, R. S., Canham, C. D., Oggenfuss, K., Winchcombe, R. J. and Keesing, F. (2006). Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. Plos Biology 4, 1058–1068. doi: E14510.1371/journal.pbio.0040145.CrossRefGoogle ScholarPubMed
Ostfeld, R. S., Miller, M. C. and Schnurr, J. (1993). Ear tagging increases tick (Ixodes dammini) infestation rates of white-footed mice (Peromyscus leucopus). Journal of Mammalogy 74, 651–655. doi: 10.2307/1382286.CrossRefGoogle Scholar
Ostfeld, R. S., Hazler, K. R. and Cepeda, O. M. (1996 a). Temporal and spatial dynamics of Ixodes scapularis (Acari: Ixodidae) in a rural landscape. Journal of Medical Entomology 33, 90–95.CrossRefGoogle Scholar
Ostfeld, R. S., Miller, M. C. and Hazler, K. R. (1996 b). Causes and consequences of tick (Ixodes scapularis) burdens on white-footed mice (Peromyscus leucopus). Journal of Mammalogy 77, 266–273. doi: 10.2307/1382727.CrossRefGoogle Scholar
Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. and Hudson, P. J. (2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology 33, 909–917. doi: 10.1016/s0020-7519(03)00128-0.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, Princeton University Press, Princeton, NJ, USA.Google Scholar
R Development Core Team (2010). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org,ISBN3-900051-07-0.Google Scholar
Randolph, S. E. (1975). Patterns of distribution of tick Ixodes trianguliceps Birula on its hosts. Journal of Animal Ecology 44, 451–474. doi: 10.2307/3606.CrossRefGoogle Scholar
Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, S37–S65. doi: 10.1017/s0031182004004925.CrossRefGoogle ScholarPubMed
Randolph, S. E., Miklisova, D., Lysy, J., Rogers, D. J. and Labuda, M. (1999). Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177–186. doi: 10.1017/s0031182098003643.CrossRefGoogle ScholarPubMed
Randolph, S. E. and Steele, G. M. (1985). An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L)(Acari, Ixodidae). 2. The dynamics of the tick-host interaction. Bulletin of Entomological Research 75, 501–518.CrossRefGoogle Scholar
Raty, M. and Kangas, A. (2007). Localizing general models based on local indices of spatial association. European Journal of Forest Research 126, 279–289. doi: 10.1007/s10342-006-0147-1.CrossRefGoogle Scholar
Robinson, S. A., Forbes, M. R. and Hebert, C. E. (2009). Parasitism, mercury contamination, and stable isotopes in fish-eating double-crested cormorants: no support for the co-ingestion hypothesis. Canadian Journal of Zoology-Revue Canadienne de Zoologie 87, 740–747. doi: 10.1139/z09-062.CrossRefGoogle Scholar
Rosenberg, M. S. and Anderson, C. D. (2011). PASSaGE: Pattern Analysis, Spatial Statistics and Geographic Exegesis. Version 2. Methods in Ecology and Evolution 2, 229–232.CrossRefGoogle Scholar
Rowsemitt, C. N. (1989). Activity of castrated male voles- Rhytms of responses to testosterone replacement. Physiology & Behavior 45, 7–13. doi: 10.1016/0031-9384(89)90159-5.CrossRefGoogle Scholar
Sanchez, A., Devevey, G. and Bize, P. (2011). Female-biased infection and transmission of the gastrointestinal nematode Trichuris arvicolae infecting the common vole. International Journal for Parasitology 41, 1397–1402.CrossRefGoogle ScholarPubMed
Schmidt, K. A. and Ostfeld, R. S. (2001). Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619. doi: 10.2307/2680183.Google Scholar
Schmidt, K. A., Ostfeld, R. S. and Schauber, E. M. (1999). Infestation of Peromyscus leucopus and Tamias striatus by Ixodes scapularis (Acari: Ixodidae) in relation to the abundance of hosts and parasites. Journal of Medical Entomology 36, 749–757.CrossRefGoogle Scholar
Seivwright, L. J., Redpath, S. M., Mougeot, F., Leckie, F. and Hudson, P. J. (2005). Interactions between intrinsic and extrinsic mechanisms in a cyclic species: testosterone increases parasite infection in red grouse. Proceedings of the Royal Society of London, B 272, 2299–2304. doi: 10.1098/rspb.2005.3233.Google Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610. doi: 10.1017/s0031182098003448.CrossRefGoogle ScholarPubMed
Shaw, M. T., Keesing, F., McGrail, R. and Ostfeld, R. S. (2003). Factors influencing the distribution of larval blacklegged ticks on rodent hosts. American Journal of Tropical Medicine and Hygiene 68, 447–452.CrossRefGoogle ScholarPubMed
Siegel, J. P., Kitron, U. and Bouseman, J. K. (1991). Spatial and temporal distribution of Ixodes dammini (Acari, Ixodidae) in a northwestern Illinois state park. Journal of Medical Entomology 28, 101–104.CrossRefGoogle Scholar
Sokal, R. R. and Rohlf, F. J. (1995). Biometry. W. H. Freeman and company, New York, USA.Google Scholar
Steiner, F. E., Pinger, R. R., Vann, C. N., Grindle, N., Civitello, D., Clay, K. and Fuqua, C. (2008). Infection and co-infection rates of Anaplasma phagocytophilum variants, Babesia spp., Borrelia burgdorferi, and the rickettsial endosymbiont in Ixodes scapularis (Acari : Ixodidae) from sites in Indiana, Maine, Pennsylvania, and Wisconsin. Journal of Medical Entomology 45, 289–297. doi: 10.1603/0022-2585(2008)45[289:iacroa]2.0.co;2.CrossRefGoogle ScholarPubMed
Stafford, K. C. (1992). Oviposition and larval dispersal of Ixodes dammini (ACARI, Ixodidae). Journal of Medical Entomology 29,129–132.CrossRefGoogle ScholarPubMed
Wilson, K., Grenfell, B. T. and Shaw, D. J. (1996). Analysis of aggregated parasite distributions: A comparison of methods. Functional Ecology 10, 592–601. doi: 10.2307/2390169.CrossRefGoogle Scholar
Wilson, M. L. and Spielman, A. (1985). Seasonal activity of immature Ixodes dammini (ACARI, Ixodidae). Journal of Medical Entomology 22, 408–414.CrossRefGoogle ScholarPubMed
Wilson, M. L. (1998). Distribution and abundance of Ixodes scapularis (Acari : Ixodidae) in North America: Ecological processes and spatial analysis. Journal of Medical Entomology 35, 446–457.CrossRefGoogle ScholarPubMed
Wolff, J. O. (1985). The effect of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Canadian Journal of Zoology-Revue Canadienne de Zoologie 63, 2657–2662.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. and 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. doi: 10.1073/pnas.94.1.338.CrossRefGoogle ScholarPubMed
Yeagley, T. J., Reichard, M. V., Hempstead, J. E., Allen, K. E., Parsons, L. M., White, M. A., Little, S. E. and Meinkoth, J. H. (2009). Detection of Babesia gibsoni and the canine small Babesia ‘Spanish isolate’ in blood samples obtained from dogs confiscated from dogfighting operations. Javma-Journal of the American Veterinary Medical Association 235, 535–539.CrossRefGoogle ScholarPubMed
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: Patterns and processes. International Journal for Parasitology 26, 1009–1023. doi: 10.1016/s0020-7519(96)00086-0.CrossRefGoogle ScholarPubMed