Parasitism among individuals in a population often varies more than expected by chance only, leading to parasite aggregation, which is a parameter of paramount importance in parasite population dynamics and particularly in vector-borne epidemiology. However, the origin of this phenomenon is yet not fully elucidated. An increasing body of literature has demonstrated that individuals vary consistently in their behaviour, which is referred to as animal personality. Such behavioural variation could potentially lead to different encounter rates with parasites. To test this hypothesis, the relationship between personality and burden with ticks (Ixodes spp.) in the bank vole, Myodes glareolus (Schreber), was assessed. Wild rodents (eight females and 18 males) were live-trapped, identified, sexed, weighted, and inspected for ticks. Behavioural profiling was then performed using standardised tests measuring activity/exploration and boldness with a combination of automatically and manually recorded behavioural variables summarised using multivariate analyses. The resulting personality descriptors and questing tick variables were used as explanatory variables in negative binomial generalised linear models of tick burden and Bayesian simulations were performed to better estimate coefficients. Tick burden was associated to body mass and sex, but not to personality descriptors, which was mainly associated to activity/exploration. These results are discussed regarding the complex relationships among individual personality, physiological status, space use and health status.

Current affiliation Laboratoire de Biometrie et Biologie Evolutive Universite Claude Bernard Lyon 1 VetAgro Sup France

Laboratoire Chrono Environnement UMR 6249 CNRS Universite de Franche Comte France

Laboratoire Cogitamus France

Zobrazit více v PubMed

Arriero E., Wanelik K.M., Birtles R.J., Bradley J.E., Jackson A., Paterson S., Begon M. 2017: From the animal house to the field: are there consistent individual differences in immunological profile in wild populations of field voles (Microtus agrestis)? PLoS ONE 12: 1-10. PubMed DOI

Aubry J. 1950: [Deux pièges pour la capture de petits rongeurs vivants]. Mammalia 14: 174-177. (In French.) DOI

Barton K. 2020: MuMIn: Multi-Model Inference, https://cran.r-project.org/web/packages/MuMIn/index.html.

Beldomenico P.M., Telfer S., Gebert S., Lukomski L., Bennett M., Begon M. 2008: The dynamics of health in wild field vole populations: a haematological perspective. J. Anim. Ecol. 77: 984-997. PubMed DOI

Beldomenico P.M., Telfer S., Gebert S., Lukomski L., Bennett M., Begon M. 2009: The vicious circle and infection intensity: the case of Trypanosoma microti in field vole populations. Epidemics 1: 162-167. PubMed DOI

Bello-Arroyo E., Roque H., Marcos A., Orihuel J., Higuera-Matas A., Desco M., Caiolfa V.R., Ambrosio E.,Lara-Pezzi E., Gómez-Gaviro M.V. 2018: MouBeAT: a new and open toolbox for guided analysis of behavioral tests in mice. Front. Behav. Neurosci. 12: 1-12. PubMed DOI

Bjornstad O.N. 2020: Ncf: Spatial Covariance Functions, https://cran.r-project.org/web/packages/ncf/index.html.

Boratyński Z., Szyrmer M., Koteja P. 2020: The metabolic performance predicts home range size of bank voles: a support for the behavioral-bioenergetics theory. Oecologia 193: 547-556. PubMed DOI

Bougeard S., Dray S. 2018: Supervised multiblock analysis in R with the ade4 package. J. Stat. Softw. 86: 1-17. DOI

Boyard C., Vourc'h G., Barnouin J. 2008: The relationships between Ixodes ricinus and small mammal species at the woodland-pasture interface. Exp. Appl. Acarol. 44: 61-76. PubMed DOI

Boyer N., Réale D., Marmet J., Pisanu B., Chapuis J.-L. 2010: Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J. Anim. Ecol. 79: 538-547. PubMed DOI

Breheny P., Burchett W. 2017: Visualization of regression models using visreg. R J. 9: 56-71. DOI

Brehm A.M., Mortelliti A., Maynard G.A., Zydlewski J. 2019: Land-use change and the ecological consequences of personality in small mammals. Ecol. Lett. 22: 1387-1395. PubMed DOI

Brehm A.M., Tironi S., Mortelliti A. 2020: Effects of trap confinement on personality measurements in two terrestrial rodents. PLoS ONE 15: 1-14. PubMed DOI

Brunner J.L., Ostfeld R.S. 2008: Multiple causes of variable tick burdens on small-mammal hosts. Ecology 89: 2259-2272. PubMed DOI

Bürkner P.-C. 2017: brms: an R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80: 1-28. DOI

Bürkner P.-C. 2018: Advanced Bayesian multilevel modeling with the R package brms. R J. 10: 395-411. DOI

Carter A.J., Feeney W.E., Marshall H.H., Cowlishaw G., Heinsohn R. 2013: Animal personality: what are behavioural ecologists measuring? Biol. Rev. 88: 465-475. PubMed DOI

Cayol C., Giermek A., Gomez-chamorro A., Hyto J., Kallio E.R., Mappes T., Salo J., Voordouw M.J., Koskela E. 2018: Borrelia afzelii alters reproductive success in a rodent host. Proc. R. Soc. B Biol. Sci. 285: 20181056. PubMed DOI

Chessel D., Dufour A.-B., Thioulouse J. 2004: The ade4 package - I: One-table methods. R News 4: 5-10.

Cote J., Clobert J., Brodin T., Fogarty S., Sih A. 2010: Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 365: 4065-4076. PubMed DOI

Crofton H.D. 1971: A quantitative approach to parasitism. Parasitology 62: 179-193. DOI

Dammhahn M., Almeling L. 2012: Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim. Behav. 84: 1131-1139. DOI

Devevey G., Brisson D. 2012: The effect of spatial heterogeneity on the aggregation of ticks on white-footed mice. Parasitology 139: 915-25. PubMed DOI

Dingemanse N.J., Wright J. 2020: Criteria for acceptable studies of animal personality and behavioural syndromes. Ethol. 126: 865-869. DOI

Dingemanse N.J., Wright J., Kazem A.J., Thomas D.K., Hickling R., Dawnay N. 2007: Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J. Anim. Ecol. 76:1128-38. PubMed DOI

Dray S., Dufour A.B. 2007: The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22: 1-20. DOI

Dray S., Dufour A.B., Chessel D. 2007: The ade4 Package - II: Two-table and K -table Methods. R News 7: 47-52.

Fox J., Weisberg S. 2019: An R Companion to Applied Regression. SAGE, Thousand Oaks, CA, USA.

Gaitan J., Millien V. 2016: Stress level, parasite load, and movement pattern in a small mammal reservoir host for Lyme disease. Can. J. Zool. 94: 565-573. DOI

Godinho L.N., Cripps J.K., Coulson G., Lumsden L.F. 2013: The effect of ectoparasites on the grooming behaviour of gould's wattled bat (Chalinolobus gouldii): an experimental study. Acta Chiropterologica 15: 463-472. DOI

Harrison A., Scantlebury M., Montgomery W.I. 2010: Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119: 1099-1104. DOI

Hofmeester T.R., Coipan E.C., van Wieren S.E., Prins H.H.T.T., Takken W., Sprong H. 2016: Few vertebrate species dominate the Borrelia burgdorferi s.l. life cycle. Environ. Res. Lett. 11: 043001. DOI

Hu R., Yeh M.-T., Hyland K.E., Mather T.N. 1996: Experimental Babesia microti infection in golden hamsters: immunoglobulin G response and recovery from severe hemolytic anemia. J. Parasitol. 82: 728-732. PubMed DOI

Hughes V.L., Randolph S.E. 2001: Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. J. Parasitol. 87: 49-54. PubMed DOI

Johns J.L., Macnamara K.C., Walker N.J., Winslow G.M., Borjesson D.L. 2009: Infection with Anaplasma phagocytophilum induces multilineage alterations in hematopoietic progenitor cells and peripheral blood cells. Infect. Immun. 77: 4070-4080. PubMed DOI

Karlsson A.F., Potapov E.R. 1998: Consistency and change in bank vole (Clethrionomys glareolus) home ranges across a decade. Can. J. Zool. 76: 1329-1334. DOI

Kenagy G.J., Pearson O.P. 2000: Life with fur and without: experimental field energetics and survival of naked meadow voles. Oecologia 122: 220-224. PubMed DOI

Kiffner C., Vor T., Hagedorn P., Niedrig M., Rühe F. 2011: Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany. Parasitol. Res. 108: 323-35. PubMed DOI

Korn H. 1986: Changes in home range size during growth and maturation of the wood mouse (Apodemus sylvaticus) and the bank vole (Clethrionomys glareolus). Oecologia 68: 623-628. PubMed DOI

Korpela K., Sundell J., Ylönen H. 2011: Does personality in small rodents vary depending on population density? Oecologia 165: 67-77. PubMed DOI

Koskela E., Mappes T., Ylönen H. 1997: Territorial behaviour and reproductive success of bank vole Clethrionomys glareolus females. J. Anim. Ecol. 66: 341-349. DOI

Krasnov B.R., Bordes F., Khokhlova I.S., Morand S. 2012: Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76: 1-13. DOI

Larsen M.H., Mikkelsen J.D., Hay-Schmidt A., Sandi C. 2010: Regulation of brain-derived neurotrophic factor (BDNF) in the chronic unpredictable stress rat model and the effects of chronic antidepressant treatment. J. Psychiatr. Res. 44: 808-816. PubMed DOI

Liesenjohann M., Liesenjohann T., Trebaticka L., Haapakoski M., Sundell J., Ylönen H., Eccard J.A. 2011: From interference to predation: type and effects of direct interspecific interactions of small mammals. Behav. Ecol. Sociobiol. 65: 2079-2089. DOI

MacLeod J. 1932: The bionomics of Ixodes ricinus L., the "sheep tick" of Scotland. Parasitology 24: 382-400. DOI

Mazzamuto M.V., Cremonesi G., Santicchia F., Preatoni D., Martinoli A., Wauters L.A. 2019: Rodents in the arena: a critical evaluation of methods measuring personality traits. Ethol. Ecol. Evol. 31: 38-58. DOI

Mills S.C., Grapputo A., Jokinen I., Koskela E., Mappes T., Poikonen T. 2010: Fitness trade-offs mediated by immunosuppression costs in a small mammal. Evolution 64: 166-179. PubMed DOI

Milne A. 1943: The comparison of sheep-tick populations (Ixodes ricinus L.). Ann. Appl. Biol. 30: 240-250. DOI

Mysterud A., Byrkjeland R., Qviller L., Viljugrein H. 2015: The generalist tick Ixodes ricinus and the specialist tick Ixodes trianguliceps on shrews and rodents in a northern forest ecosystem - a role of body size even among small hosts. Parasit. Vectors 8: 639. PubMed DOI

Payne E., Sinn D.L., Spiegel O., Leu S.T., Gardner M., Godfrey S.S., Wohlfeil C., Sih A. 2021: Consistent after all: behavioural repeatability in a long-lived lizard across a 6-year field study. Anim. Behav. 174: 263-277. DOI

Perals D., Griffin A.S., Bartomeus I., Sol D. 2017: Revisiting the open-field test: what does it really tell us about animal personality? Anim. Behav. 123: 69-79. DOI

Perez G., Bastian S., Chastagner A., Agoulon A., Plantard O., Vourc'h G., Butet A. 2017: Ecological factors influencing small mammal infection by Anaplasma phagocytophilum and Borrelia burgdorferi s.l. in agricultural and forest landscapes. Environ. Microbiol. 19: 4205-4219. PubMed DOI

Perez-Eid C. 1990: Relationships between ticks and small mammals in the Alsatian focus of tickborne encephalitis. Acarologia 31: 131-141.

Perkins S.E., Cattadori I.M., Tagliapietra V., Rizzoli A.P., Hudson P.J. 2003: Empirical evidence for key hosts in persistence of a tick-borne disease. Int. J. Parasitol. 33: 909-917. PubMed DOI

Porto Neto L.R., Bunch R.J., Harrison B.E., Barendse W. 2011: DNA variation in the gene ELTD1 is associated with tick burden in cattle. Anim. Genet. 42: 50-55. PubMed DOI

R Core Team, The. 2020: R: A Language and Environment for Statistical Computing.

Rasband W. 2018: ImageJ 1.52a software available at https://imagej.nih.gov/ij/index.html.

Revelle W. 2021: Psych: Procedures for Psychological, Psychometric, and Personality Research, https://cran.r-project.org/web/packages/ncf/index.html.

Rollins R.E., Mouchet A., Margos G., Chitimia-Dobler L., Fingerle V., Becker N.S., Dingemanse N.J. 2021: Repeatable differences in exploratory behaviour predict tick infestation probability in wild great tits. Behav. Ecol. Sociobiol. 75: 48. DOI

Roth K.A., Katz R.J. 1979: Stress, behavioral arousal, and open field activity-a reexamination of emotionality in the rat. Neurosci. Biobehav. Rev. 3: 247-263. PubMed DOI

RStudio Team 2019: RStudio: Integrated Development Environment for R, https://www.rstudio.com/.

Santicchia F., Romeo C., Ferrari N., Matthysen E., Vanlauwe L., Wauters L.A., Martinoli A. 2019: The price of being bold? Relationship between personality and endoparasitic infection in a tree squirrel. Mamm. Biol. 97: 1-8. DOI

Sasaki M., Fujii Y., Iwamoto M., Ikadai H. 2013: Effect of sex steroids on Babesia microti infection in mice. Am. J. Trop. Med. Hyg. 88: 367-375. PubMed DOI

Savje F. 2019: Distances: Tools for Distance Metrics, https://cran.r-project.org/web/packages/distances/index.html.

Schad J., Dechmann D.K.N., Voigt C.C., Sommer S. 2012: Evidence for the "good genes" model: association of MHC class II DRB alleles with ectoparasitism and reproductive state in the Neotropical lesser bulldog bat, Noctilio albiventris. PLoS ONE 7: e37101. PubMed DOI

Schirmer A., Herde A., Eccard J.A., Dammhahn M. 2019: Individuals in space: personality-dependent space use, movement and microhabitat use facilitate individual spatial niche specialization. Oecologia 189: 647-660. PubMed DOI

Schradin C., Schmohl G., Rödel H.G., Schoepf I., Treffler S.M., Brenner J., Bleeker M., Schubert M., König B., Pillay N. 2010: Female home range size is regulated by resource distribution and intraspecific competition: a long-term field study. Anim. Behav. 79: 195-203. DOI

Shaw D.J., Dobson A.P. 1995: Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111: S111-S133. PubMed DOI

Steen H., Taitt M., Krebs C.J. 2002: Risk of parasite-induced predation: an experimental field study on Townsend's voles (Microtus townsendii). Can. J. Zool. 80: 1286-1292. DOI

Takumi K., Sprong H., Hofmeester T.R. 2019: Impact of vertebrate communities on Ixodes ricinus-borne disease risk in forest areas. Parasit. Vectors 12: 434. PubMed DOI

Telfer S., Lambin X., Birtles R., Beldomenico P., Burthe S., Paterson S., Begon M. 2010: Species interactions in a parasite community drive infection risk in a wildlife population. Science 330: 243-246. PubMed DOI

Tersago K., Schreurs A., Linard C., Verhagen R., Van Dongen S., Leirs H. 2008: Population, environmental, and community effects on local bank vole (Myodes glareolus) Puumala virus infection in an area with low human incidence. Vector-Borne Zoon. Dis. 8: 235-244. PubMed DOI

Thioulouse J., Dray S., Dufour A.-B., Siberchicot A., Jombart T., Pavoine S. 2018: Multivariate Analysis of Ecological Data with ade4. Springer, New York, 344 pp. DOI

Tschirren B. 2015: Borrelia burgdorferi sensu lato infection pressure shapes innate immune gene evolution in natural rodent populations across Europe. Biol. Lett. 11: 17-19. PubMed DOI

Vassallo M., Pichon B., Cabaret J., Figureau C.U., Pérez-Eid C. 2000: Methodology for sampling questing nymphs of Ixodes ricinus (Acari: Ixodidae), the principal vector of Lyme disease in Europe. J. Med. Entomol. 37: 335-339. PubMed DOI

Venables W.N., Ripley B.D. 2002: Modern Applied Statistics with S. Springer, New York, 498 pp. DOI

Wauters L.A., Mazzamuto M.V., Santicchia F., Martinoli A., Preatoni D.G., Lurz P.W.W., Bertolino S., Romeo C. 2021: Personality traits, sex and food abundance shape space use in an arboreal mammal. Oecologia 196: 65-76. PubMed DOI

Wiger R. 1978: Fatal experimental Babesia microti infections in the Norwegian lemming, Lemmus lemmus. Folia Parasitol. 25: 103-108.

Wold S., Esbensen K., Geladi P. 1987: Principal Component Analysis. Chemom. Intell. Lab. Syst. 2: 37-52. DOI

Wolf M., Weissing F.J. 2012: Animal personalities: consequences for ecology and evolution. Trends Ecol. Evol. 27: 452-461. PubMed DOI

Wolff J.O. 1985: The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can. J. Zool. 63: 2657-2662. DOI

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. Proc. Natl. Acad. Sci. U.S.A 94: 338-342. PubMed DOI