Survival of Ixodes ricinus (Acari: Ixodidae) nymphs under cold conditions is negatively influenced by frequent temperature variations

Ticks and Tick-borne Diseases

Volumn 4, Issue 5, 2013, Pages 445-451

  Herrmann, Coralie ^a   Gern, Lise ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Borrelia burgdorferi s.l.; Cold conditions; Ixodes ricinus; Lyme borreliosis; Survival; Winter

Indexed keywords

AGE; ANALYTIC METHOD; ARTICLE; AUTUMN; BACTERIUM IDENTIFICATION; BLOTTING; COLD; DISEASE ASSOCIATION; ENVIRONMENTAL TEMPERATURE; IXODES RICINUS; LONG TERM EXPOSURE; LYME DISEASE; NONHUMAN; NYMPH; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVERSE LINE BLOTTING; SIMULATION; SPECIES IDENTIFICATION; SPRING; SURVIVAL RATE; WINTER; ANIMAL; BORRELIA; ISOLATION AND PURIFICATION; IXODES; MICROBIOLOGY; PARASITE VECTOR; PHYSIOLOGY; SEASON; SWITZERLAND;

ACARI; BORRELIA; BORRELIA BURGDORFERI; BORRELIA BURGDORFERI GROUP; IXODES RICINUS; IXODIDA; IXODIDAE;

FAT;

ANIMALS; ARACHNID VECTORS; BORRELIA; COLD TEMPERATURE; FATS; IXODES; NYMPH; SEASONS; SWITZERLAND;

EID: 84883256768     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2013.05.002     Document Type: Article

References (43)

1. Alekseev A.N., Dubinina H.V., Van de Pol I., Schouls L.M. Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia. J. Clin. Microbiol. 2001, 39:2237-2242.
2. Belozerov V.N. Diapause and biological rhythms in ticks. Physiology of Ticks 1982, 469-500. Pergamon Press, Oxford. F.D. Obenchain, R. Galun (Eds.).
3. Brunner J.L., Killilea M., Ostfeld R.S. Overwintering survival of nymphal Ixodes scapularis (Acari: Ixodidae) under natural conditions. J. Med. Entomol. 2012, 49:981-987.
4. Burks C.S., Stewart R.L., Needham G.R., Lee R.E. The role of direct chilling injury and inoculative freezing in cold tolerance of Amblyomma americanum, Dermacentor variabilis and Ixodes scapularis. Physiol. Entomol. 1996, 21:44-50.
5. Burri C., Morán Cadenas F., Douet V., Moret J., Gern L. Ixodes ricinus density and infection prevalence with Borrelia burgdorferi sensu lato along a north-facing altitudinal gradient in the RhÔne Valley (Switzerland). Vector Borne Zoonotic Dis. 2007, 7:50-58.
6. Crooks E., Randolph S.E. Walking by Ixodes ricinus ticks: intrinsic and extrinsic factors determine the attraction of moisture or host odour. J. Exp. Biol. 2006, 209:2138-2142.
7. Daniel M., Černý V., Dusbábek F. Stratification of overwintering engorged larvae and nymphs of Ixodes ricinus (L.). Wiad. Parazytol. 1972, 18:727-730.
8. Dautel H., Dippel C., Kämmer D., Werkhausen A., Kahl O. Winter activity of Ixodes ricinus in a Berlin forest. Int. J. Med. Microbiol. 2008, 298(Suppl. 1):50-54.
9. Dautel H., Knülle W. Cold hardiness, supercooling ability and causes of low-temperature mortality in the soft tick, Argas reflexus, and the hard tick, Ixodes ricinus (Acari: Ixodidae) from Central Europe. J. Insect Physiol. 1997, 43:843-854.
10. Dennis D.T., Nekomoto T.S., Victor J.C., Paul W.S., Piesman J. Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the United States. J. Med. Entomol. 1998, 35:629-638.
11. Dusbábek F., Daniel M., Černý V. Stratification of engorged Ixodes ricinus larvae overwintering in soil. Folia Parasitol. 1971, 18:261-266.
12. Fujimoto K. Comparison of the cold hardiness of Ixodes nipponensis and I. persulcatus (Acari: Ixodidae) in relation to the distribution patterns of both species in the Chichibu mountains. Jpn. J. Sanit. Zool. 1994, 45:333-339.
13. Gern L., Douet V., Lopez Z., Rais O., Morán Cadenas F. Diversity of Borrelia genospecies in Ixodes ricinus ticks in a Lyme borreliosis endemic area in Switzerland identified by using new probes for reverse line blotting. Ticks Tick Borne Dis. 2010, 1:23-29.
14. Gigon F. Biologie d'Ixodes ricinus L. sur le Plateau Suisse - une contribution à l'écologie de ce vecteur 1985, Université de Neuchâtel, Neuchâtel, Switzerland, (Ph.D. Thesis).
15. Herrmann C., Gern L. Survival of Ixodes ricinus (Acari: Ixodidae) under challenging conditions of temperature and humidity is influenced by Borrelia burgdorferi sensu lato infection. J. Med. Entomol. 2010, 47:1196-1204.
16. Herrmann C., Gern L. Do level of energy reserves, hydration status and Borrelia infection influence walking by Ixodes ricinus (Acari: Ixodidae) ticks?. Parasitology 2012, 139:330-337.
17. Herrmann C., Voordouw M.J., Gern L. Ixodes ricinus ticks infected with the causative agent of Lyme disease, Borrelia burgdorferi sensu lato, have higher energy reserves. Int. J. Parasitol. 2013, 43:477-483.
18. Jaenson T.G.T., Jaenson D.G.E., Eisen L., Petersson E., Lindgren E. Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasite Vector 2012, 5:8.
19. Jore S., Viljugrein H., Hofshagen M., Brun-Hansen H., Kristoffersen A.B., Nygard K., Brun E., Ottesen P., Saevik B.K., Ytrehus B. Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit. Parasite Vector 2011, 4:84.
20. Jouda F., Perret J.-L., Gern L. Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. J. Med. Entomol. 2004, 41:162-169.
21. Lebet N., Gern L. Histological examination of Borrelia burgdorferi infections in unfed Ixodes ricinus nymphs. Exp. Appl. Acarol. 1994, 18:177-183.
22. Leighton P.A., Koffi J.K., Pelcat Y., Lindsay L.R., Ogden N.H. Predicting the speed of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J. Appl. Ecol. 2012, 49:457-464.
23. Lindgren E., Tälleklint L., Polfeldt T. Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ. Health Persp. 2000, 108:119-123.
24. MacLeod J. Ixodes ricinus in relation to its physical environment. II. The factors governing survival and activity. Parasitology 1935, 27:123-144.
25. MacLeod J. Ixodes ricinus in relation to its physical environment. IV. An analysis of the ecological complexes controlling distribution and activities. Parasitology 1936, 28:295-319.
26. MétéoSuisse Evolution climatique pour des stations du réseau Suisse de mesures climatiques 2012, http://www.meteosuisse.admin.ch/web/fr/climat/climat_aujourdhui/evolution_climatique_nbcn/Neuchatel.html.
27. Morán Cadenas F., Rais O., Jouda F., Douet V., Humair P.-F., Moret J., Gern L. Phenology of Ixodes ricinus and infection with Borrelia burgdorferi sensu lato along a North- and South-facing altitudinal gradient on Chaumont Mountain, Switzerland. J. Med. Entomol. 2007, 44:683-693.
28. Neelakanta G., Sultana H., Fish D., Anderson J.F., Fikrig E. Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J. Clin. Invest. 2010, 120:3179-3190.
29. North N., Kljun N., Kasser N., Heldstab J., Maibach M., Reutimann J., Guyer M. Changements climatiques en Suisse - indicateurs des causes, des effets et mesures. Etat de l'environnement No. 0728 2007, 77. Office Fédéral de l'Environnement, Bern.
30. Perret J.-L., Guigoz E., Rais O., Gern L. Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitol. Res. 2000, 86:554-557.
31. Postic D., Assous M.V., Grimont P.A.D., Baranton G. Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf(5S)-rrl(23S) intergenic spacer amplicons. Int. J. Syst. Bacteriol. 1994, 44:743-752.
32. Poupon M.-A., Lommano E., Humair P.-F., Douet V., Rais O., Schaad M., Jenni L., Gern L. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl. Environ. Microb. 2006, 72:976-979.
33. R Development Core Team R: A Language and Environment for Statistical Computing 2012, R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, http://www.R-project.org.
34. Randolph S.E., Green R.M., Hoodless A.N., Peacey M.F. An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int. J. Parasitol. 2002, 32:979-989.
35. Randolph S.E., Storey K. Impact of microclimate on immature tick-rodent interactions (Acari: Ixodidae): implications for parasite transmission. J. Med. Entomol. 1999, 36:741-748.
36. Rebetez M. Changes in daily and nightly day-to-day temperature variability during the twentieth century for two stations in Switzerland. Theor. Appl. Climatol. 2001, 69:13-21.
37. Rijpkema S.G.T., Molkenboer M.J.C.H., Schouls L.M., Jongejan F., Schellekens J.F.P. Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. J. Clin. Microb. 1995, 33:3091-3095.
38. Schwaiger M., Péter O., Cassinotti P. Routine diagnosis of Borrelia burgdorferi (sensu lato) infections using real-time PCR assay. Clin. Microbiol. Infect. 2001, 7:461-469.
39. Sharon M., Rowley W.A., Novak M.G., Platt K.B. Rates of Borrelia burgdorferi infection in Ixodes dammini (Acari: Ixodidae) in southwestern Wisconsin. J. Med. Entomol. 1992, 29:314-317.
40. Steele G.M., Randolph S.E. An experimental evaluation of conventional control measures against the sheep tick, Ixodes ricinus (L.) (Acari: Ixodidae). I. A unimodal seasonal activity pattern. Bull. Entomol. Res. 1985, 75:489-499.
41. Van Es R.P., Hillerton J.E., Gettinby G. Lipid consumption in Ixodes ricinus (Acari: Ixodidae): temperature and potential longevity. Bull. Entomol. Res. 1998, 88:567-573.
42. Vandyk J.K., Bartholomew D.M., Rowley W.A., Platt K.B. Survival of Ixodes scapularis (Acari: Ixodidae) exposed to cold. J. Med. Entomol. 1996, 33:6-10.
43. Yasyukevich V.V., Kazakova E.V., Popov I.O., Semenov S.M. Distribution of Ixodes ricinus L., 1758 and Ixodes persulcatus Schulze, 1930 (Parasitiformes, Ixodidae) in Russia and adjacent countries in view of observable climate changes. Dokl. Earth Sci. 2009, 427:1030-1034.