Particle and Fibre Toxicology | |
Lyme disease bacterium does not affect attraction to rodent odour in the tick vector | |
Maarten Jeroen Voordouw1  Jérémy Berret1  | |
[1] Laboratory of Ecology and Evolution of Parasites, Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, Neuchâtel, 2000, Switzerland | |
关键词: Vector-borne pathogen; Tick-borne disease; Tick questing behaviour; Lyme borreliosis; Ixodes ricinus; Host manipulation; Host choice behaviour; Borrelia garinii; Borrelia afzelii; Borrelia burgdorferi; | |
Others : 1181772 DOI : 10.1186/s13071-015-0856-8 |
|
received in 2015-03-17, accepted in 2015-04-13, 发布年份 2015 | |
【 摘 要 】
Background
Vector-borne pathogens experience a conflict of interest when the arthropod vector chooses a vertebrate host that is incompetent for pathogen transmission. The qualitative manipulation hypothesis suggests that vector-borne pathogens can resolve this conflict in their favour by manipulating the host choice behaviour of the arthropod vector.
Methods
European Lyme disease is a model system for studying this conflict because Ixodes ricinus is a generalist tick species that vectors Borrelia pathogens that are specialized on different classes of vertebrate hosts. Avian specialists like B. garinii cannot survive in rodent reservoir hosts and vice versa for rodent specialists like B. afzelii. The present study tested whether Borrelia genospecies influenced the attraction of field-collected I. ricinus nymphs to rodent odours.
Results
Nymphs were significantly attracted to questing perches that had been scented with mouse odours. However, there was no difference in questing behaviour between nymphs infected with rodent- versus bird-specialized Borrelia genospecies.
Conclusion
Our study suggests that the tick, and not the pathogen, controls the early stages of host choice behaviour.
【 授权许可】
2015 Berret and Voordouw; licensee BioMed Central.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150515080307708.pdf | 528KB | download | |
Figure 2. | 11KB | Image | download |
Figure 1. | 9KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
【 参考文献 】
- [1]Gern L, Humair P. Ecology of Borrelia burgdorferi sensu lato in Europe. Lyme Borreliosis Biology, Epidemiology and Control. CABI Int. 2002; 6:149-174.
- [2]Hoogstraal H, Aeschlimann A. Tick-host specificity. Bulletin de la société entomologique suisse. 1982; 55:5-32.
- [3]Keirans JE, Hutcheson H, Durden LA, Klompen J. Ixodes (Ixodes) scapularis (Acari: Ixodidae): redescription of all active stages, distribution, hosts, geographical variation, and medical and veterinary importance. J Med Entomol. 1996; 33(3):297-318.
- [4]McCoy KD, Léger E, Dietrich M. Host specialization in ticks and transmission of tick-borne diseases: a review. Front Cell Infect Microbiol. 2013; 3:57-68.
- [5]Ostfeld RS, Keesing F. Biodiversity series: the function of biodiversity in the ecology of vector-borne zoonotic diseases. Can J Zool. 2000; 78(12):2061-2078.
- [6]LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci. 2003; 100(2):567-571.
- [7]Casher L, Lane R, Barrett R, Eisen L. Relative importance of lizards and mammals as hosts for ixodid ticks in northern California. Exp Appl Acarol. 2002; 26(1-2):127-143.
- [8]Slowik TJ, Lane RS. Feeding preferences of the immature stages of three western North American ixodid ticks (Acari) for avian, reptilian, or rodent hosts. J Med Entomol. 2009; 46(1):115-122.
- [9]Salkeld DJ, Lane RS. Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology. 2010; 91(1):293-298.
- [10]Lane RS, Quistad G. Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis). J Parasitol. 1998; 84:29-34.
- [11]Lefèvre T, Koella JC, Renaud F, Hurd H, Biron DG, Thomas F. New prospects for research on manipulation of insect vectors by pathogens. PLoS Pathog. 2006; 2(7):e72.
- [12]Lefèvre T, Thomas F. Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect Genet Evol. 2008; 8(4):504-519.
- [13]Hurd H. Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol. 2003; 48(1):141-161.
- [14]Moore J. Parasites and the behavior of biting flies. J Parasitol. 1993; 79:1-16.
- [15]Beach R, Kiilu G, Leeuwenburg J. Modification of sand fly biting behavior by Leishmania leads to increased parasite transmission. Am J Trop Med Hyg. 1985; 34(2):278-282.
- [16]Wekesa JW, Copeland RS, Mwangi RW. Effect of Plasmodium falciparum on blood feeding behavior of naturally infected Anopheles mosquitoes in western Kenya. Am J Trop Med Hyg. 1992; 47(4):484-488.
- [17]Rossignol P, Ribeiro J, Spielman A. Increased intradermal probing time in sporozoite-infected mosquitoes. Am J Trop Med Hyg. 1984; 33:17-20.
- [18]Koella JC, SÖrensen FL, Anderson R. The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae. Proc Roy Soc Lond B Biol Sci. 1998; 265(1398):763-768.
- [19]Anderson RA, Koellaf J, Hurd H. The effect of Plasmodium yoeliinigeriensis infection on the feeding persistence of Anopheles stephensi Liston throughout the sporogonic cycle. Proc Roy Soc Lond B Biol Sci. 1999; 266(1430):1729-1733.
- [20]Koella JC, Rieu L, Paul RE. Stage-specific manipulation of a mosquito’s host-seeking behavior by the malaria parasite Plasmodium gallinaceum. Behav Ecol. 2002; 13(6):816-820.
- [21]Lacroix R, Mukabana WR, Gouagna LC, Koella JC. Malaria infection increases attractiveness of humans to mosquitoes. PLoS Biol. 2005; 3(9):1590-1593.
- [22]O'Shea B, Rebollar-Tellez E, Ward R, Hamilton J, El Naiem D, Polwart A. Enhanced sandfly attraction to Leishmania-infected hosts. Trans R Soc Trop Med Hyg. 2002; 96(2):117-118.
- [23]Cornet S, Nicot A, Rivero A, Gandon S. Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecol Lett. 2013; 16(3):323-329.
- [24]De Moraes CM, Stanczyk NM, Betz HS, Pulido H, Sim DG, Read AF, Mescher MC. Malaria-induced changes in host odors enhance mosquito attraction. Proc Natl Acad Sci. 2014; 111(30):11079-11084.
- [25]Meiners T, Werkhausen A, Nierhaus L, Dautel H. Infection of ticks with Borrelia afzelii cuts of olfactory orientation towards certain host kairomones. XI International Jena Symposium on Tick-Borne Diseases. Jena, Germany; 2011.
- [26]Vollandt D, Ruzek D, Dautel H, Meiners T, Niedrig M. Infection with tick-borne encephalitis virus changes responses of Ixodes ricinus nymphs and adults to mammal odours. XI International Jena Symposium on Tick-Borne Diseases. Jena, Germany; 2011.
- [27]Piesman J, Gern L. Lyme borreliosis in Europe and North America. Parasitology. 2004; 129:S191.
- [28]Hanincová K, Schäfer S, Etti S, Sewell H-S, Taragelova V, Ziak D, Labuda M, Kurtenbach K. Association of Borrelia afzelii with rodents in Europe. Parasitology. 2003; 126(01):11-20.
- [29]Kurtenbach K, Peacey M, Rijpkema SG, Hoodless AN, Nuttall PA, Randolph SE. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl Environ Microbiol. 1998; 64(4):1169-1174.
- [30]Kurtenbach K, Sewell H-S, Ogden NH, Randolph SE, Nuttall PA. Serum complement sensitivity as a key factor in Lyme disease ecology. Infect Immun. 1998; 66(3):1248-1251.
- [31]Kurtenbach K, De Michelis S, Etti S, Schäfer SM, Sewell H-S, Brade V, Kraiczy P. Host association of Borrelia burgdorferi sensu lato–the key role of host complement. Trends Microbiol. 2002; 10(2):74-79.
- [32]Huegli D, Hu C, Humair P-F, Wilske B, Gern L. Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. J Clin Microbiol. 2002; 40(12):4735-4737.
- [33]Humair P-F, Peter O, Wallich R, Gern L. Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland. J Med Entomol. 1995; 32(4):433-438.
- [34]Humair P-F, Gern L. Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Trop. 1998; 69(3):213-227.
- [35]Hanincová K, Taragelová V, Koci J, Schäfer SM, Hails R, Ullmann AJ, Piesman J, Labuda M, Kurtenbach K. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl Environ Microbiol. 2003; 69(5):2825-2830.
- [36]Heylen D, Matthysen E, Fonville M, Sprong H. Songbirds as general transmitters but selective amplifiers of Borrelia burgdorferi sensu lato genotypes in Ixodes rinicus ticks. Environ Microbiol. 2014; 16(9):2859-2868.
- [37]Humair P-F, Postic D, Wallich R, Gern L. An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralblatt für Bakteriologie. 1998; 287(4):521-538.
- [38]Kurtenbach K, Schäfer SM, Sewell H-S, Peacey M, Hoodless A, Nuttall PA, Randolph SE. Differential survival of Lyme borreliosis spirochetes in ticks that feed on birds. Infect Immun. 2002; 70(10):5893-5895.
- [39]Lommano E, Dvořák C, Vallotton L, Jenni L, Gern L. Tick-borne pathogens in ticks collected from breeding and migratory birds in Switzerland. Ticks and Tick-Borne Diseases. 2014; 5(6):871-882.
- [40]Norte A, Ramos J, Gern L, Núncio M, Lopes de Carvalho I. Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: circulation of B. turdi and other genospecies in bird–tick cycles in Portugal. Environ Microbiol. 2013; 15(2):386-397.
- [41]Norte AC, Lopes de Carvalho I, Núncio MS, Ramos JA, Gern L. Blackbirds Turdus merula as competent reservoirs for Borrelia turdi and Borrelia valaisiana in Portugal: evidence from a xenodiagnostic experiment. Environ Microbiol Rep. 2013; 5(4):604-607.
- [42]Taragel'ová V, Koči J, Hanincová K, Kurtenbach K, Derdáková M, Ogden NH, Literák I, Kocianová E, Labuda M. Blackbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of borreliosis in Central Europe. Appl Environ Microbiol. 2008; 74(4):1289-1293.
- [43]Crooks E, Randolph SE. Walking by Ixodes ricinus ticks: intrinsic and extrinsic factors determine the attraction of moisture or host odour. J Exp Biol. 2006; 209(11):2138-2142.
- [44]QIAGEN. Purification of total DNA from ticks using the DNeasy® Blood & Tissue Kit for detection of Borrelia DNA (DY16 Jun-08). In. QIAGEN Supplementary Protocol; 2008.
- [45]Schwaiger M, Peter O, Cassinotti P. Routine diagnosis of Borrelia burgdorferi (sensu lato) infections using a real‐time PCR assay. Clin Microbiol Infect. 2001; 7(9):461-469.
- [46]Wallich R, Moter S, Simon M, Ebnet K, Heiberger A, Kramer M. The Borrelia burgdorferi flagellum-associated 41-kilodalton antigen (flagellin): molecular cloning, expression, and amplification of the gene. Infect Immun. 1990; 58(6):1711-1719.
- [47]Alekseev AN, Dubinina HV, Van De Pol I, Schouls LM. Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia. J Clin Microbiol. 2001; 39(6):2237-2242.
- [48]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(6):1196-1204.
- [49]Richter D, Postic D, Sertour N, Livey I, Matuschka F-R, Baranton G. Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp. nov. Int J Syst Evol Microbiol. 2006; 56(4):873-881.
- [50]Madden T. The BLAST Sequence Analysis Tool. The NCBI Handbook [Internet] 2002, Chapter 16(Bethesda (MD): National Center for Biotechnology Information (US)).
- [51]RStudio. RStudio: Integrated development environment for R (Version 0.98.1102) [Computer software]. 2014, http://www.rstudio.org/.
- [52]Cadenas FM, Rais O, Humair P-F, Douet V, Moret J, Gern L. Identification of host bloodmeal source and Borrelia burgdorferi sensu lato in field-collected Ixodes ricinus ticks in Chaumont (Switzerland). J Med Entomol. 2007; 44(6):1109-1117.
- [53]Herrmann C, Gern L. Survival of Ixodes ricinus (Acari: Ixodidae) nymphs under cold conditions is negatively influenced by frequent temperature variations. Ticks and Tick-Borne Diseases. 2013; 4(5):445-451.
- [54]Herrmann C, Gern L. Do the level of energy reserves, hydration status and Borrelia infection influence walking by Ixodes ricinus (Acari: Ixodidae) ticks? Parasitology. 2012; 139(03):330-337.
- [55]Herrmann C, Voordouw M, 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(6):477-483.
- [56]Lefcort H, Durden L. The effect of infection with Lyme disease spirochetes (Borrelia burgdorferi) on the phototaxis, activity, and questing height of the tick vector Ixodes scapularis. Parasitology. 1996; 113(02):97-103.
- [57]Romashchenko AV, Ratushnyak AS, Zapara TA, Tkachev SE, Moshkin MP. The correlation between tick (Ixodes persulcatus Sch.) questing behaviour and synganglion neuronal responses to odours. J Insect Physiol. 2012; 58(7):903-910.
- [58]Herrmann C, Gern L. Search for blood or water is influenced by Borrelia burgdorferi in Ixodes ricinus. Parasites & Vectors. 2015; 8(1):6-6. BioMed Central Full Text
- [59]Waladde S, Rice M. The sensory basis of tick feeding behaviour. In: The Physiology of Ticks. Obenchain FD, Galun R, editors. Pergamon Press, Oxford; 1982: p.71-118.
- [60]Carroll J, Mills G, Schmidtmann E. Field and laboratory responses of adult Ixodes scapularis (Acari: Ixodidae) to kairomones produced by white-tailed deer. J Med Entomol. 1996; 33(4):640-644.
- [61]Carroll J, Klun J, Schmidtmann E. Evidence for kairomonal influence on selection of host-ambushing sites by adult Ixodes scapularis (Acari: Ixodidae). J Med Entomol. 1995; 32(2):119-125.
- [62]Carroll J. Notes on responses of blacklegged ticks (Acari: Ixodidae) to host urine. J Med Entomol. 1999; 36(2):212-215.
- [63]Carroll J. Responses of adult Ixodes scapularis (Acari: Ixodidae) to urine produced by white-tailed deer of various reproductive conditions. J Med Entomol. 2000; 37(3):472-475.
- [64]Lees A. The sensory physiology of the sheep tick, Ixodes ricinus L. J Exp Biol. 1948; 25(2):145-207.
- [65]Gern L. Tiques et borréliose de Lyme en Suisse occidentale. Bull Soc Neuchateloise Scie Nat. 2004; 127(1):5-21.
- [66]Ogden N, Nuttall P, Randolph S. Natural Lyme disease cycles maintained via sheep by co-feeding ticks. Parasitology. 1997; 115(6):591-599.
- [67]Pichon B, Rogers M, Egan D, Gray J. Blood-meal analysis for the identification of reservoir hosts of tick-borne pathogens in Ireland. Vector Borne Zoonotic Dis. 2005; 5(2):172-180.
- [68]Harrison A, Montgomery W, Bown K. Investigating the persistence of tick-borne pathogens via the R0 model. Parasitology. 2011; 138(7):896.
- [69]Ekner A, Dudek K, Sajkowska Z, Majláthová V, Majláth I, Tryjanowski P. Anaplasmataceae and Borrelia burgdorferi sensu lato in the sand lizard Lacerta agilis and co-infection of these bacteria in hosted Ixodes ricinus ticks. Parasites & Vectors. 2011; 4(1):1-7. BioMed Central Full Text
- [70]De Sousa R, de Carvalho IL, Santos A, Bernardes C, Milhano N, Jesus J, Menezes D, Núncio M. Role of the lizard Teira dugesii as a potential host for Ixodes ricinus tick-borne pathogens. Appl Environ Microbiol. 2012; 78(10):3767-3769.
- [71]Kempf F, De Meeûs T, Vaumourin E, Noel V, Taragel’ová V, Plantard O, Heylen DJ, Eraud C, Chevillon C, McCoy KD. Host races in Ixodes ricinus, the European vector of Lyme borreliosis. Infect Genet Evol. 2011; 11(8):2043-2048.
- [72]Shaw MT, Keesing F, McGrail R, Ostfeld RS. Factors influencing the distribution of larval blacklegged ticks on rodent hosts. Am J Trop Med Hyg. 2003; 68(4):447-452.
- [73]Swei A, Ostfeld RS, Lane RS, Briggs CJ. Impact of the experimental removal of lizards on Lyme disease risk. Proc Biol Sci. 2011; 278(1720):2970-2978.