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Relative density of host-seeking ticks in different habitat types of south-western Slovakia

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Abstract

Ixodes ricinus is a vector of microbial pathogens of medical and veterinary importance in Europe. Recently, increasing abundance of ticks has been observed in urban and suburban areas. The aim of this study was to investigate the tick species composition and examine correlations between local environmental variables and the relative density of host-seeking I. ricinus in two habitat types. Questing ticks were collected along six 100 m2 transects in urban/suburban locations of Bratislava town, and in a non-fragmented deciduous forest in the Small Carpathians Mountains (south-western Slovakia) during 2011–2013. In total, 6015 I. ricinus were collected (3435 and 2580 in the urban/suburban and natural habitat, respectively), out of which over 80 % were nymphs. Haemaphysalis concinna comprised 1.3 % of the tick collections. Peak I. ricinus nymph and adult host-seeking activities were registered in April–June. Spatial and temporal variation in tick relative density and differences in the subadult/adult ratio were observed between habitats and between locations within the same habitat type. The relative density of questing I. ricinus nymphs correlated negatively with altitude, geographical aspect and saturation deficit in a 64-day period comprising the 8-day period including the date of tick sampling and previous 56 days. No significant correlation was found between roe deer density and questing nymph density. The study revealed the presence of abundant I. ricinus populations in green areas of Bratislava, suggesting a risk of exposure of town dwellers and domestic and companion animals to potentially infected ticks.

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References

  • Atlas Krajiny Slovenskej Republiky. http://globus.sazp.sk/atlassr/. Accessed 24 April 2015

  • Allen RG, Pereira LS, Raes D, Smith M (1998) Crop evapotranspiration-Guidelines for computing crop water requirements-FAO Irrigation and drainage paper 56. FAO Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Alonso-Carné J, García-Martín A, Estrada-Peña A (2015) Modelling the phenological relationships of questing immature Ixodes ricinus (Ixodidae) using temperature and NDVI data. Zoonoses Public Health. doi:10.1111/zph.12203

    PubMed  Google Scholar 

  • Balashov YS (1998) Ixodid ticks, parasites and vectors of infections. Nauka, St. Petersburg

    Google Scholar 

  • Bartoń K (2013) MuMIn: Multi-model inference. R package version 1.9.0. https://r-forge.r-project.org/scm/viewvc.php/*checkout*/www/MuMIn-manual.pdf?revision=196&root=mumin

  • Bowman A, Nuttall P (2008) Ticks: biology, disease and control. Cambridge University Press, NewYork

    Book  Google Scholar 

  • Boyard C, Barnouin J, Gasqui P, Vourc’h G (2007) Local environmental factors characterizing Ixodes ricinus nymph abundance in grazed permanent pastures for cattle. Parasitology 134:987–994

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Burri C, Morán Cadenas F, Douet V, Moret J, Gern L (2007) Ixodes ricinus density and infection prevalence of Borrelia burgdorferi sensu lato along a north-facing altitudinal gradient in the Rhône Valley (Switzerland). Vector Borne Zoonotic Dis 7:50–58

    Article  PubMed  Google Scholar 

  • Carpi G, Cagnacci F, Neteler M, Rizzoli A (2008) Tick infestation on roe deer in relation to geographic and remotely sensed climatic variables in a tick-borne encephalitis endemic area. Epidemiol Infect 136:1416–1424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daniel M, Materna J, Hönig V, Metelka L, Danielová V, Harčarik J et al (2009) Vertical distribution of the tick Ixodes ricinus and tick-borne pathogens in the northern Moravian mountains correlated with climate warming (Jeseníky Mts., Czech Republic). Cent. Eur J Public Health 17(3):139–145

    Google Scholar 

  • Daniel M, Malý M, Danielová V, Kříž B, Nuttall P (2015) Abiotic predictors and annual seasonal dynamics of Ixodes ricinus, the major disease vector of Central Europe. Parasit Vectors 8:478

    Article  PubMed  PubMed Central  Google Scholar 

  • Dautel H, Kahl O (1999) Ticks (Acari: Ixodoidea) and their medical importance in the urban environment. In: Robinson WH, Rettich F, Rambo GW (eds) Proceedings of the 3rd International Conference on Urban Pests Czech, University of Agriculture, Prague, pp 7382

  • Dautel H, Dippel C, Kämmer D, Werkhausen A, Kahl O (2008) Winter activity of Ixodes ricinus in a Berlin forest. Int J Med Microbiol 298(S1):50–54

    Article  Google Scholar 

  • Derdáková M, Václav R, Pangrácova-Blaňarová L, Selyemová D, Koči J, Walder G, Špitalská E (2014) Candidatus Neoehrlichia mikurensis and its co-circulation with Anaplasma phagocytophilum in Ixodes ricinus ticks across ecologically different habitats of Central Europe. Parasit Vectors 7:160

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobson ADM, Randolph SE (2011) Modelling the effects of recent changes in climate, host density and acaricide treatments on population dynamics of Ixodes ricinus in the UK. J Appl Ecol 48:1029–1037

    Article  Google Scholar 

  • Dobson ADM, Taylor JL, Randolph SE (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 Tick Borne Dis 2:67–74

    Article  PubMed  Google Scholar 

  • Egyed L, Élő P, Sréter-Lancz Z, Széll Z, Balogh Z, Sréter T (2012) Seasonal activity and tick-borne pathogen infection rates of Ixodes ricinus ticks in Hungary. Ticks Tick Borne Dis 3:90–94

    Article  PubMed  Google Scholar 

  • Estrada-Peña A (2001) Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in Northern Spain. J Med Entomol 38:361–370

    Article  PubMed  Google Scholar 

  • Estrada-Peña A, de la Fuente J (2014) The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Res 108:104–128

    Article  PubMed  Google Scholar 

  • Estrada-Peña A, Venzal JM, Sánchez Acedo C (2006) The tick Ixodes ricinus: distribution and climate preferences in the western Palaearctic. Med Vet Entomol 20:189–197

    Article  PubMed  Google Scholar 

  • Gaede K, Knülle W (1997) On the mechanism of water vapour sorption from unsaturated atmospheres by ticks. J Exp Biol 200:1491–1498

    PubMed  Google Scholar 

  • Gern L, Morán Cadenas F, Burri C (2008) Influence of some climatic factors on Ixodes ricinus ticks studied along altitudinal gradients in two geographic regions in Switzerland. Int J Med Microbiol 298:55–59

  • Gilbert L (2010) Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? Oecologia 162:217–225

    Article  PubMed  Google Scholar 

  • Gilbert L, Aungier J, Tomkins JT (2014) Climate of origin affects tick (Ixodes ricinus) host-seeking behavior in response to temperature: implications for resilience to climate change? Ecol Evol 4:1186–1198

    Article  PubMed  PubMed Central  Google Scholar 

  • Gray JS (1998) The ecology of ticks transmitting Lyme borreliosis. Exp Appl Acarol 22:249–258

    Article  Google Scholar 

  • Gray JS, Dautel H, Estrada-Peña A, Kahl O, Lindgren E (2009) Effects of climate change on ticks and tick-borne diseases in Europe. Interdiscipl Perspect Infect Dis. doi:10.1155/2009/593232

    Google Scholar 

  • Hai VV, Almeras L, Socolovschi C, Raoult D, Parola P, Pagès F (2014) Monitoring human tick-borne disease risk and tick bite exposure in Europe: available tools and promising future methods. Ticks Tick Borne Dis 5:607–619

    Article  PubMed  Google Scholar 

  • Heyman P, Cochez C, Hofhuis A, van der Giessen J, Sprong H, Porter SR et al (2010) A clear and present danger: tick-borne diseases in Europe. Expert Rev Anti Infect Ther 8(1):33–50

    Article  PubMed  Google Scholar 

  • Hönig V, Svec P, Halas P, Vavruskova Z, Tykalova H, Kilian P, Vetiskova V et al (2015) Ticks and tick-borne pathogens in South Bohemia (Czech Republic)–Spatial variability in Ixodes ricinus abundance, Borrelia burgdorferi and tick-borne encephalitis virus prevalence. Ticks Tick Borne Dis 6:559–567

    Article  PubMed  Google Scholar 

  • Jaenson TGT, Jaenson DGE, Eisen L, Petersson E, Lindgren E (2012) Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasit Vectors 5:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Jore S, Viljugrein H, Hofshagen M, Brun-Hansen H, Kristoffersen AB, Nygård K et al (2011) Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit. Parasit Vectors 4:84

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiffner C, Lödige C, Alings M, Vor T, Rühe F (2010) Abundance estimation of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus). Exp Appl Acarol 52:73–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Knap N, Durmiši E, Saksida A, Korva M, Petrovec M, Avšič-Županc T (2009) Influence of climatic factors on dynamics of questing Ixodes ricinus ticks in Slovenia. Vet Parasitol 16:275–281

    Article  Google Scholar 

  • Koči J, Tarageľová V, Derdáková M, Selyemová D, Cíglerová I, Lenčáková D et al (2009) Tick seasonal dynamics and prevalence of tick-borne pathogens in Slovakia. In: Špitalská E, Kazimírová M, Kocianová E, Šustek Z (eds) Zborník z Konferencie „Labudove dni“2009. Virologický ústav SAV, Bratislava, pp 45–47

    Google Scholar 

  • Korbel L (1956) Poznámky o výskyte ixodových kliešťov v Podunajsku a v Malých Karpatoch. Acta Facultatis Rerum Naturalium Universitatis Comenianae, Zoologia 1:67–78

    Google Scholar 

  • Kožuch O, Labuda M, Lysy J, Wiesmann P, Krippel E (1990) Longitudinal study of natural foci of Central European encephalitis virus in West Slovakia. Acta Virol 34:537–544

    PubMed  Google Scholar 

  • Lauterbach R, Wells K, O’Hara RB, Kalko EKV, Renner SC (2013) Variable strength of forest stand attributes and weather conditions on the questing activity of Ixodes ricinus ticks over years in managed forests. PLoS One 8(1):e55365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George J-C et al (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors 6:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Mejlon HA, Jaenson TGT (1997) Questing behaviour of Ixodes ricinus ticks (Acari: Ixodidae). Exp Appl Acarol 21:747–754

    Article  Google Scholar 

  • Morán Cadenas F, Rais O, Jouda F, Douet V, Humair PF, Moret J, Gern L (2007) 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 44:683–693

    Article  PubMed  Google Scholar 

  • Nosek J (1971) Thew ecology, bonomics and behavior of Haemaphysalis (Haemaphysalis) concinna tick. Z Parasitenk 36:233–241

    CAS  PubMed  Google Scholar 

  • Obsomer V, Wirtgen M, Linden A, Claerebout E, Heyman P, Heylen D et al (2013) Spatial disaggregation of tick occurrence and ecology at a local scale as a preliminary step for spatial surveillance of tick-borne diseases: general framework and health implications in Belgium. Parasit Vectors 6:190

    Article  PubMed  PubMed Central  Google Scholar 

  • Ostfeld RS, Brunner JL (2015) Climate change and Ixodes tick-borne diseases of humans. Philos Trans R Soc B 370:2014–2051

    Article  Google Scholar 

  • Pan Y, Jackson RT (2008) Ethnic difference in the relationship between acute inflammation and serum ferritin in US adult males. Epidemiol Infect 136:421–431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Papáčová L, Stanko M (2008) Sezónna dynamika kliešťov (Ixodida) v rekreačných oblastiach Rimavskej kotliny. Natura Carpatica 49:211–216

    Google Scholar 

  • Perret J-L, Guigoz E, Rais O, Gern L (2000) Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitol Res 86:554–557

    Article  CAS  PubMed  Google Scholar 

  • Perret J-L, Guerin PM, Diehl P-A, Vlimant M, Gern L (2003) Darkness induces mobility, and saturation deficit limits questing duration, in the tick Ixodes ricinus. J Exp Biol 206:1809–1815

    Article  PubMed  Google Scholar 

  • Pfäffle M, Littwin N, Muders SV, Petney TN (2013) The ecology of tick-borne diseases. Int J Parasitol 43:1059–1077

    Article  PubMed  Google Scholar 

  • Porretta D, Mastrantonio V, Amendolia S, Gaiarsa S, Epis S, Genchi C et al (2013) Effects of global changes on the climatic niche of the tick Ixodes ricinus inferred by species distribution modeling. Parasit Vectors 6:271

    Article  PubMed  PubMed Central  Google Scholar 

  • Randolph SE (2009) Tick-borne disease systems emerge from the shadows: the beauty lies in molecular detail, the message in epidemiology. Parasitology 136:1403–1413

    Article  CAS  PubMed  Google Scholar 

  • Randolph SE, Storey K (1999) Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): implications for parasite transmission. J Med Entomol 36:741–748

    Article  CAS  PubMed  Google Scholar 

  • Randolph SE, Miklisova D, Lysy J, Rogers DJ, Labuda M (1999) Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118:177–186

    Article  PubMed  Google Scholar 

  • Randolph SE, Green RM, Hoodless AM, Peacey FM (2002) An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol 32:979–989

    Article  PubMed  Google Scholar 

  • Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári G et al (2014) Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Public Health 2:251

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Fons F, Fernández-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J (2012) Factors driving the abundance of Ixodes ricinus ticks and the prevalence of zoonotic I. ricinus-borne pathogens in natural foci. Appl Environ Microbiol 78:2669–2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salman M, Tarrés-Call J (2013) Ticks and tick-borne diseases. Geographical distribution and control strategies in the Euro-Asia region. CABI, Wallingford

    Book  Google Scholar 

  • Schulz M, Mahling M, Pfister K (2014) Abundance and seasonal activity of questing Ixodes ricinus ticks in their natural habitats in southern Germany in 2011. J Vector Ecol 39(1):56–65

    Article  PubMed  Google Scholar 

  • Schwarz A, Maier WA, Kistemann T, Kampen H (2009) Analysis of the distribution of the tick Ixodes ricinus L. (Acari: Ixodidae) in a nature reserve of western Germany using Geographic Information Systems. Int J Hyg Environ Health 212:87–96

    Article  PubMed  Google Scholar 

  • Siuda K (1993) Kleszcze Polski (Acari: Ixodida) Systematyka i rozmieszczenie. Polskie Towarzystwo Parazytologiczne, Warszawa

    Google Scholar 

  • Sonenshine DE, Roe RM (2014) Biology of Ticks, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Spitalska E, Kocianova E (2003) Tick-borne microorganisms in Southwestern Slovakia. Ann NY Acad Sci 990:196–200

    Article  PubMed  Google Scholar 

  • Špitalská E, Kocianová E, Výrosteková V (2002) Natural focus of Coxiella burnetii and rickettsiae of spotted fever group in southwestern Slovakia. Biol Bratisl 57:589–595

    Google Scholar 

  • Špitalská E, Boldiš V, Derdáková M, Selyemová D, Rusňáková Tarageľová V (2014) Rickettsial infection in Ixodes ricinus ticks in urban and natural habitats of Slovakia. Ticks Tick Borne Dis 5(2):161–165

    Article  PubMed  Google Scholar 

  • Svitálková Z, Haruštiaková D, Mahríková L, Berthová L, Slovák M, Kocianová E, Kazimírová M (2015) Anaplasma phagocytophilum prevalence in ticks and rodents in an urban and natural habitat in South-Western Slovakia. Parasit Vectors 8:276

    Article  PubMed  PubMed Central  Google Scholar 

  • Tack W, Madder M, De Frenne D, Vanhellemont M, Gruwez R, Verheyen K (2011) The effects of sampling method and vegetation type on the estimated abundance of Ixodes ricinus ticks in forests. Exp Appl Acarol 54:285–292

    Article  PubMed  Google Scholar 

  • Tack W, Madder M, Baeten L, Vanhellemont M, Gruwez R, Verheyen K (2012) Local habitat and landscape affect Ixodes ricinus tick abundances in forests on poor, sandy soils. Forest Ecol Manag 265:30–36

    Article  Google Scholar 

  • Tagliapietra V, Rosà R, Arnoldi D, Cagnacci F, Capelli G, Montarsi F et al (2011) Saturation deficit and deer density affect questing activity and local abundance of Ixodes ricinus (Acari, Ixodidae) in Italy. Vet Parasitol 183:114–124

    Article  CAS  PubMed  Google Scholar 

  • Uspensky I (2014) Tick pests and vectors (Acari: Ixodoidea) in European towns: Introduction, persistence and management. Ticks Tick-Borne Dis 5:41–47

    Article  PubMed  Google Scholar 

  • Walker AR (2001) Age structure of a population of Ixodes ricinus (Acari: Ixodidae) in relation to its seasonal questing. Bull Entomol Res 91:69–78

    CAS  PubMed  Google Scholar 

  • Welc-Falęciak R, Kowalec M, Karbowiak G, Bajer A, Behnke JM, Siński E (2014) Rickettsiaceae and Anaplasmataceae infections in Ixodes ricinus ticks from urban and natural forested areas of Poland. Parasit Vectors 7:121

    Article  PubMed  PubMed Central  Google Scholar 

  • Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W et al (2006) Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands. Appl Environ Microbiol 72:7594–7601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was funded by EU grant FP7-261504 EDENext and is catalogued by the EDENext Steering Committee as EDENext397 (http://www.edenext.eu). The contents of this publication are the sole responsibility of the authors and don’t necessarily reflect the views of the European Commission. Financial support by grant APVV DO7RP–0014–11 is also acknowledged. The authors wish to thank Neil Alexander for extracting and providing MODIS Data, the Slovak Hydrometeorological Institute for providing climatic data and Ing. Martin Čikovský (Ministry of Agriculture and Rural Development of the Slovak Republic) for providing data on game censuses.

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Authors and Affiliations

  1. Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia

    Mária Kazimírová, Zuzana Hamšíková, Lenka Mahríková & Mirko Slovák

  2. Institute of Virology, Biomedical Research Center, Slovak Academy of Sciences, Bratislava, Slovakia

    Elena Kocianová & Lenka Berthová

  3. Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010, San Michele all’Adige, TN, Italy

    Giovanni Marini & Roberto Rosá

  4. Department of Zoology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia

    Michala Mojšová

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  1. Mária Kazimírová
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  3. Elena Kocianová
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Correspondence to Mária Kazimírová.

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Kazimírová, M., Hamšíková, Z., Kocianová, E. et al. Relative density of host-seeking ticks in different habitat types of south-western Slovakia. Exp Appl Acarol 69, 205–224 (2016). https://doi.org/10.1007/s10493-016-0025-6

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