Abstract
Host-seeking ticks were collected in the Northern Apennines, Italy, by dragging at 35 sites, at altitudes ranging from 680 and 1670 m above sea level (asl), from April to November, in 2010 and 2011. Ixodes ricinus (4431 larvae, 597 nymphs and 12 adults) and Haemaphysalis punctata (11,209 larvae, 313 nymphs, and 25 adults) were the most abundant species, followed by Haemaphysalis sulcata (20 larvae, five nymphs, and 13 adults), Dermacentor marginatus (42 larvae and two adults) and Ixodes hexagonus (one nymph). Greatest numbers of ticks were collected at locations characterised by southern exposure and limestone substratum, at altitudes <1400 m asl; I. ricinus was most abundant in Turkey oak (Quercus cerris) wood, whereas H. punctata was mostly collected in hop hornbeam (Ostrya carpinifolia) wood and on exposed rocks. Ixodes ricinus was also found up to 1670 m asl, in high stand beech (Fagus sylvatica) wood. The overall prevalence of Borrelia burgdorferi sensu lato (sl) in 294 host-seeking I. ricinus nymphs was 8.5 %. Borrelia garinii was the most frequently identified genospecies (64.0 % of positive nymphs), followed by B. valaisiana, B. burgdorferi sensu stricto, B. afzelii, and B. lusitaniae. Based upon the comparison with the results of previous studies at the same location, these research findings suggest the recent invasion of the study area by the tick vector and the agents of Lyme borreliosis.
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References
Amore G, Tomassone L, Grego E, Ragagli C, Bertolotti L, Nebbia P, Rosati S, Mannelli A (2007) Borrelia lusitaniae in immature Ixodes ricinus (Acari: Ixodidae) feeding on common wall lizards in Tuscany, central Italy. J Med Entomol 44:303–307
Barandika JF, Berriatua E, Barral M, Juste RA, Anda P, García-Pérez AL (2006) Risk factors associated with ixodid tick species distributions in the Basque region in Spain. Med Vet Entomol 20:177–188
Bisanzio D, Amore G, Ragagli C, Tomassone L, Bertolotti L, Mannelli A (2008) Temporal variations in the usefulness of normalized difference vegetation index as a predictor for Ixodes ricinus (Acari: Ixodidae) in a Borrelia lusitaniae focus in Tuscany, central Italy. J Med Entomol 45:547–555
Ceballos L, Pintore MD, Tomassone L, Pautasso A, Bisanzio D, Mignone W, Casalone C, Mannelli A (2014) Habitat and occurrence of ixodid ticks in the Liguria region, northwest Italy. Exp Appl Acarol l64:121–135
Ciancio O, Corona P, Lamonaca A, Portoghesi L, Travaglini D (2006) Conversion of clearcut beech coppices into high forests with continuous cover: a case study in central Italy. For Ecol Manag 224:235–240
Ciucci P (1994) Movimenti attività e risorse del lupo (Canis lupus) in due aree dell’Appennino centro-settentrionale. Dissertation, Università La Sapienza, Roma
Cringoli G, Iori A, Rinaldi L, Veneziano V, Genchi C (2005) Zecche. Rolando Editore, Napoli
Curioni V, Cerquetella S, Scuppa P, Pasqualini L, Beninati T, Favia G (2004) Lyme disease and babesiosis: preliminary findings on the transmission risk in highly frequented areas of the Monti Sibillini National Park (Central Italy). Vector Borne Zoonotic Dis 4:214–220
Daniel M, Materna J, Honig V, Metelka L, Danielová V, Harcarik J, Kliegrová S, Grubhoffer L (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 17:139–145
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. Parasites Vectors 8:478
Danielová V, Daniel M, Schwarzová L, Materna J, Rudenko N, Golovchenko M, Holubová J, Grubhoffer L, Kilián P (2010) Integration of a tick-borne encephalitis virus and Borrelia burgdorferi sensu lato into mountain ecosystems, following a shift in the altitudinal limit of distribution of their vector, Ixodes ricinus (Krkonose mountains, Czech Republic). Vector Borne Zoonotic Dis 10:223–230
Dantas-Torres F, Otranto D (2013) Species diversity and abundance of ticks in three habitats in southern Italy. Ticks Tick Borne Dis 4:251–255
Dantas-Torres F, Lia RP, Capelli G, Otranto D (2013) Efficiency of flagging and dragging for tick collection. Exp Appl Acarol 61:119–127
Estrada-Peña A, Dehesa V, Sánchez C (1990) The seasonal dynamics of Haemaphysalis punctata, Rhipicephalus bursa and Dermacentor marginatus (Acari: Ixodidae) on sheep of Pais Vasco (Spain). Acarologia 31:17–24
Estrada-Peña A, Martinez J, Sanchez Acedo C, Quilez J, Del Cacho E (2004) Phenology of the tick, Ixodes ricinus, in its southern distribution range (central Spain). Med Vet Entomol 18:387–397
Estrada-Peña A, Farkas R, Jaenson TG, Koenen F, Madder M, Pascucci I, Salman M, Tarrés-Call J, Jongejan F (2013a) Association of environmental traits with the geographic ranges of ticks (Acari: Ixodidae) of medical and veterinary importance in the western Palearctic. A digital data set. Exp Appl Acarol 59:351–366
Estrada-Peña A, Gray JS, Kahl O, Lane RS, Nijhof AM (2013b) Research on the ecology of ticks and tick-borne pathogens-methodological principles and caveats. Front Cell Infect Microbiol 3:29
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(S1):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
Gray JS (1991) The development and seasonal activity of the tick, Ixodes ricinus: a vector of Lyme borreliosis. Rev Med Vet Entomol 79:323–333
Hartelt K, Pluta S, Oehme R, Kimmig P (2008) Spread of ticks and tick-borne diseases in Germany due to global warming. Parasitol Res 103(S1):109–116
Jaenson TG, Jaenson DG, 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
Jore S, Viljugrein H, Hofshagen M, Brun-Hansen H, Kristoffersen AB, Nygård K, Brun E, Ottesen P, Sævik BK, Ytrehus B (2011) Multi-source analysis reveals latitudinal and altitudinal shifts in range of Ixodes ricinus at its northern distribution limit. Parasit Vectors 4:84
Jore S, Vanwambeke SO, Viljugrein H, Isaksen K, Kristoffersen AB, Woldehiwet Z, Johansen B, Brun E, Brun-Hansen H, Westermann S, Larsen IL, Ytrehus B, Hofshagen M (2014) Climate and environmental change drives Ixodes ricinus geographical expansion at the northern range margin. Parasit Vectors 7:11
Jouda F, Perret J, Gern L (2004) Ixodes ricinus density and distribution and prevalence of Borrelia burgdorferi sl infection along and altitudinal gradient. J Med Entomol 41:162–169
Karbowiak G (2014) The occurrence of the Dermacentor reticulatus tick-its expansion to new areas and possible causes. Ann Parasitol 60:37–47
Kiewra D, Czulowska A (2013) Evidence for an increased distribution range of Dermacentor reticulatus in south-west Poland. Exp Appl Acarol 59:501–506
Léger E, Vourc’h G, Vial L, Chevillon C, McCoy KD (2013) Changing distributions of ticks: causes and consequences. Exp Appl Acarol 59:219–244
Lindgren E, Gustafson R (2001) Tick-borne encephalitis in Sweden and climate change. Lancet 358:16–18
Manilla G (1998) Acari, Ixodida (Fauna d’Italia 36). Edizioni Calderoni, Bologna
Mannelli A, Tolari F, Pedri P, Stefanelli S (1997) Spatial distribution and seasonality of ticks (Acarina: Ixodidae) in a protected area in the northern Apennines. Parassitologia 39:41–45
Mannelli A, Boggiatto G, Grego E, Cinco M, Murgia R, Stefanelli S, De Meneghi D, Rosati S (2003) Acarological risk of exposure to agents of tick-borne zoonoses in the first recognized Italian focus of Lyme borreliosis. Epidemiol Infect 131:1139–1147
Mannelli A, Bertolotti L, Gern L, Gray J (2012) Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiol 36:837–861
Martello E, Selmi M, Ragagli C, Ambrogi C, Stella MC, Mannelli A, Tomassone L (2013) Rickettsia slovaca in immature Dermacentor marginatus and tissues from Apodemus spp. in the northern Apennines, Italy. Ticks Tick Borne Dis 4:518–521
Martello E, Mannelli A, Ragagli C, Ambrogi C, Selmi M, Ceballos L, Tomassone L (2014) Range expansion of Ixodes ricinus to higher altitude, and co-infestation of small rodents with Dermacentor marginatus in the Northern Apennines, Italy. Ticks Tick Borne Dis 5:970–974
Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George JC, Golovljova I, Jaenson TGT, Jensen JK, Jensen PM, Kazimirova M, Oteo JA, Papa A, Pfister K, Plantard O, Randolph SE, Rizzoli AP, Santos-Silva MM, Sprong H, Vial L, Hendrickx G, Zeller H, Van Bortel W (2013) Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors 6:1–11
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
Pichon B, Estrada-Peña A, Kahl O, Mannelli A, Gray S (2006) Detection of animal reservoirs of tick-borne zoonoses in Europe. Int J Med Microbiol 296:129–130
Pintore MD, Ceballos L, Iulini B, Tomassone L, Pautasso A, Corbellini D, Rizzo F, Mandola ML, Bardelli M, Peletto S, Acutis L, Mannelli A, Casalone C (2015) Detection of invasive Borrelia burgdorferi strains in North-Eastern Piedmont, Italy. Zoonoses Public Health 62:365–374
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Regione Toscana (2015a) Scheda Stazione 097—ORECCHIELLA. http://agrometeo.arsia.toscana.it/modules.php?op=modload&name=CF_MenuBlock&file=Manager&act=P_1_1:@99&act2=97. Accessed Dec 2015
Regione Toscana (2015b) Dati meteo Stazione Meteo ORECCHIELLA. http://agroambiente.info.arsia.toscana.it. Accessed Dec 2015
Rijpkema SG, Molkenboer MJ, Schouls LM, Jongejan F, Schellekens JF (1995) 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 Microbiol 33:3091–3095
Rizzoli A, Hauffe HC, Tagliapietra V, Neteler M, Rosà R (2009) Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. PLoS ONE 4:e4336
Rudenko N, Golovchenko M, Grubhoffer L, Oliver JH Jr (2009) Borrelia carolinensis sp. nov., a new (14th) member of the Borrelia burgdorferi Sensu Lato complex from the southeastern region of the United States. J Clin Microbiol 47:134–141
Schwarz A, Hönig V, Vavrušková Z, Grubhoffer L, Balczun C, Albring A, Schaub G (2012) Abundance of Ixodes ricinus and prevalence of Borrelia burgdorferi s.l. in the nature reserve Siebengebirge, Germany, in comparison to three former studies from 1978 onwards. Parasit Vectors 5:268
Selmi M, Bertolotti L, Tomassone L, Mannelli A (2008) Rickettsia slovaca in Dermacentor marginatus ticks and tick borne lymphadenopathy (TIBOLA/DEBONEL) in Tuscany, central Italy. Emerg Infect Dis 14:817–820
Selmi M, Martello E, Bertolotti L, Bisanzio D, Tomassone L (2009) Rickettsia slovaca and Rickettsia raoultii in Dermacentor marginatus ticks collected on wild boars in Tuscany, Italy. J Med Entomol 46:1490–1493
Sprong H, Hofhuis A, Gassner F, Takken W, Jacobs F, van Vliet AJH, van Ballegooijen M, van der Giessen J, Takumi K (2012) Circumstantial evidence for an increase in the total number and activity of Borrelia-infected Ixodes ricinus in the Netherlands. Parasit Vectors 5:294
Tack W, Madder M, Baeten L, De Frenne P, Verheyen K (2012) The abundance of Ixodes ricinus ticks depends on tree species composition and shrub cover. Parasitology 139:1273–1281
Tagliapietra V, Rosà R, Arnoldi D, Cagnacci F, Capelli G, Montarsi F, Hauffe HC, Rizzoli A (2011) Saturation deficit and deer density affect questing activity and local abundance of Ixodes ricinus (Acari, Ixodidae) in Italy. Vet Parasitol 183:114–124
Acknowledgments
The Corpo Forestale dello Stato, Ufficio Territoriale per la Biodiversità, Lucca, provided accommodation, animal handling facilities, and valuable help. Michela Adami and Maurizio Pieroni, helped with fieldwork. The study was funded by the Fondazione Cassa di Risparmio di Lucca, and by the Department of Veterinary Sciences, University of Torino.
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Ragagli, C., Mannelli, A., Ambrogi, C. et al. Presence of host-seeking Ixodes ricinus and their infection with Borrelia burgdorferi sensu lato in the Northern Apennines, Italy. Exp Appl Acarol 69, 167–178 (2016). https://doi.org/10.1007/s10493-016-0030-9
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DOI: https://doi.org/10.1007/s10493-016-0030-9