Table Of Content©EntomologicaFennica.13March2012
Ixodes persulcatus [Schulze 1930] (Acari: Ixodidae)
in eastern Finland
SergeyBugmyrin,TimoJ.Hokkanen*,LidiyaRomanova,Lubov’Bespyatova,
FyodorFyodorov,LudmilaBurenkova,AlinaYakimova&EvgeniyIeshko
Bugmyrin,S,Hokkanen.T.J.,Romanova,L.,Bespyatova,L.,Fyodorov,F.,Bu-
renkova,L.,Yakimova,A.&Ieshko,E.2011:Ixodespersulcatus[Schulze1930]
(Acari:Ixodidae)ineasternFinland.—Entomol.Fennica22:268–273.
DataconcerningtheoccurrenceandabundanceofthetaigatickIxodespersul-
catus in eastern Finland (North Karelia and Kainuu regions) are presented.
SamplingwascarriedoutinMay2008andJune2009,aroundtheUniversityof
JoensuuMekrijärviResearchStationandtheCityofKuhmo.In2008and2009,
theabundanceofadulttaigaticksinthefirststudyareawas0.17and0.13ticks
perflag-km,respectively.OnlyasingleI.persulcatusspecimenwasfoundinthe
secondstudyarea(abundancewas0.02specimensperflag-km).Allticks(635
specimens)collectedfromcatsanddogsinsouth-easternFinlandwereidentified
asIxodesricinus.
S.Bugmyrin,L.Bespyatova,F.Fyodorov,A.Yakimova&E.Ieshko,Instituteof
Biology,KarelianResearchCentre,RussianAcademyofScience,11Pushkins-
kayaSt.,185910,Petrozavodsk,Russia.E-mail:[email protected]
T.J.Hokkanen(*correspondingauthor),NorthKareliaBiosphereReserve,P.O.
Box69,80101Joensuu,Finland.E-mail:[email protected]
L.Romanova&L.Burenkova,M.P.ChumakovInstituteofPoliomyelitisandVi-
ral Encephalitides, Russian Academy of Medical Sciences, Moscow Region
142782,Russia
Received1May2010,accepted18April2011
1.Introduction Karelia connecting the points N 63°15 E 33°15
andN61°15E31°55(Lutta&Shulman1954).
Changesintherangeofnaturalfocusinfections, Later (1960’s–70’s), the species was also noted
includinginfectionstransmittedbyixodidticks, ontheNWshoreofLakeLadoganearthecityof
isa“hot”topicinrecentdiscussionsonemerging Sortavala(Korenberg1985).Morerecentlythere
infectious diseases (Lindgren et al. 2000, Ran- have been several records of the ticks from the
dolph 2000, Broker & Gniel 2003, Zeman & Kokkola Archipelago in western Finland
Benes2003,Sumiloetal.2006,Eisen2008,Gray (Jääskeläinen et al. 2006), which is still further
etal.2009).Themainreasonforthisinterestis north from the long-standing NW limit of its
thegrowingabundanceanddistributionofIxodes distribution. Furthermore, the abundance of the
ticks–themainvectorsoftick-borneencephalitis taiga tick within its historical range in Russian
(TBE)andLymeborreliosis. Kareliahasincreasedmarkedlyoverthepastfew
In the 1950’s, the northwestern limit of the decades (Bespyatova et al. 2006). In this study
range of Ixodes persulcatus ran across Russian weinvestigatethespeciescompositionandabun-
ENTOMOL.FENNICAVol.22 (cid:127) IxodespersulcatusineasternFinland 269
gether, 20 male ticks 19 females and 4 nymphs
werecollectedinthestudyperiod.Thetickswere
keptinmoistbandagewrappedinfoilorplastic
bagsandstoredat+4°Cbeforeidentification.
Additional samples of adult ticks were col-
lectedfromcatsanddogsduringJune–September
2008 with the help of pet owners in Liperi,
Parikkala, Pyhäselkä, Uukuniemi, Kesälahti,
Tohmajärvi,Värtsilä,Kiteeandvariouspartsof
Joensuutown.Tickscollectedfromtheseanimals
werefixedin70%ethanol(withacollectingin-
formationlabel).Atotalof635ticks(192male,
443female)werecollectedfrompets.
Theabundanceofticklarvaeandnymphswas
estimatedfromtheinfestationrateonsmallmam-
malscapturedintraps.Intotal,32transectswith
25–50trapseachwerearrangedandexposeddur-
ing2–5nights,amountingintotalto3,525trap-
nights(2,925inMekrijärviand600inKuhmo).
We captured 45 small mammals (43 of them
(from Mekrijärvi) belonging to three species:
common shrew Sorex araneus Linnaeus, 1758
Fig.1.Fieldstudyareas.MekrijärviResearchStation (16 specimens), bank vole Myodes glareolus
anditssurroundings.–a.20–30May2008and3–8 (Schreber, 1780) (24 specimens) and field vole
June2009;Kuhmoarea(FriendshipPark).–b.9–13 Microtusagrestis(Linnaeus,1761)(1specimen).
June2009.Separatedotsdenotesiteswhereticks
Theseyielded13nymphsand16larvaeofIxodes.
werecollectedfromdogsandcats.
The tick infestation rate of small mammals was
calculatedasprevalence(Pr)–thepercentageof
danceofticksineasternFinlandneartheRussian infected hosts, and as abundance index (Ab) –
bordertoobtainbase-linedataontheabundance mean abundance of Ixodes per small mammal
ofIxodespersulcatusandI.ricinusinthisarea. (Margolis et al. 1982). The larvae and nymphs
werefixedin70%ethanol.Forfurtheridentifica-
tion, temporary mounts with Fora-Berlese me-
2.Materialandmethods diumwereprepared.Thetickspecieswereidenti-
fied using morphology, following Filippova
TicksamplingtookplaceinEastFinland(North- (1977).
ernKareliaandKainuuregions),aroundtheUni- Taxonomicidentityoftheticksin2poolsof3
versity of Joensuu Mekrijärvi Research Station and4ticks(collectedbyflagging)and5individ-
andtheCityofKuhmo(Fig.1).Thesurveyswere ualticks(collectedfrompets)wasconfirmedby
carriedoutinMay2008andinJune2009. sequencingpartofITS2rRNA.Forthispurpose
Tickabundancewasestimatedusingstandard the ticks were pre-treated by rinsing with 96%
methods. Adults and nymphs werecollected by ethanolandtwicewithphysiologicalNaClsolu-
flagging (a square of white waffle cotton cloth tion. The ticks were homogenized in 200 µl of
(0.7×1.1m)ispulledalongthegroundandover medium199onEarle’ssolution(PIPVE,Russia).
vegetation),andtheabundancewasconvertedto Nucleic acids (both RNA and DNA) were iso-
“ticksper1flag-kilometer”.AroundMekrijärvi, latedusingastandardkitprotocol(“RNA/DNA
160 and 75 flag-km were covered in 2008 and extractionkitforbloodserumorplasmasamples”
2009respectively.About100transectsofvarying Lytech, Russia). ITS2 rRNA was amplified by
lengthwerecovered.WithinKuhmo(2009only), PCRwithprimers3SAandJB9A(Barker1998).
44 flag-km were sampled in 28 transects. Alto- This method is originally to determine rhipi-
270 Bugmyrinetal. (cid:127) ENTOMOL.FENNICAVol.22
Table1.Ixodesricinuscollectedfromcatsanddogs Table2.Numbers,prevalenceandabundanceof
fromvariousFinnishmunicipalitiesalongthewestern Ixodespersulcatuslarvaeandnymphsonsmallmam-
sideoftheFinnish-Russianborderin2008. malsinMekrijärviarea.
Site No.of No.ofticks No. Pr% Ab
collectors
(petowners) CommonshrewSorexaraneus(n=16)
ofticks Females Males Larvae 8 6.2 0.5
Patvinsuo 1 1 0 BankvoleMyodesglareolus(n=26)
Joensuu 7 103 26 Larvae 2 7.7 0.1
Liperi 1 2 2 Nymphs 2 7.7 0.1
Pyhäselkä 1 6 2 Total
Tohmajärvi 7 159 70 Larvae 10 7.1 0.2
Värtsilä 2 14 23 Nymphs 2 4.8 0.05
Kitee 18 119 49
Kesälahti 4 17 4 No.=Numberofticks
n=Numberofsmallmammals
Uukuniemi 1 22 7
Pr%=Prevalence:percentageofinfectedhosts
Parikkala 1 0 9 Ab=Abundanceindex:meanabundanceofI.persulcatus
persmallmammal
Totalno. 443 192
cephalineticks.However,ithasalsobeenusedto Mekrijärvi site. These equated to a prevalence
estimatethephyleticrelationshipsamongIxodes (and abundance) of I. persulcatus of 7.1% (0.2
spp.(Fukunagaetal.2000). larvaeperrodent)and4.8%(0.05nymphsperro-
To determine the infection rates of Borrelia dent)forlarvaeandnymphsrespectively(Table
burgdorferi(sensulato)andtick-borneencepha- 2). At the other site (Kuhmo), only two small
litis virus in the ticks RNAwas reversely tran- mammalswerecaptured(abankandafieldvole),
scribed using M-MLV reverse transcriptase kit andnotickswerefoundonthem.
(Promega, USA) and random hexanucleotides All adult ticks (39 specimens) collected by
(Syntol,Russia),accordingtothemanufacturer’s flaggingwereidentifiedasI.persulcatus.For2
protocol. The 16S rRNA of the Borrelia burg- tickpools(of3and4ticks)identificationbymor-
dorferi(sensulato)complexwasidentifiedusing phologicalcriteriawasconfirmedbysequencing
PCRwiththeLDprimersetofMarconi&Garon part ITS2 rRNA (GenBank HM055905,
(1992).ThepresenceofTBEviruswasdemon- HM072039). The obtained sequence was clear
stratedusingprimersspecifictoNS5regionsof enoughtoruleoutthepossibilityofhavingsev-
the TBEV genome: TBEL1 (5’-TCT-GAG- eralspeciesinthosetwopools.Theonly speci-
GGA-GAC-ACA-CTT-GG-3’) and Kgg57 (5’- menofI.ricinus(Linnaeus,1758)identifiedwas
TGC-TGA-ACA-CAT-CCA-TTC-C-3’). a nymph found in the south of the study area
Theticksin5poolsof2–4ticks(13male,2fe- (N62°18.3;E30°48.9).
male) and 9 individual ticks (3 male, 6 female) In 2008 and 2009, the abundance of adult
collectedbyflagginginMekrijärviweretestedby taigaticksinthefirststudypolygon(Fig.1a)was
thismethod. 0.17and0.13ticksperflag-km,respectively,and
I.persulcatuswasfoundin11of96transectssur-
veyed(Table3).Allofthefindswerelocatedin
3.Results the immediate vicinity of settlements (or aban-
donedhamlets),andthisrepresentsthemosttypi-
Allticklarvaeandnymphscollectedfromsmall cal habitat of this species. Mean abundance of
mammalsfromthestudiedareasbelongedtotwo adulttaigaticksinthesetransectswas2.6and0.8
speciesI.persulcatusSchulze,1930(10larvae,2 ticksperflag-kmin2008and2009,respectively.
nymphs)andI.triangulicepsBirula,1895(6lar- TheonlyI.persulcatusspecimen(female)in
vae, 11 nymphs). These were found only at the the second polygon (Fig. 1b) was found in one
ENTOMOL.FENNICAVol.22 (cid:127) IxodespersulcatusineasternFinland 271
Table3.AbundanceofIxodespersulcatusintwelvestudylocationsinsouth-easternFinland.Dashes=notstud-
ied.
Siteid. Coordinate 2008 2009
No.ofticks No.ofticks No.ofticks No.ofticks
(males/females/ perflag-km (males/ perflag-km
nymphs) (males/females/ females) (males/
nymphs) females)
Mekrijärvi(ainFig.1)
1 N62°42’E31°21.8’ 3/2/0 1.1/0.8/0 1/0 0.7/0
2 N62°40.2’E31°19.9’ 3/4/0 4.7/6.2/0 0 0
3 N62°50.2’E31°16.7’ 0/0/2 0/0/0.6 – –
4 N62°51.9’E31°29.4’ 2/3/0 0.6/1.0/0 1/1 0.6/0.6
5 N62°46’E30°59.3’ 2/0/1 0.2/0/0.1 1/1 0.1/0.1
6 N62°50.5’E30°46.0’ 3/1/0 1.4/0.5/0 1/1 0.6/0.6
7 N62°49.8’E30°41.3’ 0/3/0 0/1.4/0 0/1 0/0.6
8 N62°39’E31°01.2’ 1/0/0 0.2/0/0 – –
9 N62°42.9’E30°35.8’ – – 1/0 0.7/0
10 N63°11’E31°01.6’ – – 0/1 0/0.5
11 N63°16.9’E30°36.4’ – – 1/0 0.7/0
Kuhmo(binFig.1)
12 N63°57.1’;E29°43.2’ – – 0/1 0/0.7
(N63°57.1 ; E29°43.2 ) of the 28 transects sur- 4.Discussion
veyedin2009.Thisequatedtoanabundanceof
0.02ticksperflag-km. Thefirstconclusionfromthisstudyisthatviable
Thetickscollectedfromcatsanddogsfrom I. persulcatus populations exist in eastern Fin-
variouspartsofNorthKareliain2008(Table1) land.Theevidenceforthisisthenumberofposi-
wereallidentifiedasI.ricinusbymorphological tive transects, the repeated recording of ticks in
criteria.However,itwasnotpossibletoidentify thetransects,andthepresenceofalldevelopment
tospecies5specimensbymorphologicalcriteria. stages. The specific identity of ticks was deter-
PartialsequencingofITS2rRNAidentifiedthese mined not only by morphological criteria, but
ticks as I. ricinus (GenBank HM055901- wasconfirmedbygenotyping.
HM055904,HM208308). Most taiga ticks were found in the area be-
NoBorreliaburgdorferi(sensulato)complex tween N 63° in the north and N 62° 30 in the
spirochaetesorTBEvirus-infectedtickswerede- south.ThenorthernmostfindingofI.persulcatus
tected.Weweresomewhatsurprisedwiththere- wasfromasite60kmsouthofKuhmo(Table3),
sultthatnoBorreliawasfoundinticksexamined suggestingthatmoresamplingisnecessarytode-
by us, because it is usually found in the area finethenorthernborderofI.persulcatusdistribu-
(Bugmyrinetal.2008).Butwedonothavebases tionineasternFinland.
todoubtthecorrectnessofthetechnique,asthe Theestimatedabundancesoftaigaticksinthe
materialwasprocessednotasaseparatesample studied area are very low for all stages – much
butinparallelwithticksfromotherregions(the lowerthanincentralandeasternKarelia(Russia).
Moscow region, Karelia) for which positive re- Forexample,insomepartsofRussianKareliathe
sultswerereceived.TBEvirus,ontheotherhand, abundance of adult ticks I. persulcatus in 2008
isusually foundonly inlowfrequency (Jääske- wasgreaterthan20ticksperflag-km(Bugmyrin
läinenetal.2010).Accordingly,ournegativere- et al. 2008), while in the Mekrijärvi area the
sultforitintotalof29tickswasnotunexpected. abundancewastwoordersofmagnitudelower–
0.17in2008and0.13in2009.Thelowerabun-
dance in 2009, estimated using monitoring sur-
272 Bugmyrinetal. (cid:127) ENTOMOL.FENNICAVol.22
veys (Table 2), could have been the result of a References
slightlylatersurvey(2weekslaterintheseason)
orofunfavourableweatherconditionswithrain. Barker,S.C.1998:Distinguishingspeciesandpopulations
The distribution of I. persulcatus was con- ofRhipicephalinetickswithITS2RibosomalRNA.
—TheJournalofParasitology84:887–892.
finedtoareasclosetotheFinnish-Russianborder
Bespyatova, L., Ieshko, E., Ivanter, E. & Bugmyrin, S.
and the species was not found in samples pro-
2006:Long-termpopulationdynamicsofixodidticks
videdbypetownersfromvillagesandtowns.The anddevelopmentoftick-borneencephalitisfociunder
areaswherepeoplelivearedry,bushyandover- conditions of the middle taiga subzone. — Russian
grown,andlessfavourableforI.persulcatus.On JournalofEcology37:325–329.
Bobrovskikh,T.K.1989:(KarelianIxodidTicks.)—Ka-
the other hand, these territories with a high an-
relianBranchofUSSRAcademyofScience,Petroza-
thropogenic influence are typical habitat of I.
vodsk.85pp.[InRussian.]
ricinusinRussianKarelia(Luttaetal.1959).
Broker,M.&Gniel,D.2003:Newfocioftick-borneen-
Wesuspectthathumanexploitationandland- cephalitisvirusinEurope:consequencesfortravelers
use structure restrict the distribution and abun- fromabroad.—TravelMedicineandInfectiousDise-
dance of I. persulcatus in the eastern Finnish ase1:181–184.
Bugmyrin,S.V.,Romanova,L.Yu.,Bespyatova,L.A.,
landscape. Forests are intensively managed in
Burenkova,L.A.,Korotkov,Yu.S.,Ieshko,E.P.&
Finland and their structure is quite different in
Karganova,G.G.2008:SimultaneousinfectionofIx-
RussianandFinnishKarelia.Miresandmoistfo- odespersulcatuswithagentsofLymediseaseinthe
restshavepracticallyallbeendrainedinFinland. Karelia. — Transactions of the Karelian Research
Bothintensivemanagementresultingintosparse CentreofRAS13:41–44.
Eisen,L.2008:Climatechangeandtick-bornediseases:A
stands, and well-maintained drainage decrease
researchfieldinneedoflong-termempiricalfieldstu-
favourablehabitatsforI.persulcatus.Sofarithas
dies.—InternationalJournalofMedicalMicrobiolo-
beenfoundatverylowabundanceandlittlecan gy298,Supplement1:12–18.
besaidaboutitspopulationdynamics,although Filippova,N.A.1977:(IxodidTicksofsubfamilyIxodi-
thepopulationintheIlomantsiareaseemstobe nae.)—Nauka,Leningrad.396pp.[InRussian.]
wellestablished.Furtherstudiesareneededcon- Fukunaga,M.,Yabuki,M.,Hamase,A.,Oliver,J.H.Jr.,
Nakao,M.2000:Molecularphylogeneticanalysisof
cerning the life-cycle and hosts, and the abun-
ixodidticksbasedontheribosomalDNAspacer,inter-
danceofI.persulcatusindifferentbiotopes.
naltranscribedspacer2,sequences.—JournalofPa-
rasitology86:38–43
Acknowledgements.TheresearchwassupportedbyFed- Gray,J.S.,Dautel,H.,Estrada-Pen(cid:1),A.,Kahl,O.&Lind-
eralTechnicalProgram(No02.512.11.2171)andRussian gren,E.2009:EffectsofClimateChangeonTickand
FoundationforBasicResearch(No08-04-90720,No09- Tick-BorneDiseasesinEurope.—Interdisciplinary
04-90792-mob_st). We would particularly like to thank PerspectivesonInfectiousDiseases2009,ID593232.
Prof.PhilipD.Harrisforhiscommentsandvaluablecor- 12pp.
rectionsoftheoriginalmanuscript. DrThomasJaenson Jääskeläinen,A.E,Tikkakoski,T.,Uzcátegui,N.Y.,Alek-
andananonymousrefereeprovidedvaluablecommentsto seev,A.N.,Vaheri,A.&Vapalahti,O.2006:Siberian
improvethemanuscript.Logisticsupportwasprovidedby subtype tickborne encephalitis virus, Finland. —
MekrijärviResearchCentreemployees,KareliaRegional EmergingInfectiousDiseases12.[wwwdocument].
Environment Centre/North Karelia Biosphere Reserve, URLhttp://www.cdc.gov/ncidod/EID/vol12no10/06-
Ilomantsi (Research assistant Markku Tietäväinen) and 0320.htm(Sitevisitedon19October,2006).
Friendship Park Research Centre, Kuhmo (Dr. Jari Jääskeläinen,A.E.,Sironen,T.,Murueva,G.B.,Subboti-
Heikkilä).WeareverygratefultoDr.GalinaKarganova, na,N.,Alekseev,A.N.,Castrén,J.,Alitalo,I.,Vaheri,
r.YuryKorotkovandOksanaBelova(M.P.Chumakov A.&Vapalahti,O.2010:Tick-borneencephalitisvirus
Institute of Poliomyelitis and Viral Encephalitides, inticksinFinland,RussianKareliaandBuryatia.—
RAMS,Russia)foridentificationofticksanddetectionof JournalofGeneralVirology91:2706–2712.
TBEvirusandBorrelia.Weappreciatehelpofnumerous Korenberg,E.I.1985:(Limitofareaanditstype).—In:
petanimalownersfromneartheFinnish-Russianborder TaigatickIxodespersulcatusSchulze(Acarina,Ixodi-
provideduswithticksamples.Ourwarmthankstoallper- dae).Morphology,Systematics,Ecology,Medicalim-
sonswhohelpedus. portance.Nauka,Leningrad.Pp.188–193.
Lindgren,E.,Tälleklint,L.&Polfeldt,T.2000:Impactof
climatechangeonthenorthernlatitudelimitandpopu-
lation density of the disease-transmitting European
tickI.ricinus.—EnvironmentalHealthPerspectives
108:119–123.
ENTOMOL.FENNICAVol.22 (cid:127) IxodespersulcatusineasternFinland 273
Lutta, A. S. & Shulman, R. E. 1954. (On the Western Randolph,S.E.2000:Ticksandtick-bornediseasesystem
BoundaryofIxodespersulcatusdistributionintheter- inspaceandfromspace.—AdvancesinParasitology
ritoryofKarelian-FinnishASSR.)—Zoologicheskij 47:217–243.
Zhurnal33:1231–1235.[InRussian.] Sumilo,D.,Bormane,A.,Asokline,L.,Lucenko,I.,Vasi-
Lutta,A.S.,Heysin,E.M.&Shulman,R.E.1959:(Ticks lenko,V.&Randolph,S.2006:Tick-borneencephali-
in KarSSR and methods of control.) — Karel. Fil. tisintheBalticStates:Identifyingriskfactorsinspace
Akad.NaukSSSR,Petrozavodsk.68pp.[InRussian.] andtime.—InternationalJournalofMedicalMicro-
Marconi,R.T.&Garon,C.F.1992:Developmentofpoly- biology296,Supplement1:76–79.
merasechainreactionprimersetsfordiagnosisofLy-
Zeman, P. & Benes, C. 2004: Atick-borne encephalitis
mediseaseandforspecies-specificidentificationof
ceilinginCentralEuropehasmovedupwardsduring
Lymediseaseisolatesby16SrRNAsignaturenucleo-
thelast30years:possibleimpactofglobalwarming?
tideanalysis.—JournalofClinicalMicrobiology30:
— International Journal of Medical Microbiology
2830–2834.
Supplements293,Supplement37:48–54.
Margolis,L.,Esch,G.W.,Holmes,J.C.,Kuris,A.M.&
Schad,G.A.1982:TheuseofecologicaltermsinPara-
sitology.—TheJournalofParasitology68:131–133.
