Catches of bloodsucking blackflies (Diptera: Simuliidae) tell different stories depending on sampling method

2007·0.12 MB·

by  Björn Malmqvist

©EntomologicaFennica.6June2007
Catches of bloodsucking blackflies (Diptera: Simuliidae)
tell different stories depending on sampling method
BjörnMalmqvist,DariusStrasevicius&PeterH.Adler
Malmqvist,B.,Strasevicius,D.&Adler,P.H.2007:Catchesofbloodsucking
blackflies (Diptera: Simuliidae) tell different stories depending on sampling
method.—Entomol.Fennica18:110–116.
To compare different sampling techniques, blackflies were captured along six
Swedishriversin2001and2002,usingtwofundamentallydifferentmethods:(1)
daytime trapping with a vehicle-mounted net, and (2) exposure ofCO-baited
2
traps.Themethodswereselectivelydifferentfordifferentspeciesofblackflies.
Some species were caught relatively more frequently by vehicle trapping and
othersbyCO trapping.Onlyrarelywerespeciescatchesproportionallysimilar
2
betweenthetwomethods.Wesuggestthatthedifferentcatchsuccessreflectsdif-
ferencesinhost-searchingbehaviourinthespeciespresentandthatthesampling
methodsarecomplementary.
Björn Malmqvist, Department of Ecology and Environmental Science, Umeå
University,SE-90187Umeå,Sweden;E-mail:[email protected]
DariusStrasevicius,DepartmentofEcologyandEnvironmentalScience,Umeå
University,SE-90187Umeå,Sweden;E-mail:[email protected]
PeterH.Adler,ClemsonUniversity,DepartmentofEntomology,Soils,andPlant
Sciences, 114 Long Hall, Clemson SC 29634, USA; E-mail: padler@clem-
son.edu
Received21March2006,accepted22August2006
1.Introduction
ofactivitiesfrommating,sugarfeeding,hostlo-
cation,bloodfeeding,eggmaturation,tothere-
Blackflies are haematophagous parasites and turntoflowingwaterforoviposition,sometimes
vectorsofapicomplexans,bacteria,filarialnema- repeated in multiple cycles (Sutcliffe 1986).
todes,flagellates,andviruses(Adleretal.2004). Hosts are located by means of olfactory and, at
Apart from their role as vectors of the filarial closer range, visual and possibly thermal cues
agents that cause onchocerciasis (river blind- (Sutcliffe 1986). To the hosts, blackfly attacks
ness), a widespread and serious disease in hu- causedistress,bloodloss,andparasitetransmis-
mans(Crosskey1990),muchoftheircapacityas sion,andduringmassattacks,anaphylacticshock
vectorsispoorlyknown.Femalesofmostspecies andothermaliciouseffects(Crosskey1990).
ofblackfliesrequirebloodforeggdevelopment. Quantitative methods are crucial to under-
Theirhostsareendothermic,andblackflyspecies standingtheecologicalrolesofblackfliesinthe
are either mammalophilic or ornithophilic terrestriallandscapeandtoimprovingcontrolof
(Crosskey1990,Malmqvistetal.2004b).Black- deleteriousspecies.However,nouniversalsam-
flies,afteremergence,showanorderedsequence plingmethodexists,andquantifyingthemisei-
ENTOMOL.FENNICAVol.18 (cid:127) Comparingsamplingmethodsforblackflies 111
therdonebymakingdirectcountsonhosts,e.g. Table1.Descriptionofriversites.Riversarearranged
exposedhumans,domesticanimals(e.g.Ander- fromsouthtonorth.Dammingandassociatedhabitat
son&Yee1995),orcaptivewildanimals(Ander- destructionisextensiveinregulatedrivers(‘R’),
whereasfree-flowingrivers(‘F’)haveintactlarvalhab-
son&DeFoliart1961,Ojanenetal.2004).They
itats.Samplingwascarriedoutonthesamedatesin
are also caught overhead with standardised net
riverpairs.
sweeps(Grayetal.1996)orattractedusingcar-
bondioxidebaitedtrapsthatcanbespikedwith
Rivers Coordinates Regulation Elevation
additionalattractantsormodelledtothelikeness
(ma.s.l.)
ofapotentialhost(Helleetal.1992,Martinetal.
1994,Andersonetal.2001).Othermethodsare
14–15.and26–27.VI.2001,1–2.VII.2002
passive and involve the collection of flying in- Ume 64o03’16”N R 179
sects with vehicle-mounted nets (e.g. Davies & 19o36’29”E
Roberts1980)orsuctiontrapswithoutattractants Vindel 64°00’54”N F 155
19°56’14”E
(Choeetal.1984).
Ourpreviousworkonblackfliesinnorthern
19–20.VI.and2–3.VII.2001,11–12.VII.2002
Swedenhasdemonstratedlargeinterspecificdif- Skellefte 65°06’25”N R 247
ferences in breeding habitats (Malmqvist et al. 19°25’45”E
1999)andhostchoice(Malmqvistetal.2004b). Pite 65°57’02”N F 270
19°33’49”E
Forinstance,thelarvaeofcertainspeciesdevelop
uniquelyinlargeriversoriginatinginthemoun-
21–22.VI.and4–5.VII.2001,7–8.VIII.2002
tain region in the borderland between Norway Lule 65°44’17”N(2001) R 54
andSweden,whereasthoseofotherspeciesare 24°43’32”E
confinedtosmalloreventinystreams,depending 66°04’42”N(2002) 19
20°56’36”E
on morphological constraints in the head fans
Kalix 66°37’27”N(2001) F 117
usedforcapturingfoodparticlesfromthewater
22°46’15”E
current(Zhang&Malmqvist1996).Femalesdis- 65°59’51”N(2002) 47
persing from large rivers may travel relatively 22°56’04”E
long distances in search ofhosts (e.g. Garms &
Walsh 1987). To achieve a distribution corre-
sponding to species developing in widely sepa-
rated,largerivers,blood-seekingfemalesemerg- catedinthetaiga,withcatchmentsprimarilycov-
ingfromlocalstreamnetworkscanbeexpected eredbyNorwegianspruceandScotspineforests,
to show movement patterns that are compara- althoughalsoincludingareaswithfarmland,mire
tively more spatially restricted. We have made and clear-cut forest in the investigation area.
considerable efforts to sample flying blackflies, Trappingtookplaceabout1kmfromthenearest
usingvehicle-mountednets,butpreliminarytest- largerivers. Theriverssampled representpairs,
ing of attractant traps suggested that these nets whereby one river in each pair is regulated for
mightgiveadifferentpictureoftheblackflyas- hydropowerpurposesandtheotherisfreeflow-
semblagespresent. Hereweexamine, concomi- ing (Table 1). The comparison with respect to
tantly using vehicle-mounted traps and CO- riverregulationwillbepresentedelsewhere.
2
baitedtraps,towhatextentthehuntingmode,as Ateachsite,weusednineCO-baitedtrapsof
2
expressed in flying and attraction, respectively, CDCtype(CentersforDiseaseControlandPre-
differswithrespecttospeciesandhosttype. vention, USA; manufacturer: Machine Works,
TomsRiver,NewJersey)modifiedbyreplacing
the traditional live-catch mosquito fabric cage
2.Materialandmethods
unitbyafunnel-shapedfine-meshnetwithatube
containing70%ethanolattachedtoitsbaseand
The investigation was performed at sites along lightbulbsremoved.Eachtrapwassuppliedwith
sixofthemainriversinnorthernSwedeninthe ca1kgofdryiceasasourceofcarbondioxide
summersof2001and2002.Thestudyareaislo- fastenedunderthetopofthetrap.Thedryicewas
112 Malmqvistetal. (cid:127) ENTOMOL.FENNICAVol.18
Table2.Meanproportion(acrossrivers)ofspeciesrepresentationinCO andvehicletraps,respectively,inthe
2
2001dataset(twoseasonscombined).Multiplespeciesnamesareindicatedincaseswherespeciescouldnot
beseparated.
Species Primary Breeding Riverswith Proportionofcatch
host1 habitat2 species
recorded(N) CO trap Vehicletrap
2
Prosimuliumhirtipes M S-L 1 0 0.016
Stegopternatrigonium M S 2 0.010 0
Metacnephialyra B L 6 0.165 0.527
M.saileri B V 2 <0.001 0.014
Simuliumannulus B L 3 <0.001 0.170
S.bicorne,carpathicum, B S 4 0.007 0.010
cryophilum,urbanum,
vernum
S.equinum M M 2 0.001 0.040
S.erythrocephalum M M-L 1 0.053 0.120
S.intermedium M V 1 0.004 0
S.lundstromi B S 3 0.040 0.003
S.murmanum M L 4 0.061 0.067
S.ornatum M V 5 0.047 0.001
S.pusillum,subpusillum M L 3 0.020 0.010
S.rostratum M M-L 4 0.023 0
S.rubtzovi,curvistylus, M M-L 6 0.028 0.010
morsitans
S.silvestre,curvans B S 5 0.179 0.006
S.truncatum,paramorsitans M M-L 6 0.348 0.153
posticatum
S.transiens B L 2 0.033 0.003
S.tuberosum,vulgare M S-L 6 0.140 0.086
S.usovae/rendalense B S 1 0.001 0
1B=Birds;M=Mammals.
2L=Largerivers;M=Medium-sizedrivers;S=Streams;V=Variablebreedinghabitats.
wrappedinseverallayersofnewspapersandthe fromAdleretal.(2004).Onlyfemaleswerecon-
release rate was ca 400 ml CO/min. The traps sidered;however,gravidandengorgedindividu-
2
weredistributedalongadistanceof3–5kmand alswereexcluded,thusfocussingonhost-seek-
locatedca1m(range0.5–1.5)abovetheground, ing blackflies. Females of certain species are
i.e.operatingapproximatelyatthesameheightas presentlyinseparable(seeTable2).Onlythema-
the vehicle trap. Exposure time was about 20 terial from 2001 was identified to the species
hours.Allsamplingwascarriedoutundergood level.
weather conditions, i.e. at temperatures (cid:1)12oC, AnalyticalmethodsincludedChi-squaretests
withnooronlyweakwindsonprecipitation-free thatwereusedtoassessprobabilityvaluesforthe
days. relationshipbetweentwodichotomousvariables,
Acarwithanetmountedontheroof(Malm- suchastheefficiencyoftwosamplingmethodsin
qvistetal.2004b)wasoperatedtwiceat40kmh–1 capturinginsectsderivedfromtwohabitattypes
over the same 3–5 km stretch along which the (largeandsmallrivers),hostcategories(birdsand
CO trapsweredeployed.Samplingwascarried mammals) and phylogenetic groups (Simulium
2
outapproximatelybetweennoonand10a.m.the vs.non-Simuliumgenera,i.e.Prosimulium,Me-
next day. Samples were labelled and stored in tacnephia, and Stegopterna). Pearson bivariate
70%ethanoluntilidentificationinthelaboratory. correlationwasusedtorelatecatchesbetweenthe
Species were identified using a key modified twosamplingmethodsinthetwoyears.
ENTOMOL.FENNICAVol.18 (cid:127) Comparingsamplingmethodsforblackflies 113
Fig.1.Proportionsof
speciesrelativetoentire
blackflycatches,using
CO andvehicletrap-
2
ping.Panela)indicates
equalsuccessforthe
twomethods,b)that
CO trappingwasmore
2
efficientthanvehicle
trapping,c)thatvehicle
trappingwasmoreeffi-
cientthanCO,andd)
2
thattherewasanunex-
plainedpattern.
3.Results
thesingleseason(July/August)of2002(Table1).
Thelargestnumbercaughtinasingletrap,10,773
CO trapsalmostexclusivelycollectedfemalesof blackflyfemales,wasrecordedonthePiteRiver
2
blackflies, mosquitoes (Culicidae) and biting 11–12.VII.2002. Vehicletrapping yielded much
midges(Ceratopogonidae).Thetrapsyieldedin lower numbers: 196 and 450, respectively, in
total 8,471 and 6,507 blackflies (all females) in 2001,and227in2002,andthesenumbersrepre-
JuneandJuly 2001,respectively,and25,913in sentamixtureofmalesandfemales(Table2).Fe-
114 Malmqvistetal. (cid:127) ENTOMOL.FENNICAVol.18
malesmadeup,onaverage,76.7and77.6%ofthe square = 23.69; p < 0.001). CO trapping also
2
vehicle-trapcatchesinthefirstandsecondround captured relatively more females of mammalo-
in2001,respectively,butonly46.3%inthe2002 philic species (60%) than did vehicle trapping
sampling. Small numbers of gravid (5) or (53%)(Chi-square=12.68;p<0.001).Finally,
engorged (1) females were captured but not in- vehicle trapping (45% of catch) was more effi-
cludedinanalyses. cient relative to CO trapping (35% of catch)
2
Therelativecatchstatisticspertainingtothe (Chi-square=23.41;p<0.001)incatchingnon-
two methods of sampling showed four types of Simuliumfemales,suggestingaphylogeneticef-
relationships. First, as in Simulium murmanum, fectofthesamplingmethodaswell.
theproportionalrepresentationwasnearlyidenti- Comparing catches, using the two methods,
cal for the two methods (Fig. 1a). Second, the resulted in correlations that varied in strength
CO traps were highly efficient for S. sil- (July 2001 data: r = 0.638, p>0.05; July 2001
2
vestre/curvans,whereasvehicletrappingwasnot data:r=0.950,p<0.005;2002data:r=0.589,p
(Fig.1b).Adecreasingtrendtowardthenorthis >0.05)(alldf=4).
alsoevidentinthisblackflygroup.Thirdly,vehi-
cle trapping was relatively more efficient than
4.Discussion
CO trappingforMetacnephialyra(Fig.1c),and
2
lastly, in some species, there was inconsistent
variation; S. truncatum/paramorsitans/posti- Thevariabilityincapturesuccessamongdiffer-
catum,forexample,showedahighvehicle-trap ent species is intriguing. Our observations sug-
catch in one instance (Skellefte River) but was, gestthatblackflyfemalesuseatleasttwosearch
despite presence in CO traps, rare or absent in modes for detecting a host: (1) sit-and-wait,
2
vehicle-trapcatchesonallotherriversites(Fig. wherebytheflyprobablywaitsinactivelyinthe
1d). Examining additional species (Table 2) vegetationforacuetobeginhostpursuit,which
yieldedseveralotherexampleswhereCO trap- couldincludeCO oravisualstimulus(e.g.col-
2 2
ping appeared more efficient than vehicle trap- our,shape),or(2)activesearch,againprobably
ping(S.ornatum,S.lundstromi,S.rostratum,and involving CO, although visual cues cannot be
2
S.transiens)orviceversa(Metacnephiasalieri, ruledout.Thesefindingssupportthecontention
S.annulus,S.erythrocephalum,andProsimulium thatblackflieseitherroaminsearchofhostsorsit
hirtipes). Variable success was found in the S. andwaituntilahostcomesnearenoughtobede-
venustum group, S. vernum group, S. pusillum/ tected(Simmons1985).
subpusillum,andinS.equinum. However, CO-baited traps sample females
2
Slightlymorespecies(19)werecapturedby engagedonlyinhostseeking,whichrepresentsa
CO trappingthanbyvehicletrapping(16).This subsetofthebehavioursoffemalescollectedby
2
smalldifferenceremainedwhenhosttype(birds vehicle traps. Females taken in vehicle traps
vs. mammals) was considered (CO: 8 ornitho- could be engaged not only in host seeking, but
2
philicspecies, 11mammalophilicspecies;vehi- alsoindispersalflights,searchesforsugarmeals
cle: 7 ornithophilic species, 9 mammalophilic and resting sites, and mating encounters with
species; Chi-square = 0.01; p > 0.05). Neither males. The proportions of females in the two
were non-Simulium species captured more fre- typesoftraps,therefore,mightreflectdifferences
quently by any of the methods (Chi-square = inthefrequenciesofthevariousbehavioursatthe
0.05;p>0.05).River-sizeoriginalsodidnotmat- timesofcollection.
ter(Chi-square=0.28;p>0.05). Discrepancies between the outcomes of the
Incontrasttotheanalysesofspeciesnumbers, differentmethodsalsomightindicatethatspecies
thoseconsideringabundancesshowedstrongef- ofblackfliesdifferindiurnalactivity.Somespe-
fectsofsamplingmethod.Theanalysisoflarge- cies would be active at the time when vehicle
rivervs.small-streamspeciesdemonstratedthat trappingisperformed(afternoon),whichwould
CO trappingcapturedrelativelyhighernumbers yield catches using both CO and vehicle-trap-
2 2
ofsmall-streamderived females(10% ofcatch) ping methods, whereas such species that have
than did vehicle trapping (3% of catch) (Chi- early-morning or late-evening activity peaks
ENTOMOL.FENNICAVol.18 (cid:127) Comparingsamplingmethodsforblackflies 115
wouldavoidbeingcaughtandhenceproducerel- Ourstudyshowsthatrelyingonasinglesam-
atively lower vehicle-trapping catches. More- plingapproachmightcarryrisks.Inouropinion,
over,highervehicle-trappingsuccessrelativeto therearearraysofdifferentblackflyassemblages
CO trapping would suggest that the blackflies invadingtheterrestriallandscape,dependingon
2
relymoreonvisualthanchemicalcues.However, the regional availability and quality of stream
our night-time vehicle trapping has generally habitats, which together with thefemalebehav-
showed little activity. Instead, females tend to iour(widelysearchingorsit-and-wait)ofdiffer-
show peak activity in late morning (10.30) and entspecies,governtheirdistributionacrossthese
earlynight(19.30),withfewfemalesbeingactive landscapes. Toassesspopulationswithhighac-
between21.00and09.00(Strasevicius&Malm- curacyisprobablynotpossiblewiththemethods
qvist,unpubl.),andthenmainlythoseofSimuli- presently available. However, vehicle-mounted
um tuberosum/vulgare, a rodent specialist traps should provide a reasonably standardised
(Malmqvistetal. 2004b).Lowcapturesuccess, measurebutwithanunder-representationofcer-
usingvehicletrapping,couldpotentiallyalsobe tain species, whereas if attractant traps are the
thecaseiffemalesflyhighabovetheground,as solemethodused,ahighyieldpereffortofblack-
reportedfortheS.aureumspeciescomplex(2–8 flieswouldbeobtainedbutagainwithaskewed
maboveground)(Bennett1960),orverycloseto speciesrepresentation.
theground,asinS.rugglesi(Smith1966). Aparticularadvantageofvehicletrappingis
The difficulties in separating the females in thatmaleswillbecaught,whichfavourscorrect
certaingroupscouldhavecontributedtosomeof identification,evenifnotinallcasestothespe-
thevariationinthecatchesifsuchgroupscontain cieslevel.AlthoughCO trappingprovideshigh
2
specieswithcontrastinghuntingmodes.Forex- numbersofblackflies,ithasthedrawbacksofan
ample, females of the indistinguishable species absenceofmalesandtheneedfortwovisitsifde-
Simuliumtruncatum,S.posticatum,andS.para- ployedovernight.CO trapswouldalsonotcap-
2
morsitansmighthavedifferentdielactivitypat- ture obligately autogenous (i.e. non-blood-
terns(e.g.withoneortwospeciesnotflyingin sucking) species, which represent some ten per
theafternoon)anddifferentrepresentationacross centofthespeciesinnorthernSweden(Adleret
thestudyregion,whichpotentiallycouldresultin al.1998).
patternsgeneratinginconsistenciesbetweenCO Blackflies are highly important members of
2
andvehicletrapping(cf.Fig.1C). theborealecosystem,withmanylikelybutunex-
ThehigherspeciesnumberobservedforCO ploredinfluencesintheaquaticaswellasinthe
2
trappingislikelytobearesultofthehighernum- terrestrial environments (Adler & Malmqvist
berofindividualscapturedbecausespeciesrich- 2004, Malmqvist et al. 2004a). This contention
nessisdependentonnumbers(Gotelli&Colwell stillneedsmorespecificationstobetterdetermine
2001).Wefoundnoselectivitybyeithermethod theirvariousimpacts.Forsomeofthemostim-
onhowmanyspeciesofbirdvs.mammalspecial- portantimpacts,suchasbitinganddiseasetrans-
istswerecaptured.Likewise,therewasnosuch mission, efficient methods of quantification are
selectivity concerning the main phylogenetic required. On the aspect of host-location behav-
groups, i.e. Simulium vs. non-Simulium genera, iourweneedbetterinformationonflightheight
orriverorigin.Incontrast,theanalysesofabun- and diel activity. To our knowledge, there is no
dancesindicatedthatsmall-streamspecieswere suchinformationforEuropeanspecies.Otherfu-
represented in larger proportion in the CO trap tureneedsincludetheabilitytotracktheoriginof
2
catches,suggestingthatthese,inaccordancewith capturedspeciesandtomaptheirsubsequentdis-
ourpredictions,betterreflectedlocallyproduced persal patterns, which would enable effective
blackflies.Althoughmany small-streamspecies controlifdeemednecessary.Westressthatinall
are ornithophilic, this tendency did not show in this work, blackflies must be recognized as a
the catches, where mammalophilic species still composite group of insects showing multiple
werebetterrepresentedinCO trapsthaninvehi- strategies with respect to habitats, behavioural
2
cletraps,whichwaspartlyduetotheabundant, patterns, and hosts, for which study methods
large-riverdominantspeciesMetacnephialyra. mightvarydependingonwhichspeciesisinfo-
116 Malmqvistetal. (cid:127) ENTOMOL.FENNICAVol.18
cus.Moregeneralstudiesshouldpreferablyem- Merritt,R.W.(eds.),Blackflies.Ecology,population
ployacombinationofsamplingtechniques. management and annotated world list: 201–214.
PennsylvaniaStateUniversity,UniversityPark.
Gotelli, N. J., &Colwell. R. K. 2001:Quantifyingbio-
Acknowledgements. We thank Karl Malmqvist for his
diversity:proceduresandpitfallsinthemeasurement
carefulassistancewiththeprocessingoftheblackflysam-
andcomparisonofspeciesrichness.—Ecol.Lett.4:
ples.
379–391.
Gray,E.W.,Adler,P.H.&Noblet,R.1996:Economicim-
pact of black flies (Diptera: Simuliidae) in South
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