Differences in mosquito (Diptera: Culicidae) biodiversity across varying climates and land-use categories in Eastern Spain

2011·0.24 MB·

by  Rubén Bueno Marí

©EntomologicaFennica.20December2011
Differences in mosquito (Diptera: Culicidae) biodiversity
across varying climates and land-use categories
in Eastern Spain
RubénBuenoMarí&RicardoJiménez-Peydró
BuenoMarí,R.&Jiménez-Peydró,R.2011:Differencesinmosquito(Diptera:
Culicidae)biodiversityacrossvaryingclimatesandland-usecategoriesinEast-
ernSpain.—Entomol.Fennica22:190–198.
Intensivelarvalsamplingsofmosquitoes(Diptera:Culicidae)werecarriedout
between2005and2008inseveralbiotopeslocatedinavaryingclimateregionin
EasternSpain.Thebiodiversitywasanalyzedanddividedintoalpha,betaand
gamma components with the aim of comparing the mosquito biodiversity ac-
cordingtothedifferentstructureofthelandscapeduetotheincidenceofclimatic
andanthropicpatterns.LikewisethesynanthropicindexofNuortevawascalcu-
latedforeachspecies.Atotalof11,279mosquitoesbelongingto29specieswas
collectedandidentified.Mosquitobiodiversityishigherinthewettestandnon-
anthropizedareas.Usingaclusteranalysis,allthisinformationwasalsousedto
groupthedifferentregionsstudieddependingonitsmosquitofauna.Moreover
there-emergenceofantroponosis,likemalaria,seemsunlikelygiventhelowval-
uesofthesynanthropicindexfortheanophelinescaptured.
R.BuenoMarí&R.Jiménez-Peydró,EntomologyandPestControlLaboratory,
CavanillesInstituteforBiodiversityandEvolutionaryBiology,UniversityofVa-
lencia,OfficialPost22085,46071Valencia,Spain;E-mailaddressofthecorre-
spondingauthor:[email protected]
Received29July2010,accepted10January2011
1.Introduction tobeaveryusefultool(Whittaker1972).Theal-
phadiversity(a)isthespecificrichnessofacom-
Mosquitoes,likeotherorganismsshowaspatial munitythatweconsiderhomogeneous.Thebeta
variationinrelationtoseveralfactorssuchasen- diversity(b)referstothedegreeofreplacementin
vironmental heterogeneity or habitat and host thespecificcompositionbetweendifferentcom-
preferences (Zhong et al. 2003). Understanding munitiesofalandscape.Andlastlywecandefine
thelinksbetweenhabitats,environmentalfactors thegammadiversity(g)asthespecificrichnessof
andoccurrenceofimmaturemosquitoes(Dipte- thegroupedcommunitiesthatformalandscape,
ra:Culicidae)isessentialforanefficientapplica- resulting from both alpha and beta diversities.
tionofmosquitocontrolmethods(PemolaDevi Thismethodofbiodiversityanalysisisusefulnot
&Jauhari2007). onlytoexploretheclimatic,physicalorbiologi-
Tocomparemosquitodiversity accordingto cal influences on biodiversity, but also to study
thestructureofthelandscape,thedivisionofthe the effects of human pressure on biodiversity
alpha,betaandgammacomponentsisconsidered (Halffter 1998, Moreno 2001). Although it is a
ENTOMOL.FENNICAVol.22 (cid:127) MosquitobiodiversityinSpain 191
methodmuchusedtoestimatethebiodiversityof
manyinsects,thereislittleinformationaboutits
useinmosquitostudies.
Our aim was to investigate the changes in
mosquitobiodiversityduetoenvironmental(cli-
maticandanthropic)factorsinEasternSpain.
2.Materialandmethods
2.1.Studyarea
In Spain studies of mosquito biodiversity are
scantandoutdated,mostlyconcernedwithtimes
whenmalariawasendemic(BuenoMarí&Jimé-
nezPeydró2008).Atotalof64mosquitospecies
havebeen reported in Spain, butsomeofthem,
like Anopheles labranchiae Falleroni or Aedes
aegypti (Linnaeus), are currently considered
eradicated or absent (Bueno Marí & Jiménez
Peydró2011).Consequently,recordsofonly54
speciesareconsideredvalidatpresent(Eritjaet
al.2000).ForourstudyweselectedtheValencian
AutonomousRegion(Fig.1)duetoitsheteroge-
neity of climate. In this Mediterranean area we
differentiatedbetweenfiveregionsorsectorsac-
cordingtotheirpatternsoftemperatureandpre-
cipitation(GVA,2003):
– Setabensesector(S):Characterizedbyatypi-
cal Mediterranean climate, with low oscilla-
tionsofmeantemperature((cid:1)13ºC)between
winterandsummer,andpeakprecipitationsin
autumn. Fig.1.Situationofthestudyareawiththefivecoro-
– Valenciano-Tarraconense sector (VT): Simi- logicalsectors.AM:Alicantino-Murcianosector,MN:
larly represents a typical Mediterranean cli- Manchegosector,MS:Maestracensesector,S:Seta-
bensesectorandVT:Valenciano-Tarraconensesec-
mate,butwithhigherhomogeneityinthespa-
tor.
tialdistributionofprecipitationsthanS.
– Maestracensesector(MS):Characterizedby
aMediterranean climatestrongly influenced ing an intermediate climate between typical
byaContinentalclimate.Therearewidetem- MediterraneanandDeserticclimate.
peratureoscillations((cid:1)18ºC)betweenwinter
and summer, and peak precipitations during Tostudy theeffectsofhumanpressureonmos-
spring.Moreoveritisthecoldestandwettest quitobiodiversity,eachlarvalbiotopewastypi-
regionofthestudyarea. fiedaccordingtoitsanthropizationdegreeasfol-
– Manchegosector(MN):Despiteitalsohasa lows:
Continentalinfluence,itcanbeeasilydistin-
guishedfromMSduetoitslowertopography. – Urban biotope or high anthropization area:
– Alicantino-Murciano sector (AM): Charac- situated in permanent human settlements or
terizedbyadryMediterraneanclimate,show- surroundings.
192 BuenoMarí&Jiménez-Peydró (cid:127) ENTOMOL.FENNICAVol.22
Table1.Indicesandformulaeusedtoestimatealpha,betaandgammadiversities.
Estimation Indices Formulae#
Alphadiversity Margalef(D ) D =S–1/lnN
Simpson(l)Mg lM=gSp²
Shannon-Wiener(H’) H’=–Si p lnp
i i
EquityofPielou(J’) J’=H’/H’max=H’/lnS
Betadiversity Jaccard(I) I =c/a+b–c
J J
Whittaker(b )/(b)* b =S/a–1/(b)*=1–d
w w
Gammadiversity Gamma(g) g=a×b×e
#S:speciesrichness,N:totalnumberofindividuals,p:frequencyofspeciesi,a:numberofspeciespresentinsiteA,b:number
i
ofspeciespresentinsiteB,c:numberofspeciespresentinbothsiteAandB,d:averagenumberofsamplesoccupiedbyone
species,a:averagenumberofspeciesinacommunity,e:totalnumberofcommunitiesstudied.
*ModificationproposedbySchluter&Ricklefs(1993)tocalculatetheaverageb.
– Ruralbiotopeormediumanthropizationarea: 2.2.Samplingmethods
placedintemporaryhumansettlements(live-
stockoragriculturalareas)orsurroundings. Usingsimplerandomsampling,wesampledlar-
– Wildbiotopeorlowanthropizationarea:po- val forms frommultiple sites within each study
sitionedinnaturalareaswithoutapparenthu- sector using thedipping method (Service1993)
manactionsaroundit. for8monthsayear(March–October)2005–2008
(4 years). Data were collected fromall identifi-
Thishabitatcharacterizationallowedustoapply ableaquaticenvironmentsacross23,260km2of
the Nuorteva synanthropic index (Nuorteva thestudyarea.
1963) to evaluate the domiciliation degree of
eachspeciescaught:
2.3.Dataanalysis
(S)=(2a+b –2c)/2 (1),
i i i
Mosquitoeswereidentifiedaccordingtothekeys
wherea,bandcrepresentsthepercentageofcap- ofEncinasGrandes(1982),Darsie&Saminadou
turesoftheispeciesinurban,ruralandwildareas Voyadjoglou(1997)andSchaffneretal.(2001).
respectively.Thevaluesoftheindexrangefrom ThenomenclaturalcriteriawerebasedonReinert
+100 (highest degree of domiciliation) to –100 (2000).Datawereanalyzedstatisticallyusingthe
(lowest degree of domiciliation). The domicili- Biodiversity.Rpackage(Kindt&Coe2005).For
ationdegreereferstothepreferenceofdifferent eachenvironmentwecalculatedseveralbiodiver-
speciestobreedand/ordevelopinanthropicenvi- sityindices(Table1).Tocalculatetheecological
ronments.Fromthepointofviewofdiseasevec- distancebetweendifferentenvironments,wede-
tors, the domiciliation degree is postulated as a velopedaclusteranalysisandaprincipalcompo-
veryimportantevolutionaryissuetoexplainthe nentanalysis(PCA),bothbasedonJaccarddis-
emergenceandendemismofhumandiseasesthat tance.Thecopheneticcorrelationwasalsocalcu-
previously wereexclusivezoonoses.TheNuor- latedforeachJaccardclusterwiththeaimofcal-
tevaindexwasinitiallyproposedforthestudyof culatingthedegreeofreliabilityoftheclassifica-
synanthropic flies, but has also been used with tion system used (R Development Core Team
culicidmosquitoes(Forattinietal.1993).Given 2005).
the fact that human settlements are frequently
linkedtotheworseningofwaterquality,theuse
ofthisindexcouldbeinteresting,notonlytoeval- 3.Results
uate the anthropophilic degree of each species,
butalsotoelucidatetheirtolerancelevelsofwater In the larval captures of 679 different sampling
eutrophication. points,atotalof11,279mosquitoesbelongingto
ENTOMOL.FENNICAVol.22 (cid:127) MosquitobiodiversityinSpain 193
Table2.–A.Numberspecimensofspeciesinfivegenusescapturedindifferentenvironments,andsynanthropic
indices(SI).–B.Estimatorsofalphabiodiversity.Fortheabbreviationsofcorologicalsectors,seeFig.1.
Corologicalsectors Areas
AM MN MS S VT Urban Rural Wild SI
A.No.ofspecimensandSI
Aedes
A.vexans 0 0 89 0 8 0 85 12 6.5
A.vittatus 0 0 0 1 50 0 5 46 –79
Anopheles
A.algeriensis 16 9 0 20 0 0 33 12 12.5
A.atroparvus 0 4 61 0 26 0 25 66 –56.5
A.claviger 0 7 25 2 0 0 2 32 –79
A.maculipennis 0 0 61 0 13 0 9 65 –67
A.marteri 0 0 3 0 0 0 0 3 –50
A.petragnani 0 7 147 187 145 0 88 398 –61
A.plumbeus 0 0 171 0 0 0 171 0 50
Culiseta
C.annulata 0 0 4 2 35 0 18 23 –37
C.longiareolata 239 102 693 788 797 411 1,379 829 13
C.subochrea 1 2 10 8 108 0 60 69 –35.5
Culex
C.hortensis 18 44 455 75 111 0 207 496 –58.5
C.impudicus 0 7 30 22 26 0 20 65 –64
C.laticinctus 1 47 205 177 482 158 451 303 –12.5
C.mimeticus 7 15 74 123 123 0 111 231 –53.5
C.modestus 2 0 5 122 70 0 164 35 17
C.pipiens 587 61 346 1,395 1,129 729 2,011 778 21
C.territans 10 27 197 133 121 0 158 330 –51
C.theileri 26 2 0 6 42 0 50 26 0.5
Ochlerotatus
O.berlandi 0 0 42 0 0 0 42 0 50
O.caspius 312 12 4 103 207 69 364 205 21
O.detritus 60 0 0 24 77 13 90 58 2
O.echinus 0 0 45 89 11 0 119 26 0.5
O.geniculatus 0 0 4 49 9 0 48 14 6.5
O.gilcolladoi 0 0 2 13 0 0 0 15 –50
O.pulcritarsis 0 0 14 0 0 0 14 0 50
Orthopodomyia
O.pulchripalpis 0 0 10 0 0 0 10 0 50
Uranotaenia
U.unguiculata 0 0 0 0 28 0 17 11 0.5
B.Alphadiversity
Abundance 1,279 346 2,687 3,339 3,618 1,380 5,751 4,148
Specificrichness(S) 12 14 24 20 21 5 27 25
Margalefindex(D ) 1.54 2.22 2.91 2.34 2.44 0.55 3 2.88
Mg
Simpsonindex(l) 0.69 0.84 0.87 0.76 0.83 0.62 0.8 0.88
Shannon-Wienerindex(H’) 1.44 2.09 2.37 1.9 2.19 1.14 2.17 2.46
EquityofPielouindex(J’) 0.58 0.79 0.75 0.63 0.72 0.36 0.66 0.89
29specieswereidentified(Table2).Thecompar- sector;itfeaturesbodiesofwateringreaterquan-
isonofabiodiversityindicesrevealsthattheMS tityandtypologicaldiversity.
sectoristhemostdiverse(D =2.91,l=0.87, Concerning the degree of environmental
Mg
H’=2.37)andtheAMtheleastdiverse(D = anthropization, we suggest that human settle-
Mg
1.54,l=0.69,H’=1.44).MSsectoristhewettest mentsnegativelyinfluencemosquitobiodiversi-
194 BuenoMarí&Jiménez-Peydró (cid:127) ENTOMOL.FENNICAVol.22
Table3.Estimatorsofbetabiodiversityforeachcommunitycomparison.Fortheabbreviationsofcorologicalsec-
tors,seeFig.1.Theaveragebforcomparisonsofcorologicalsectorsis0.32andthatforareasis0.51.
Comparisons Jaccard(I) Jaccarddistance(Cluster) Whittaker(b )
J w
Corologicalsectors
AM-MN 0.63 0.84 1.33
AM-MS 0.33 0.81 1.47
AM-S 0.6 0.72 1.33
AM-VT 0.5 0.69 1.42
MN-MS 0.46 0.88 1.39
MN-S 0.62 0.9 1.31
MN-VT 0.52 0.9 1.39
MS-S 0.57 0.6 1.29
MS-VT 0.61 0.6 1.06
S-VT 0.71 0.3 1.07
Areas
Urban-Wild 0.2 0.6 1.79
Urban-Rural 0.19 0.7 1.8
Wild-Rural 0.8 0.5 1.16
ty: urban biotopes (D = 0.55, l = 0.62, H’ =
Mg
1.14),ruralbiotopes(D =3,l=0.80,H’=2.17)
Mg
and wild biotopes (D = 2.88, l = 0.88, H’ =
Mg
2.46). With the exception of tree hole breeding
mosquitoes,associatedmostlywithforestdistri-
bution,thesynanthropicindexofNuortevaindi-
cates that anophelines, excepting Anopheles
algeriensis Theobald (S = 12.5), show low
domiciliation degree, whereas Culex pipiens
Linnaeus,Ochlerotatuscaspius(Pallas),Culiseta
longiareolata (Macquart) and Culex modestus
Ficalbiarespeciesbetterassociatedwithhabitats
which present surrounding human settlements.
Furthermore,otherspecies,likeCulexhortensis
Ficalbi(S=–58.5),CuleximpudicusFicalbi(S=
–64),CulexterritansWalker(S=–55)andCulex
mimeticusNoè(S=–53.5),exhibitastrongpref-
erenceforwildenvironments.
Theanalysisofbbiodiversity(Table3)indi-
catesthatSandVTaretheclosestsectorsintheir
specificcompositions(I =0.71),thespecificre-
J
placementamongthembeingconsequentlyvery
low(b =1.07).Itisimportanttorememberthat
w
both sectors are the only representatives of the
typicalMediterraneanclimateinourstudyarea.
With regard to the degree of environmental
anthropization,theruralandwildbiotopesarethe
Fig.2.ClusteranalysisusingJaccarddistance.–a.
closest(I =0.80),andconsequentlyalsoshowa
Corologicalsectors,copheneticcorrelation(r)=0.98.
lowspeciJficreplacement(b =1.16). –b.Degreeofanthropization,(r)=0.88.Forcthe
w c
The dendrograms elaborated from Jaccard abbreviationsofcorologicalsectors,seeFig.1.
ENTOMOL.FENNICAVol.22 (cid:127) MosquitobiodiversityinSpain 195
Fig.3.PrincipalcomponentanalysisbasedonJaccarddistance.Fortheabbreviationsof
corologicalsectors,seeFig.1.PCvalues(PC1,PC2)ofspecieswithintheboxes:Upperbox:
Aedesvittatus(0.2,0.2),Anophelesalgeriensis(–2.9,0.5),A.atroparvus(–3.2,–3.1),A.clavi-
ger(–2.7,–0.9),A.maculipennis(–3.1,–3.1),A.marteri(–0.2,–0.2),Culisetaannulata(–0.1,
–0.2),C.subochrea(–0.2,–0.1),Culeximpudicus(–0.2,–3.1),C.mimeticus(0.2,–2.8),C.mo-
destus(0.5,0.4),C.theileri(–0.1,–0.2),Ochlerotatusberlandi(–2.9,–2.6),O.echinus(–0.2,
–1.1),O.geniculatus(–0.2,–0.8),O.gilcolladoi(–0.1,–0.7),O.pulcritarsis(–0.2,–0.7),Ortho-
podomyiapulchripalpis(–0.2,–0.6)andUranotaeniaunguiculata(–0.2,–0.5);Lowerbox:Culex
territans(0,–8)andAnophelesplumbeus(–3.3,–8.1).
distance (Fig. 2) corroborate the same conclu- Anopheles petragnani Del Vecchio best define
sions already given. The high values of jaccard theaxisclosesttowildenvironments(Fig.4).
distance cophenitic correlations (r = 0.98, Finally,g is29.12andg is29.07.
climatic (climatic) (anthropic)
r =0.88)indicatehighcorrelationbetween Thesebotharevirtuallyidenticaltothevalueof
anthropic
theecologicaldistanceobservedinourstudyand thetotalspeciesrichness(29species)foundinthe
thedistancepredictedinthehierarchicalconfigu- studyarea.
rationoftheclusters.
ThePCAanalysisshowsthatC.hortensisand
O.caspiusarethespeciesthatbestdefinetheaxes 4.Discussion
closesttoMS(wettestandhighestbiodiversity)
andAM(driestandlowestbiodiversity),respec- Resultsfromourstudyshowthatmosquitodiver-
tively (Fig. 3). The opposite nature of the axes sityvariesacrossclimatesandlandusepatterns.
seemstoindicatethatthespeciesshouldalsoex- Previous researchers have proposed the use of
hibitoppositebehaviours. mosquitoes as bio-indicators of forest degrada-
In accordance with the values of the tion(Dorvillé1996)andofanthropicpressureon
synanthropicindex,thesecondPCAalsoreveals othernaturalenvironments(Montes2005).MSis
thatC.hortensis,C.mimeticus,C.territansand thewettestsector,consequentlytheabundanceof
196 BuenoMarí&Jiménez-Peydró (cid:127) ENTOMOL.FENNICAVol.22
Fig.4.PrincipalcomponentsanalysisbasedonJaccarddistance.PCvalues(PC1,PC2)of
specieswithinthebox:Aedesvittatus(0.8,–1),A.vexans(1.6,–2.1),Anophelesalgeriensis
(–1.1,0.2),A.atroparvus(–2.8,–3.1),A.claviger(2.2,–0.8),A.maculipennis(1.9,–1),A.mar-
teri(–0.4,0.2),Culisetaannulata(–2.2,–1.7),C.subochrea(–2,–1.5),Culeximpudicus(0.3,–
0.5),C.modestus(1.5,–2.3),C.theileri(–0.8,–1.1),Ochlerotatusdetritus(2.2,–2.1),O.berl-
andi(0.1,0.2),O.echinus(–0.2,0.6),O.geniculatus(0.3,0.9),O.gilcolladoi(–0.5,–0.9),O.
pulcritarsis(0,–0.4),Orthopodomyiapulchripalpis(0.4,–0.6),Uranotaeniaunguiculata(1.6,–2).
water and hetereogeneity of aquatic environ- the different species catched (Schaffner et al.
ments increase the appearance of colonizable 2001).However,inthissituationthereisproba-
habitats for many species, thereby increasing bly also an underlying human factor, since the
mosquitobiodiversity.Ontheotherhand,AMis coastalareasaretheregionswherehumansettle-
thedriestsector,thusonlyafewspecieswereca- ments tend to accumulate most, while inland
pableofadaptingtothisadversesituation.Simp- areashavehighermosquitobiodiversity.Thishy-
sonindicesshowdominancebyoneormorespe- pothesis is also supported by thedatarelated to
ciesthatarecharacterizedby theirhighpropor- thebiodiversityinurban,ruralandwildenviron-
tional abundance. In general, regardless of the ments. In this respect it is well known that C.
sector, C. pipiens and C. longiareolata are the hortensis is a zoophile (mainly feeding on ba-
dominant species. In addition, high dominance trachians and reptiles) and orophilic species,
should also be noted in C. hortensis in MS, O. which prefers to colonize freshwater environ-
caspiusinAMandCulexlaticinctusNoèinVT. mentsandcancompleteitsdevelopmentinvery
Ourstudyrevealsthatthewettestregionspresent varied breeding sites (Schaffner et al. 2001,
highermosquitobiodiversitythanthedriestones, BuenoMaríetal.2009a).Incontrast,O.caspius
especiallyinMediterraneanclimateswheretem- is a species characterized by a high anthropo-
peratureisnotalimitingfactor. philicbehavior,verycommonincoastalareasof
ThevaluesofNuorteva’ssynanthropicindex the Paleartic Region and highly associated with
arewellrelatedwiththehostpreferencesandtol- temporary puddles of brackish waters (Rioux
erationofdifferentwaterqualitiesdescribedfor 1958,Schaffneretal.2001).Inconclusion,ahigh
ENTOMOL.FENNICAVol.22 (cid:127) MosquitobiodiversityinSpain 197
anthropizationdoesnotimplyareductionofmos- advice on statistical treatment of data. We also want to
quito population in urban environments, but pointoutthatthisarticlewaspartiallyfundedbyResearch
ProjectCGL2009-11364(BOS),supportedbytheMinis-
ratheraselectionfilterthatisonlysurpassedbya
try of Science and Innovation of Spain (Ministerio de
fewspecies.
CienciaeInnovacióndelGobiernodeEspaña).
Moreover, Fig. 4 indicates that the co-exis-
tenceofC.hortensis,C.mimeticus,C.territans
orA.petragnanicouldbeusedasabioindicator References
element for wild environments. On the other
hand,C.pipiensandC.longiareolataarespecies
Aranda,C.,Eritja,R.&Roiz,D.2006:Firstrecordand
that have a high biological plasticity and there- establishment of the mosquito Aedes albopictus in
forecanbreedinenvironmentswithwidelyvary- Spain. — Medical and Veterinary Entomology 20:
ingdegreesofhumanpressure. 150–152.
Blázquez,J.&DeZulueta,J.1980:Thedisappearanceof
Faunistically,itisimportanttonotethatofthe
AnopheleslabranchiaefromSpain.—Parassitologia
29 mosquito species observed in this work, 13
22:161–163.
haveneverbeenrecordedpreviouslyinthestudy BuenoMarí,R.&JiménezPeydró,R.2008:Malariaen
area (Romeo Viamonte 1950, Encinas Grandes España:aspectosentomológicosyperspectivasdefu-
1982).Thisstudyallowedthecaptureofspecies turo.—RevistaEspañoladeSaludPública82:467–
489.[InSpanish.]
poorly and irregularly found in Spain such as
BuenoMarí,R.,ChordáOlmos,F.A.,BernuésBañeres,A.
AnophelesmarteriPrunelleandUranoteniaun-
&JiménezPeydró,R.2009a:Aportacionesalconoci-
guiculata Edwards (Torres Cañamares 1979, mientodelosmosquitos(Diptera,Culicidae)dealta
Bueno Marí et al. 2010), among others. The montañapresentesenlaPenínsulaIbérica.—Pirineos
synanthropicindicesfortheanophelinesconfirm 164:49–68.[InSpanish.]
BuenoMarí,R.,ChordáOlmosF.A.,BernuésBañeresA.
the low malariogenic potential described for
&JiménezPeydró,R.2009b:DeteccióndeAedesal-
Spain (Bueno Marí & Jiménez Peydró 2010a).
bopictus (Skuse, 1894) en Torrevieja (Alicante). —
Moreover, no A. labranchiae were found, the BoletíndelaAsociaciónespañoladeEntomología33:
Spanish distribution of which has previously 529–532.[InSpanish.]
beencircumscribedsouthofourstudyarea.The BuenoMarí,R.&JiménezPeydró,R.2010a:Puedenla
malariayeldenguereaparecerenEspaña?—Gaceta
dramatic reduction of irrigated agriculture in
Sanitaria24:347–353.[InSpanish.]
SoutheasternSpainperhapsledtotheeradication
BuenoMarí,R.&JiménezPeydró,R.2010b:Newanop-
ofA.labranchiae(Eritjaetal.2000).Thisspecies helinerecordsfromtheValencianAutonomousRe-
was an important malariavector and its capture gionofEasternSpain(Diptera:Culicidae:Anopheli-
was common up to 1946 (Clavero & Romeo nae).—EuropeanMosquitoBulletin23:148–156.
BuenoMarí,R.&JiménezPeydró,R.2010c:Situaciónac-
Viamonte 1948). Since then it has not been re-
tualenEspañayeco-epidemiologíadelasarbovirosis
corded in Spain (Blázquez & De Zulueta 1980,
transmitidaspormosquitosculícidos(Diptera:Culici-
BuenoMarí&JiménezPeydró2010b). dae).—RevistaEspañoladeSaludPública84:249–
Of concern is the expanding distribution of 263.[InSpanish.]
Aedes albopictus (Skuse), the Asian tiger mos- BuenoMarí,R.,BernuésBañeresA.,ChordáOlmosF.A.
&JiménezPeydró,R.2010:NuevosdatosdeUrano-
quito. This species, potential vector of several
taenia unguiculata Edwards, 1913 (Diptera: Culici-
arboviruses such as Dengue, Yellow Fever or
dae)paralaPenínsulaIbérica.—BoletíndelaSocie-
Chikungunya among others (Bueno Marí & Ji- dadEntomológicaAragonesa46:613–614.[InSpa-
ménezPeydró2010c),wasfirstrecordedinSpain nish.]
in2004(Arandaetal.2006)andwasrecentlyde- BuenoMarí,R.&JiménezPeydró,R.2011:Classification
ofSpanishmosquitoesinfunctionalgroups.—Jour-
tectedsouthofourstudyarea(BuenoMaríetal.
naloftheAmericanMosquitoControlAssociation27:
2009b).
1–7.
Clavero,G.&RomeoViamonte,J.M.1948:Elpaludismo
Acknowledgments.WearegratefultotheRegionalMinis- enlashuertasdeMurciayOrihuela.Ensayosdeapli-
try of the Generalitat Valenciana (Conselleria de Medi cacióndelosinsecticidasmodernos,D.D.T.y666,en
Ambient,Aigua,UrbanismeiHabitatge)forthegrantof laluchaantipalúdica.—RevistadeSanidadeHigiene
theinsectscapturepermissionsintheprotectedenclaves Pública22:199–228.[InSpanish.]
andtoProf.MarioSendra(DepartmentofStatisticsand Darsie,R.F.&SaminadouVoyadjoglou,A.1997:Keys
OperationalResearchoftheUniversityofValencia)forthe fortheidentificationofthemosquitoesofGreece.—
198 BuenoMarí&Jiménez-Peydró (cid:127) ENTOMOL.FENNICAVol.22
JournaloftheAmericanMosquitoControlAssocia- PemolaDevi,N.&Jauhari,R.K.2007:Mosquitospecies
tion13:247–254. associatedwithinsomewesternHimalayasphytoge-
Dorvillé,L.F.M.1996:Mosquitoesasbioindicatorsoffo- ographic zones in the Garhwal region of India. —
rest degradation in southeastern Brazil, a statistical JournalofInsectScience7:1–10.
evaluationofpublisheddataintheliterature.—Stu- Reinert,J.F.2000:Newclassificationforthecomposite
diesonNeotropicalFaunaandEnvironment31:68– genusAedes(Diptera:Culicidae:Aedini),elevationof
78. subgenusOchlerotatusto generic rank, reclassifica-
EncinasGrandes,A.1982:Taxonomíaybiologíadelos tionoftheothersubgenera,andnotesoncertainsubge-
mosquitosdeláreasalmantina(Diptera,Culicidae).— neraandspecies.—JournaloftheAmericanMosqui-
Universidad de Salamanca, Salamanca. 434 pp. [In toControlAssociation16:175–188.
Spanish.] RDevelopmentCoreTeam2005:R:alanguageandenvi-
Eritja,R.,Aranda,C.,Padrós,J.,Goula,M.,Lucientes,J., ronmentforstatisticalcomputing.—Ed.RFounda-
Escosa,R.,Marqués,E.&Cáceres,F.2000:Ananno- tionforStatisticalComputing;Vienna.[wwwdocu-
tatedchecklistandbibliographyofthemosquitoesof ment]URLwww.R-project.org.(Sitevisitedon2Oc-
Spain (Diptera: Culicidae). — European Mosquito tober,2010)
Bulletin8:10–18. Rioux,J.A.1958:Lesculicidesdu“Midi”mediterranéen.
Forattini, O. P., Kakitani, I., Massad, E. & Marucci, D. Etudesystematiqueetécologique.—Encyclopédie
1993:Studiesonmosquitoes(Diptera:Culicidae)and Entomologique.Ser.A.,XXXV,Paris.303pp.
anthropicenvironment.3–Surveyofadultstagesat RomeoViamonte,J.M.1950:LosanofelinosdeEspanay
thericeirrigationsystemandtheemergenceofAnop- delazonaespañoladelProtectoradodeMarruecos.Su
helesalbitarsisinSouth-EastemBrazil.—Revistade relaciónconladifusióndelpaludismo.—Revistade
SaúdePública27:313–325. SanidadeHigienePública24:213–295.[InSpanish.]
GeneralitatValenciana-GVA(2003):Hábitatsprioritarios Schaffner,F.,Angel,G.,Geoffroy,B.,Hervy,J.O.&Rha-
delaComunidadValenciana.—ConselleriadeTerri- eim,A.2001:ThemosquitoesofEurope/Lesmousti-
toriiHabitatgedelaGeneralitatValenciana,Valencia. quesd’Europe[computerprogram].—Montpellier,
222pp.[InSpanish.] France:IRDÉditionsandEIDMéditerranée.
Halffter,G.1998:Astrategyformeasuringlandscapebio- Schluter,D.&Ricklefs,R.E.1993:Speciesdiversityin
diversity.—BiologyInternational36:3–17. ecologicalcommunities:historicalandgeographical
Kindt,R.&Coe,R.2005:Treediversityanalysis:Amanu- perspectives. — The University of Chicago Press,
al and software for common statistical methods for Chicago.414pp.
ecologicalandbiodiversitystudies.—Ed.WorldAg- Service,M.W.1993:MosquitoEcology.FieldSampling
roforestry Centre (ICRAF), Nairobi. [www docu- Methods.2ndedition.—ElsevierSciencePublishers,
ment] URL http://www.worldagroforestry.org/tree- London.988pp.
sandmarkets/tree_diversity_analysis.asp.(Sitevisited TorresCañamares,F.1979:Breverelacióncríticadelos
on2October,2010) mosquitosespañoles.—RevistadeSanidadeHigiene
Montes,J.2005:CulicidaefaunaofSerradaCantareira, Pública53:985–1002.[InSpanish.]
SaoPaulo, Brazil. —RevistadeSaúdePública39: Whittaker,R.H.1972:Evolutionandmeasurementofspe-
578–584. ciesdiversity.—Taxon21:213–251.
Moreno,C.2001:Métodosparamedirlabiodiversidad.— Zhong,H.,Yan,Z.,Jones,F.&Brock,C.2003:Ecological
Ed.Cyted,Orcyt-Unesco&SEA,Zaragoza.86pp.[In analysisofmosquitolighttrapcollectionsfromWest
Spanish.] Central Florida. — Environmental Entomology 32:
Nuorteva,P.1963:Synanthropyofblowflies(Dipt.,Cal- 807–815.
liphoridae)inFinland.—AnnalesEntomologiciFen-
nici29:1–49.