RevistaBrasileiradeEntomologia59(2015)96–99
ww w . r b e n t o m o l o g i a . c o m
REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolutionShort
Communication
Sex
ratios
in
juveniles
and
adults
of
Dichroplus
maculipennis
(Blanchard)
and
Borellia
bruneri
(Rehn)
(Orthoptera:
Acrididae)
Yanina
Mariottini
a,∗,
Martina
E.
Pocco
a,b,
María
L.
de
Wysiecki
a,
Carlos
E.
Lange
a,caCentrodeEstudiosParasitológicosydeVectores(CONICET),BuenosAires,Argentina
bDivisiónEntomología,MuseodeLaPlata,UniversidadNacionaldeLaPlata,BuenosAires,Argentina cComisióndeInvestigacionesCientíficasdelaProvinciadeBuenosAires,BuenosAires,Argentina
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received26June2014 Accepted3February2015 Availableonline9April2015 AssociateEditor:KleberDelClaro Keywords: Acrididae Adults Nymphs Pampasregion Sexratio
a
b
s
t
r
a
c
t
DichroplusmaculipennisandBorelliabruneriaretwoofthe18grasshopperspeciesofactualorpotential economicrelevanceaspestsinArgentina.Theobjectiveofthisstudywastoestimatethesexratiosfor adultsandoldernymphsofD.maculipennisandB.bruneriinthefield,andanalyzepossibletemporal variations.Thestudywasconductedduringsevenseasons(2005–06to2011–12)inrepresentativeplant communitiesofthesouthernPampasregion.Atotalof4536individualsofD.maculipennis,and6038 individualsofB.bruneriwerecollected.ThesexratioregisteredinoldernymphsforD.maculipennisand B.brunerididnotdeviatefroma1:1ratio(p>0.05),suggestingthatthesespecieshavesuchaprimarysex ratio.However,asignificantbiasinsexcompositioninadultsofbothspecieswasobserved(p<0.05).The sexratioinadultsofD.maculipenniswasdifferentinfiveofthe18samplingdatescarriedout.Inthree samplingdatesitwasbiasedtowardmales,whileintheothertwoitwasbiasedtowardfemales.Taking intoaccountthesexratiobysamplingseason,significantdifferenceswererecordedintwoseasons.In 2007–08thesexratiowasbiasedtowardmales(1F:2.26M),whilein2008–09itwasbiasedtoward females(1.35F:1M).ThesexratioinadultsofB.bruneriwasalwaysbiasedtowardmales(p<0.05). Weconcludethatresultsobtainedinthisstudyindicatethatvariousfactorslikedifferentialsurvival, dispersion,predation,amongothers,couldhavemodifiedtheprimarysexratiointhesespecies.
©2015SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Allrightsreserved.
Populationsarecharacterizedbystructuralattributes,suchas density,spatialdistribution,dispersionpattern,age,genetic com-position,andsexratio.Theseattributeschangethroughtimeand spaceasaresultofresponsestochangingenvironmentalconditions
(Schowalter,2006).Severalauthorshavehighlightedthe
impor-tanceofestimatingthesexratioofapopulationinstudiesonlife cycles,populationdynamics,sexualselection, andalsoasa key factorinbiologicalcontrolprograms(Mulkern,1983;Smithetal.,
2004).
Dichroplusmaculipennis(Blanchard,1851)andBorelliabruneri (Rehn,1906)aretwoofthe18grasshopperspeciesconsideredto beofactualorpotentialeconomicrelevanceaspestsinArgentina
(Ciglianoetal.,2014).D.maculipennisisoneofthemostdamaging
pestsmainlyinareasofthePampasandPatagoniaregions(Lange etal.,2005).B.bruneriisalsoacommonspeciesofgrasshopper communities inhabiting thePampas grasslands and one of the mostharmfulinthePampasofUruguay(COPR,1982).Bothare univoltinewithobligatoryembryonicdiapause(Mariottinietal.,
∗ Correspondingauthor.
E-mail:[email protected](Y.Mariottini).
2011a),andtheyhaveawidegeographicdistribution,occurring
in southernmost Brazil,much of Argentina, Chile,and Uruguay
(Eadesetal.,2013).
Sincelate2005grasshoppermonitoringisbeingconductedin representativeplantcommunitiesofthesouthernPampas,anarea affectedbygrasshopperpests.MajoroutbreaksofD.maculipennis andB.bruneriwererecordedfromlate2008toearly2011 caus-ingsignificanteconomiclosses,affectingawidevarietyofcrops andnaturalgrasslandsinanareaofapproximately2.5millionha
(Mariottinietal.,2012).Consideringtheimportanceofknowing
thestructuralattributesofpopulationsofpestspecies,the objec-tivewastoestimatethesexratiosforadultsandoldernymphs (juveniles)ofD.maculipennisandB.bruneriinthefieldandanalyze possibletemporalfluctuations.
ThestudywasconductedinLapridacounty(36◦02S,59◦06W), BuenosAiresprovince,intheSouthofthePampasregionasdefined
byCabreraandWillink(1973).Grasslandsarethedominant
vege-tationtypeinthisregion,farmingandlivestockproductionbeing widespread(Batistaetal.,2005).Grasshoppersamplingswere per-formedfromlatespringtolatesummerduringsevenconsecutive seasons(2005–06to2011–12).Thesamplingsitesrepresentthe mostcommonplantcommunitiesinthearea,classifiedintofour
http://dx.doi.org/10.1016/j.rbe.2015.03.003
Y.Mariottinietal./RevistaBrasileiradeEntomologia59(2015)96–99 97
Fig.1. (A),(B),(E)–(H)Dichroplusmaculipennis.(A)Adultfemale.(B)Juvenilefemale.(E)and(F)Maleexternalgenitalia,dorsal(E)andlateral(F)views.(G)and(H)Juvenile femaleexternalgenitalia,dorsal(G)andlateral(H)views.(C),(D),(I)–(L)Borelliabruneri.(C)Adultfemale.(D)Juvenilefemale.(I)and(J)Maleexternalgenitalia,dorsal(I) andlateral(J)views.(K)and(L)Juvenilefemaleexternalgenitalia,dorsal(K)andlateral(L)views.
categories:nativegrasslands,disturbedgrasslands,implanted pas-tures,andhalophilousgrasslands(Mariottinietal.,2013).Three replicatesofeachcategorywereestablished,givingatotalof12 sites.Grasshopperswerecollectedby200sweepsof entomologi-calnets(diameter:40cm,depth:75cm,arcofsweep:180◦)along transectsthroughthevegetationateachsite,anefficientmethod forobtainingrepresentativesamplesofgrasshoppercommunities
(Larsonetal.,1999).Grasshopperscollectedweretakentothe
labo-ratoryforidentificationfollowingCarbonelletal.(2006).Sexratios weredeterminedinoldernymphs(instarsfourandfiveinB.bruneri, andfourtosixinD.maculipennis)andadultsofbothspeciesby
examinationof theexternal characteristicsofgenitalia(Uvarov, 1966)(Fig.1).Sexratioswereestimatedforadultsandnymphs independently,consideringthetotalofadultsornymphscollected inallsitesateachcollectingdate.Differencesbetweenthe propor-tionofmalesandfemalesofeachspecieswereanalyzedbyatestof comparisonoftwoproportions,andsexratioswerecomparedby samplingtimeandforsamplingseason.ThesoftwareXlstat7.5.3
wasused(Addinsoft,2005).
A total of 4536 individuals of D. maculipennis (2974 adults, 1562 nymphs)and 6038 individuals ofB. bruneri(5327 adults, 711 nymphs) were collected. Differences in the sex ratio of
98 Y.Mariottinietal./RevistaBrasileiradeEntomologia59(2015)96–99
Table1
SexratiosinoldernymphsandadultsofDichroplusmaculipennisinLapridacounty, BuenosAires,Argentina,during2005–2012.
Season Date Stage Number Ratio F M F M p 2005–06 01/10/06 A 8 7 0.53 0.47 0.79 02/16/06 A 5 6 0.45 0.55 0.76 Total 13 13 0.5 0.5 1 2006–07 12/12/06 – – – – – – 12/24/06 A 10 18 0.36 0.64 0.15 01/10/07 A 22 22 0.5 0.5 1.00 02/05/07 A 10 9 0.53 0.47 0.82 Total 42 49 0.46 0.54 0.57 2007–08 12/31/07 A 18 28 0.42 0.58 0.29 01/28/08 A 39 65 0.37 0.63 0.10 02/23/08 A 8 41 0.16 0.84 <0.0001 Total 65 134 0.33 0.67 <0.0001 2008–09 12/13/08 N 115 121 0.49 0.51 0.69 A 127 129 0.50 0.50 0.87 01/03/09 A 226 132 0.63 0.37 <0.0001 Total 468 382 0.55 0.45 0.003 2009–10 11/27/09 N 429 476 0.47 0.53 0.12 12/14/09 N 134 112 0.54 0.46 0.16 A 40 65 0.38 0.62 0.02 01/03/10 A 97 182 0.35 0.65 <0.0001 01/28/10 A 291 210 0.58 0.42 0.00 Total 991 1045 0.49 0.51 0.232 2010–11 12/11/10 A 50 66 0.43 0.57 0.14 01/17/11 A 403 414 0.49 0.51 0.57 Total 453 480 0.49 0.51 0.38 2011–12 12/06/11 N 95 80 0.54 0.46 0.25 A 3 2 0.60 0.40 0.66 01/04/12 A 105 116 0.48 0.52 055 Total 203 198 0.48 0.52 0.46 A,adult;F,female;M,male;N,nymph;p,testresultofcomparisonoftwo propor-tions.
D. maculipennis nymphs were not significant. Significant
dif-ferences were registered for adults in five sampling moments
(Table1).InFebruary2008thesexratiowasbiasedtowardmales
(1F:5.25M)whileinearlyJanuary2009therewasabiastoward females (1.71F:1M). In the three samplings carried out during 2009–10,significantdifferenceswererecordedinDecember2009 (1F:1.65M)andearlyJanuary2010(1F:1.87M),wherethesexratio wasbiasedtowardmales(Table1).InlateJanuary2010,the pro-portionoffemaleswashigherthanmales(1.39H:1M).Regarding thesexratiobysamplingseason(Table1),significantdifferences wererecordedinonlytwoseasons.
InB.bruneri,differencesinsexratioofnymphswerenot sig-nificant.However,inadultsthesexratiowasalwayssignificantly differenteitherbysamplingtimeandseasons(Table2).Inall sam-ples,thesexratiowasbiasedtowardmales.
Resultsobtainedshowthatsexproportionsrecordedinolder nymphsfor D. maculipennis and B.brunerido not deviatefrom a1:1ratio,suggestingthatthesespecies,likeothergrasshopper species,havesuchaprimarysexratio(Joernand Gaines,1990). Nevertheless,a significantbias in sex composition in adults of bothspecies wasobserved.Accordingtoseveralauthorsbiased sexratiosininsectpopulations couldbetheresultofa variety ofcausesliketheexistenceofprotandry,adifferentialsurvivalof malesandfemalesinresponsetoenvironmentalconditionsor nat-uralenemies,differentdispersionstrategies,orevendeficiencies insamplingtechniques,amongothers(BelovskyandSlade,1993;
Swordetal.,2008;Ortegoetal.,2011).
Table2
SexratiosinoldernymphsandadultsofBorelliabruneriinLapridacounty,Buenos Aires,Argentina,during2005–2012.
Season Date Stage Number Ratio F M F M p 2005–06 01/10/06 A 61 150 0.29 0.71 <0.0001 02/16/06 A 34 59 0.37 0.63 0.015 Total 95 209 0.31 0.69 <0.0001 2006–07 12/12/06 N 51 43 0.54 0.46 0.41 12/24/06 A 41 120 0.25 0.75 <0.0001 01/10/07 A 159 434 0.27 0.73 <0.0001 02/05/07 A 95 146 0.39 0.61 0.001 Total 346 743 0.32 0.68 <0.0001 2007–08 12/31/07 A 140 377 0.27 0.73 <0.0001 01/28/08 A 320 611 0.34 0.66 <0.0001 02/23/08 A 105 311 0.25 0.75 <0.0001 Total 565 1299 0.30 0.70 <0.0001 2008–09 12/13/08 N 126 109 0.54 0.46 0.27 A 30 66 0.31 0.69 <0.0001 01/03/09 A 618 836 0.43 0.57 <0.0001 Total 774 1011 0.43 0.57 <0.0001 2009–10 11/27/09 N 43 41 0.51 0.49 0.72 12/14/09 N 152 146 0.51 0.49 0.83 A 23 57 0.29 0.71 0.001 01/03/10 A 101 180 0.36 0.64 <0.0001 01/28/10 A 55 94 0.37 0.63 0.002 Total 374 518 0.42 0.59 <0.0001 2010–11 12/11/1001/17/11 –A –7 18– –0.28 –0.72 –0.044 2011–12 12/06/11 – – – – – – 01/04/12 A 24 55 0.30 0.70 0.001 A,adult;F,female;M,male;N,nymph;p,testresultofcomparisonoftwo propor-tions.
ThesexratioinadultsofD.maculipenniswassignificantly
dif-ferentinonlyfiveofthe18samplingdatescarriedoutandintwoof
thesevenseasons.InDecemberandearlyJanuary,timeintervalat
whichnormallyindividualsbegintoemergeasadults(Mariottini
etal.,2011a),significantdifferenceswereobservedinthree
samp-lingmoments.Basedontheseresults,itisnotpossibletodetect atrend thatwould indicatethatmale adultsof D.maculipennis emergefirstthanfemales.Therefore,protandryseemsnottobe thecase.
Awiderangeofinvertebrateandvertebratepredators,among othernaturalenemies,affectgrasshopperpopulations(Greathead,
1992;Bardietal.,2012).Birdsareconsideredtheprincipal
ver-tebrate predator on grasshoppers (Belovsky and Slade, 1993). Somestudiessuggestthatlargebodysizeinchemicallydefended grasshoppershasevolvedasahighlybeneficialantipredatortrait
(Whitman and Vincent,2008).However, there is alsoevidence
thatbirdstendtoselectlargerbodysizegrasshoppers,modifying thegendercomposition ofthepopulations (BelovskyandSlave,
1993; Branson, 2005). Gardner and Thompson(1998) reported
thatfemalegrasshopperswouldbepreferredbybeinglargerthan males.TheseauthorsreportedthatfemalesofHesperotettixviridis (Thomas,1872)andMelanoplusaridus(Scudder,1878)appearedto beselectedmorethanmalesbybirds.SinceD.maculipennisfemales aresignificantlylargerthanmales(Mariottinietal.,2011b)they couldbeselectedaspreymorefrequentlythanmales.Although wedidnotconductstudiesonthisplausiblefactorofbiasedsex ratios,largeflocksofavarietyofbirdswereoftenseenapparently preyinginareasofgrasshopperaggregationsandthiscouldexplain therecordedsexratiobiasedtomalesinsamplingsmomentsofthe 2007–08seasonsandinearlyJanuaryof2010.
Y.Mariottinietal./RevistaBrasileiradeEntomologia59(2015)96–99 99 Inrelationtodifferentsex-relateddispersalbehavior,itishas
beenmentionedthatmales,bybeingsmallerinsize,arefavored bywind-assisteddispersal,andthatfemaleswouldbemoreprone toremainclosetositesofbirth(Swordetal.,2008).For
exam-ple,Ortegoetal.(2011)showedthatdispersioninthegrasshopper
Mioscirtus wagneri (Eversmann, 1859) is biased to males, and femalestendtobemorephilopatric.ThedispersionbehaviorofD. maculipennisisakeyfeatureinthedynamicsofthisspeciesanditis animportantaspecttoconsiderinfuturestudies.Atlowdensities, D.maculipennisappearstoshowarelativelysedentarybehavior, butduring outbreakyears adults displaysignificantswarm-like displacementsreachingdistancesofupto50km(COPR,1982).In late2008andearly2009,anoutbreakofD.maculipennisof histor-icalmagnitudethatshowedthecharacteristicenmassedispersal flightsandaffectedthestudyareaandseveralnearbycountieswas observed(Mariottinietal.,2012).Duringthisperiod,asexratio biasedtofemaleswasrecorded,suggestingthepossibilityof dif-ferentialsex-relateddispersioninD.maculipennis.Ourresultsthen couldindicatethatmaleshaveagreaterdispersionpotentialthan females.
ThesexratioinadultsofB.bruneriwassignificantlydifferentin allsamplings,anditwasalwaysbiasedtomales.However,thesex ratiorecordedinoldernymphswas1:1.Theseresultssuggestthat justpriortoadultemergenceorimmediatelyafter,ayetunknown factoraffectedtheproportionoffemalesofthisspecies.Mulkern
(1983)indicatedthattemperature,solarradiation,windspeed,and
thetypeandamountofvegetationcanalsoinfluencetheactivity ofgrasshoppersandthustheeffectivenessofsamplingtechniques. Thisauthorstudiedthesexratioof11grasshopperspeciesinthe field,andobservedthatitwasconstantineachspecies,whichcould beattributedtoapossiblebiasinthesamplingtechniqueor repre-sentthetruecompositionofpopulations.Webelieve,however,that consideringtheextendedsamplingperiodofourstudy,thenumber ofsamplestaken,andtheamountofindividualscollectedforthe twospecies,theresultspresentedherewouldrepresentthetrue sexcompositionofpopulationsofB.bruneriandD.maculipennisin southernPampasregion.
Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgments
Thisstudy was partiallysupported by theAgencia Nacional dePromociónCientíficayTécnica(PICTN◦ 2012/1870),Consejo NacionaldeInvestigacionesCientíficasyTecnológicas(CONICET), andUniversidadNacionaldeLaPlata(UNLP,11/N595).
References
Addinsoft,2005.XLSTATProVersion7.5.3,Availableat:http://www.xlstat.com/ en/home(accessed25.04.14).
Bardi,C.J.,Mariottini,Y.,Plischuk,S.,Lange,C.E.,2012.Statusofthealienpathogen Paranosemalocustae(Microsporidia)ingrasshoppers(Orthoptera:Acridoidea) oftheArgentinePampas.BiocontrolSci.Technol.22,497–512.
Batista,W.B.,Taboada,M.A.,Lavado,R.S.,Perelman,S.B.,León,R.J.C.,2005.Asociación entrecomunidadesvegetalesysuelosenelpastizaldelaPampaDeprimida.In: Oesterheld,M.,Aguiar,M.R.,Ghersa,C.M.,Paruelo,J.M.(Eds.),Laheterogeneidad delavegetacióndelosAgroecosistemas.UnhomenajeaRolandoLeón.Editorial FacultaddeAgronomía,BuenosAires,pp.113–129.
Belovsky,G.E.,Slade,J.B.,1993.Theroleofvertebrateandinvertebratepredatorsin agrasshoppercommunity.Oikos68,193–201.
Branson,D.H.,2005.Directandindirecteffectsofavianpredationongrasshopper communitiesinnorthernmixed-grassprairie.Environ.Entomol.34,1114–1121.
Carbonell,C.,Cigliano,M.M.,Lange,C.E.,2006.AcridomorphSpeciesofArgentina andUruguay.CD-ROM.PublicationsonOrthopteranDiversity.TheOrthopterists Societyatthe“MuseodeLaPlata”,Argentina.
Cabrera,A.L.,Willink,A.,1973.BiogeografíadeAméricaLatina.Monografía13.Serie deBiología.SecretaríaGeneraldelaOrganizacióndelosEstadosAmericanos, Washington.
Cigliano,M.M.,Pocco,M.E.,Lange,C.E.,2014.Acridoideos(Orthoptera)de impor-tanciaagroeconómicaenlaRepúblicaArgentina.In:RoigJu ˜nent,S.A.,Claps, L.C.,Morrone,J.J.(Eds.),BiodiversidaddeArtrópodosArgentinos,Volumen3. EditorialINSUE-UniversidadNacionaldeTucumán,SanMigueldeTucumán, Argentina,pp.1–36.
COPR,1982.TheLocustandGrasshopperAgriculturalManual.CentreforOverseas PestResearch,London.
Eades,D.C.,Otte,D.,Cigliano,M.M.,Braun,H.,2013.OrthopteraSpeciesFileOnline. Version2.0/4.0,Availableonlineat:http://Orthoptera.SpeciesFile.org(accessed 21.04.14).
Gardner,K.T.,Thompson,D.C.,1998.Influenceofavianpredationonagrasshopper (Orthoptera:Acrididae)assemblagethatfeedsonthreadleafsnakeweed.Popul. Ecol.27,111–116.
Greathead,D.J.,1992.Naturalenemiesoftropicallocustsandgrasshoppers:their impactandpotentialasbiologicalcontrolagents.In:Lomer,C.J.,Prior,C.(Eds.), BiologicalControlofLocustsandGrasshoppers.CABI,Wallingford,pp.105–121.
Joern,A.,Gaines,S.B.,1990.Populationdynamicsandregulationingrasshoppers.In: Chapman,R.F.,Joern,A.(Eds.),BiologyofGrasshoppers.JohnWileyandSons, Inc.,NewYork,pp.415–483.
Lange,C.E.,Cigliano,M.M.,DeWysiecki,M.L.,2005.Losacridoideos(Orthoptera: Acridoidea)deimportanciaeconómicaenlaArgentina.In:BarrientosLozano, L.,AlmaguerSierra,P.(Eds.),Manejointegradodelalangostacentroamericana (Schistocercapiceifronspiceifrons,Walker)yacridoideosplagaenAméricaLatina. InstitutoTecnológicodeCiudadVictoria,Tamaulipas,pp.93–135.
Larson,D.P.,O ´Neill,K.M.,Kemp,W.P.,1999.Evaluationoftheaccuracyof sweep-samplingin determininggrasshopper(Orthoptera:Acridoidea)community composition.J.Agric.Urb.Entomol.16,207–214.
Mariottini,Y.,DeWysiecki,M.L.,Lange,C.E.,2011a.Seasonaloccurrenceoflifestages ofGrasshopper(Orthoptera:Acridoidea)intheSouthernPampas,Argentina. Zool.Stud.50,737–744.
Mariottini,Y.,DeWysiecki,M.L.,Lange,C.E.,2011b.Postembryonicdevelopment andfoodconsumptionofDichropluselongatusGiglio-TosandDichroplus mac-ulipennis(Blanchard)(Orhtoptera:Acrididae:Melanoplinae)underlaboratory conditions.Neotrop.Entomol.40,190–196.
Mariottini,Y.,DeWysiecki,M.L.,Lange,C.E.,2012.Variacióntemporaldelariqueza, composiciónydensidaddeacridios(Orthoptera:Acridoidea)endiferentes comunidadesvegetalesdelSurdelaprovinciadeBuenosAires.Rev.Soc. Ento-mol.Argent.71,275–288.
Mariottini,Y.,DeWysiecki,M.L.,Lange,C.E.,2013.Diversidadydistribuciónde acridios(Orthoptera:Acridoidea)enpastizalesdelsurdelaregiónPampeana, Argentina.Rev.Biol.Trop.61,111–124.
Mulkern, G.B.,1983.SexratiosofMelanoplussanguinipesand OtherAcrididae (Orthoptera).J.KansasEntomol.Soc.56,457–465.
Ortego,J.,Aguirre,M.P.,Cordero,P.J.,2011.Fine-scalespatialgeneticstructureand withinpopulationmale-biasedgene-flowinthegrasshopperMioscirtuswagneri. Evolut.Ecol.25,1127–1144.
Schowalter,T.,2006.InsectEcologyanEcosystemApproach2.AcademicPress, London.
Smith,M.A.H.,Wise,I.L.,Lamb,R.J.,2004.SexratiosofSitodiplosismosellana(Diptera: Cecidomyiidae):implicationsforpestmanagementinwheat(Poaceae).Bull. Entomol.Res.94,569–575.
Sword,G.A.,Lorch,P.D.,Gwynne,D.T.,2008.Radiotelemetricanalysisoftheeffects ofprevailingwinddirectiononMormoncricketmigratorybandmovement. Environ.Entomol.37,889–896.
Whitman,D.W.,Vincent,S.,2008.Largesizeasananti-predatordefenseina grasshopper.J.Orthop.Res.17,253–371.
Uvarov,B.,1966.GrasshoppersandLocusts:AHandbookofGeneralAcridology.Vol. I.CambridgeUniv.Press,Cambridge.