Notes on the nest of the social wasp Pseudopolybia langi (Hym., Vespidae, Polistinae)

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REVISTA

BRASILEIRA

DE

Entomologia

AJournalonInsectDiversityandEvolution

w w w . r b e n t o m o l o g i a . c o m

Biology,

Ecology

and

Diversity

Notes

on

the

nest

of

the

social

wasp

Pseudopolybia

langi

(Hym.,

Vespidae,

Polistinae)

Sherlem

Patricia

de

Seixas

Felizardo,

Ian

Patrick

Vilhena

dos

Santos,

Orlando

Tobias

Silveira

∗

MuseuParaenseEmílioGoeldi,Coordenac¸ãodeZoologia,DepartamentodeInvertebrados,Belém,PA,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received22November2017 Accepted16February2018 Availableonline1March2018 AssociateEditor:MarcelHermes Keywords: Nestarchitecture Socialbehavior Epiponini Neotropical Amazonia

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b

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DetaileddescriptionsofthearchitectureofPseudopolybialanginestsarepresentedfortheﬁrsttime. Struc-turalvariationsinthearrangementsofnestpartsaredescribedandcomparedwithfeaturesobservedin otherspeciesofPseudopolybiaandotherepiponinegenera.

Introduction

ThesubfamilyPolistinaeisknownforthegreatdiversityand beautyofitsnestarchitecture(Richards,1971;Wenzel,1991,1993, 1998).Somegenera,suchasPolistesandMischocyttarus,usually havesmallnestswithsimple structuresandunenvelopedsingle combs,oftenwithlessthanahundredcells.Thenestsofseveral speciesofepiponinegenera,however,maybequitelarge,with hun-dredstothousandsofcellsinseveralcombs,andareusuallycovered byanenvelope(Carpenter,1991;Jeanne,1975,1991; Richards, 1978).

Pseudopolybiavon Dalla Torre 1894 is a wasp genus of the tribeEpiponinithatisnormallyfoundinforestedareas,withfour speciesdistributedfromNicaraguatosouthernBrazil(Richardsand Richards,1951;Richards,1978).Itisdistinguishedbythethird seg-mentofthelabialpalpibearingashort,stout,curvedbristlenear itsapex,andthenumberofpalpalsegmentsbeingsixmaxillary andfourlabial(Richards,1978;Andenaetal.,2007).Thenestsof mostspeciesinthegenusareovaltosphericalarborealobjects, pre-sentingapaleyellowtobrownenvelopecomposedoflaminateor imbricatesheets(muchlikethoseofvespinespecies),witha sim-pleentry;eachcombisattachedtothecombabovebyvertically positionedpedicels.Combdiametersgraduallydecreasefromthe

∗ Correspondingauthor.

E-mail:orlando@museu-goeldi.br(O.T.Silveira).

ﬁrstcombtothelast(Jeanne,1975;Andenaetal.,2007).Details ofsuchdistinctivearchitecturescanbeobservedintheFig.4Ein thispapershowinganestofP.difﬁcilis(Ducke1905),whichisalso representativeoftheinternalstructureofthenestsofP.vespiceps (Saussure1864)andP.compressa(Saussure1854).Otherimagesof nestsofthesespeciesmaybefoundinDucke(1914,p.318),and Richards(1978,p.4).InthepapersbyWenzel(1993,1998)about vespidnestarchitecture,informationonthegenusPseudopolybia wasonlybasedonfeaturesobservedintheabovethreespecies(i.e. envelopelaminate;combsroundoroval,secondarycombs sus-pendedfromthoseabovebycentralpedicel;cocooncapssimple; entrancesimpleatlowestpoint).

PseudopolybialangiBequaert,1944differsfromitscongenersin severalaspects,beingamuchsmallerwasp(6–8mmlongversus 13–15mminotherspecies),andwithamoreelongatedbody.It hasbeenrecordedfortheGuyanas,Ecuador,andBrazil.Inthe lat-tercountry,itisknownfromthestatesofAmapáandAmazonas inareascoveredbyrelativelyundisturbed“terra-ﬁrme” rainfor-est.DuetotherelativerarityofP.langi,itsnestswereunknownto Bequaert(1944)andeventoRichards(1978),onlybeingmentioned (butnotdescribed)inapaperbyDejeanetal.(1998)inassociation withpalmtreesofthegenusAstrocaryum.Later,oneofus(OTS) encounteredafullydeveloped(althoughdamaged)nestinAmapá State(IEPAcollection;notfoundinrecentvisitsbytheauthors).A photographofthisspecimenwasusedbyAndena(2007;thesis)to prepareabriefdescriptionthatwasusedinaphylogenetic analy-sispublishedbyAndenaetal.(2007).Werecentlycollectedanew well-preservednestspecimeninAmapáState(MPEGcollection)

https://doi.org/10.1016/j.rbe.2018.02.002

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whichbetterdemonstratesbothexternalandinternalaspectsof thearchitectureofthespecies–makingitrelevanttopresentafull descriptionofthenestarchitectureofP.langiandanalyzesome observedvariationsintermsofPseudopolybianestarchitectureas wellassomeotherepiponinegenera.

Methods

Specimensexamined

Thenestsusedhereasreferencesfor thedescriptionofnest architectureofP.langiwerebothencounteredinareascoveredby ombrophilous“terra-ﬁrme”rainforestinthefollowinglocalitiesin Brazil:

Specimen#1:Amapá.LaranjaldoJari,RESEXCajari,comunidade Marinho(00◦3444S/52◦1316W),01/ix/2001,O.T.Silveira(IEPA collection;notfoundinrecentvisitsbytheauthors).Thenestwas broughttoOTSbyaboywhofounditinanorchardtree(probably Annonaceae).Ithadbeentransportedinaplasticbagandshowed somedamagecausedbycrushing.Photographsweretakenjusta fewhoursafterreceivingthespecimen.Thenestwasremovedfrom theplasticbag,theenvelopecarefullydetached,andthebrokenand loosecombsweresetapartfromtheremainingnestelementsstill

Fig.1. NestofP.langifromRESEXCajari;scale:2cm.

afﬁxedtothesubstrateleaf(seeFig.1).Thisnestwasnot reex-aminedrecently,andourpresentcommentsarebasedonOTS’s knowledgeandmemoryofthespecimenin2001,aswellas avail-ablephotographs.

Specimen #2: Amapá. Ferreira Gomes, Floresta Nacional do Amapá(FLONAAmapá;0◦5803.36N/51◦3819.09W),08/iii/2016, FelizardoS.P.S.&SantosI.P.(MPEG).Thenestwaslocatedalong atrailintheAmapáplotofthePPBiobiodiversityresearch pro-gram.Itwasfoundinarelativelydry area,approximately2km fromtheAraguariRiver,andatleast500metersdistantfromany othersmallerwatercourse.Thenestwasinayoungtreeofthe fam-ilyAnnonaceae(2.5mtall)withsmallleaves,andwasattachedto twooftheleaves,approximately2mabovetheground.Theentire nestwascollectedinaplasticbag(togetherwithwaspspresent atthemoment,numberingabout40individuals).Thebroodinthe nestcellsconsistedonlyofeggsandsmalltomedium-sizedlarvae. Duetothefragilityoftheenvelope,somedeformationoccurred aroundtheentrance,butthisdidnotprejudicetheobservationof itsoriginalform.

Informationconcerninga third nestspecimenwasalsoused for comparative purposes. It consists of a fragmented nest in the collection of the American Museum of Natural History (AMNH; Amazonas, 03/x/1991; catalog 910310-1). A photo-graph is available on the internet at http://research.amnh.org/ iz/hymenoptera/collection/display.php?sid=401491.

Measurements

MeasurementsoftheFLONA-Amapáspecimenweremadeusing apachymeter.Nestsavailableonlyfromphotographswere mea-suredindirectlyusingImageJsoftware(https://imagej.nih.gov/ij/), basedonscaleinformationavailableinthephotographs(aruler inthecaseoftheIEPA–Cajarinest;cellsizeinthecase ofthe AMNHspecimen).Measurementswereobtained(whenpossible) of:combs(majorandminordiametersandheight),celldimensions, pedicellengths,theenvelopes,andassociatedsubstrateleaves. ComparativeanalysisoftheevolutionofP.langinestfeatures

TocomparesomeofthearchitecturalfeaturesofP.langiwith thoseofotherepiponinetaxawithinaphylogeneticframework,we performedtheparsimoniousoptimizationofthesenestcharacters withtheprogramWinclada(Nixon,2002)onaphylogenetictree forthePolistinaeadaptedfromatreepublishedbyWenzeland Car-penter(1994)basedonmorphologicaladultandlarvalcharacters, aswellasonnestcharacteristics.Characterstatesweregenerally codedaccordingtothephylogeneticstudybyWenzel(1993).In theadaptedtreeshowedinFig.5(forEpiponinionly),Occipitalia andSynoecoidesareomitted,sincetheyhavebeensynonymized toClypeariaandPolybia,respectively(seeCarpenteretal.,1996, 2000).Foritsdistinctivenestarchitecture,Marimbondais main-tainedand representedinthetreeassister-groupofLeipomeles (seeCarpenter,2004);P.langiisaddedtothetreeassister-group ofotherPseudopolybiaspecies,accordingtoAndenaetal.(2007).

Results

TheFLONA-Amapánest wasusedasa primaryreference,as it was collected undamaged and its original shape was well-preserved.Theenvelopeisasmallinvertedﬂask-shapedstructure, ﬁxed laterally to two small leaves (1.7cm wide, 6.5cm long) (Fig.2A,B);thecombsareinaverticalseries,connectedtoeach other byshort vertical pedicels,and connected laterally to the substrateleavesbyequallyshortlateralpedicels,exceptforthe downmostsmallerdevelopingcomb(Fig.3A).

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Fig.2.NestofP.langifromFLONA-Amapá,showingtheenvelopeAandC;substrateB;andcombsD;scales=1cm.

Fig.3. NestschemeofP.langifromFLONA-Amapá.A–lateralview;B–frontalview; arrow:nestentrance.

Combs:Thenesthasfourcombs(thelastoneverysmall, appar-entlyhavingjustbeeninitiated)ofthesamecolorastheenvelope, mostlydark-brownwithsomesmall,light-brownspots(Fig.2D). Thecombsaresemicirculartoovalinshape,withtheborder fac-ing thesubstrate beingroughly straight;the dorsal surfacesof thecombsareslightlyconcave(Fig.3A,B).Thelargertwoupper combs both have approximately 150 cells;the third comb has approximately70cells;thefourthcombhasonlythreeincomplete cells.Theﬁrstcombhasamajordiameterof3.1cmandaminor diameterof2cm;thesecondcombis3.3×2.1cm;thethirdcomb is2.2×1.8cm;thefourthcombisonlyapproximately5×4mm (Fig.2D).

Pedicels:Thepedicelsareratherflatincross-section,withthe lowersectiontendingtobewider;thefirstpedicel(connectedto thesubstrate)isdistinctlyoblique,andverywideandbuttress-like. Verticalpedicels2–3arelaterallyandbackwardlydisplaced,being closertothesubstratesideofthecomb(Fig.3A,B).Thelarger,more fullydevelopedcombswereconnectedtothesubstrateleavesby shortlateralpedicels;thefirstcombwasconnectedbytwosuch lateralpedicels;thesecondbythreepedicels;andthethirdcomb byonlyone;therecentlyinitiateddownmostcombhangsfromthe upperonewithoutconnectionstothesubstrate(Fig.3A).

Cellsize:Thecombcellsare2mmwideandabout5mmdeep. Thetotalnumberofcellswasestimatedtobeabout370.

Envelope:Theenvelopeconsistsofa singlesheet,apparently madeoflongﬁbers,predominantlydark-brown,withlight-brown narrowbands along theconstruction lines,giving it a streaked appearance; without ridges or corrugations (Fig. 2A–C). The nest waslighter brownin colorat thetime of collection, with

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yellowishstripes.Afewhoursaftercollectingit,however,the enve-lopebecamedarker,eventually reachingthetoneshowninthe photograph.Theenveloperesemblesaninvertedﬂask,widerat thetop,andgraduallydecreasingtothebase,whereittakesona rathershortbottleneckshape(Figs.2A,3A).Theentranceisa rela-tivelyshorttube,withanaperturediameterof1.5cm(Fig.3A).The envelopeisfragileandbrittle,differentfromotherPseudopolybia whichhaveitwithmoresuppleconsistency(P.difﬁcilis,P. com-pressa;seeWenzel,1998).Ithasatotallengthofabout9cm,and itslargestwidthis5cm.

Variations:Wewerenotabletoconﬁrmtheoriginalshapesof theenvelopesoftheothertwonestsofP.langi(evaluatedas pho-tographs)astheyhadbecomebrokenordeformed,althoughother aspectsofthearchitectureoftheRESEXCajarispecimen,suchasthe typeofnestingsubstrate,combarrangement,andenvelopecolor canbediscussed.

Positionrelativetosubstrate:ThenestcollectedintheRESEX Cajariwasconstructedunder(i.e.,ontheabaxialsurface)a sin-glerelativelylargeleaf(approximately11cmlongand5cmwide) whosepositionwasinferredtoberoughlyhorizontal(basedonthe relativeorientationofnestcells),withthenestbeingattachedto thesubstratedorsally.Thisindicatesthatthepositionofthecomb seriesrelativetothesubstratecanvaryinthisspecies,orthatitcan use(oradjustto)substrateswithdifferentorvaryingspatial orien-tations(likespeciesinAngiopolybia,Leipomeles,andParachartergus; seeWenzel,1991,1998).

Combs:Thenestcombsappeartobearrangedintwoadjacent verticalcolumns.Fivecombsareclearlyvisibleinthephotograph ofFig.1;thesomewhathiddenborderofasixthsubjacentcomb canbeseenunderthemostdistallyplacedstackofcombs(atthe bottomofthephotograph).Remainsoftheenvelopecanbeseen aroundthecombs,nearthemarginofthesubstrateleaf.

Itwasnot possibletoidentifyelementsofthemainvertical comb-to-combpedicelsinthisphotographofthefragmentednest, sothatthepositionsofthoseconnectionsareuncertain.Anaspect ofinterestinFig.1isthatthetwodetachedcombs(bothmeasuring ca.3.7cminmajordiameter)inthephotographseemtobelarger thanthosestillintheiroriginalpositions(2.6and3.2cminmajor diameter)–theattachedcombsnecessarilybeingolderthanthe detachedcombs.Thecombsinthisnestspecimenareaslightly largerthanthoseoftheFLONA-Amapánest,thetotalnumberof cellsbeingestimatedasca.700(abouttwiceasmanyasintheﬁrst specimendescribedhere,basedoncombnumberandarea),butthe ovalorroughlysemicircularcombsofbotharesimilar.Thewidths ofthecellsoftheCajarispecimenarealsoestimatedtobe sim-ilar(ca.2mm;basedoncombsthatappearaccordingtoaplane nearlyhorizontalwithrespecttothephotograph)tothoseofthe FLONA-Amapánest,althoughseveralofthecellsoftheformerare capped.

Envelope:Theenvelopesofthestudiednestsarequitesimilar, withconstructionlinesdelimitingdifferentiallycoloredbands.The proportionsofyellowandbrowncolorsmayvaryfromnesttonest. Unfortunately,essentiallynothingcanbesaidabouttheshapesof theenvelopesofthebroken/damagedspecimens.

Discussion

The FLONA-Amapá specimen appears to be the ﬁrst fully-developed undamaged nest of P. langi available for detailed architecturalstudy.Insomerespects,itverymuchresemblesthe nests of some basal epiponine genera rather than other Pseu-dopolybiaspecies,especiallywithregardstotheretentionofthe plesiomorphiccharacterofa“singlesheet”envelope(Andenaetal., 2007).Theshapeoftheenvelopewashighlyconvex(character17of Wenzel,1993),asinotherPseudopolybia,butwasshortlyprolonged

downwardstoformasmall“spout”(character10ofWenzel,1993), verysimilartothoseobservedinsomespeciesoftherelated gen-eraParachartergusandChartergellus(seeourFig.5;andRichards, 1978:Pl.3,Fig.23;Wenzel,1998:Fig.18AandB),andthe epipo-ninegenusAngiopolybia(Fig.5;andJeanne,1975;Wenzel,1998: Fig.23F).

Parsimoniousoptimizationoftheabovementionedcharacter “shapeofnestentrance”(correspondingtoWenzel’s1993 char-acter10) in a genuslevel phylogenetic treewithtopology like thatofWenzelandCarpenter(1994)andwithP.langiaddedas sister-grouptootherPseudopolybia(Fig.5,terminal Pseudopoly-bia*),resultedambiguouswithrespecttotheplesiomorphicstate inPseudopolybia(Fig.5,treenode3),aswellastotheancestor ofthecladePseudopolybia–Nectarinella(Fig.5,treenode2);i.e., underfastoptimization,thestateobservedforPseudopolybialangi resulted“primitive”inthatgenus(andinthewholecomponent Pseudopolybia–Nectarinella),withthealternativestateintheother threespecies(“entrancesimpleatlowestpoint”;seeWenzel,1998) beinginferredtobeasynapomorphyofthatspeciesgroup(Fig.5, terminalPseudopolybia*). Conversely,undertheslow optimiza-tionmode,theelongatednestentranceofP.langiistreatedasan independentdevelopmentwithrespecttosimilarshapesinrelated generalikeParachartergusandChartergellus.Whatever the opti-mizationmethodused,theverytypicalelongatednestentrance ofAngiopolybiapallensappearedasindependentlyderivedrelative tosimilarfeaturesintaxaofthePseudopolybia–Nectarinella com-ponent(actually,atleastforoneofthetwolarge-sizedspeciesof Angiopolybia,i.e.A.paraensis,thenesthasbeendescribedaslacking suchelongatedentrance;seeRichards,1978).

Thelateralattachmentofcombsbypedicelstoavertical sub-strateintheFLONAAmapánestappearstobesimilartospeciesof otherrelatedgenera,suchasParachartergusandChartergellus(see Fig.5).However,thisfeatureconcernsonlytotheappearanceof secondarycombsinanalready“ﬁnished”condition,which actu-allyhidesthefactthattheyareinitiatedthroughapedicelhanging fromthecombjustabove,onlybeingconnectedtothesubstrate whenthecombmargincomesclosetothelatter(seethe down-mostcombinFig.2D),Thisisthesameconditionobservedinother Pseudopolybia(Fig.4E),andAngiopolybia(Fig.4A,B),andsimilar tosomeAgelaia(Fig.5),andisdistinctfrommostParachartergus, Chartergellus(Fig.5),andpartofLeipomeles(actually,partofthis genuscorrespondingtoformergenusMarimbonda,andthespecies ofNectarinellaconstructsessilecombs;Fig.5)(seeJeanne,1975; Richards,1978;Wenzel,1998).

Parsimonious optimization of such a character (with three states: 0 – single pedicellate comb; 1 – multiple independent pedicellatecombs;2–multiplepedicellatestackedcombs;other conditionsasnon-applicable,andsettingPolistes,Ropalidia,Agelaia, andParachartergusaspolymorphic;seeJeanne,1975)onthe phylo-genetictreementionedaboveyieldsresultsambiguous(asbefore) astotheancestralconditioninthePseudopolybia–Nectarinellaclade (Fig.5,treenode2).Fastoptimizationmakes“multiplestacked combs”ancestraltothewholeepiponinecladeAgelaia–Clypearia (Fig.5,treenode1),whileslowoptimizationassignstothissame ancestralthecondition“multipleindependentpedicellatecombs”, thusimplyingthatthesimilarstatesobservedinAngiopolybiaand Pseudopolybiashouldbeconsideredindependentlyderived. Evi-dently,theseanalysesarepreliminary,andmaybereconsideredin futurebroad-spectrumstudiesofnestarchitectureinthePolistinae. The presence oftwo combstacks, asobserved in theCajari specimenofP.langiisapparentlyveryunusualamongNeotropical polistines,andadditionalspecimenswillbeneededtodetermine thefrequencyofthattypeofcombarrangement.Thatcondition hasbeen observed,however, in at leastone otherspecies that makes pedicellate multiple-stacked combs (see the abandoned nestremainsofAngiopolybiapallensinFig4C,D),anditisindeed

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A

C

E

1 F

D

B

2

1

3

2

Fig.4.Imagesofnestsortheirremains:(A)Angiopolybiapallens(enveloperemoved)1–downmostsecondarycombhangingbyapedicelfromtheonejustabove,2– adjustmenttoverticalorientationofcombseriesfromanobliquepedicel(andsubstrate);(B)A.pallensnest(envelopepartiallyremoved)adaptedtoaverticalsubstrate consistingoftwigsandleaves,1–sameasA-1;(C)remainsofA.pallensnestshowingtwostacksofcombs(arrowsindicatingsecondarypedicels),showinglateralfusion (onuppersideofthephotograph;3);(D)sameas(C),lateralview;(E)Pseudopolybiadiﬁcillis,envelopestructureandcombarrangement;(F)Leipomelesdorsata,2–combs atmarginalobliquesectorofthesubstrate–leafadjustingtoaverticalorientation.AllnestspecimensinMPEGcollection.

possiblethattherarityof thatsituationmaybea consequence of comb fusion, something that can be observed in Fig. 4C. A relationshipbetweenthisorganizational structure andthe con-structionoflargernestsseemsplausible,asdoublecombstacks wouldallowlargernumbersofcombswithoutcreatingalonger singleverticalseries(whichwouldpresumablybemoreunstable whenattacheddorsallytothesubstrate).Jeanne(1975)discusses indetailtheoccurrenceof,anddifferentimplicationsof,thosetwo combarrangementmodes,i.e.,multipleindependentcombsversus multiplestackedcombs.

Basedonavailablespecimens, thenestsofP.langiappearto have the capacity to adapt to substrates with differing spatial orientations(i.e.,thenestscanbeattachedtoeitherlaterallyor dorsallypositionedsubstrates),whilethecombseriesstill main-tainsaverticalorientation.Adjustmentstosuchdifferentkindsof substratescan beobserved inthenestsofa singlespecies(e.g. Angiopolybiapallens,Fig.4A,B),oreveninasinglenest,incases

ofcurved surfacesor surfacesthatmay changespatial orienta-tionwithtime(i.e.,onleaves;seenestofLeipomeles dorsatain Fig.4F).

ThenestsofP.langidescribedinthispapershowthatthe sim-plemonolayerenvelopeandaspout-shapednestentrancearethe maindifferencesinrespecttootherPseudopolybiaspecies. How-ever,themannerofaddingsecondary combsis thesameinall ofthosespecies,witheachnewsecondarycombbeinginitiated fromapedicelhanging fromthecombjustaboveit.In P.langi, lateral comb-substrate pedicels are added in cases of vertical substrates.

Conﬂictsofinterest

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Polybia Epipona Protonectarina Brachygastra Chartergus Asteloeca Metapolybia Clypearia Synoeca Charterginus Protopolybia Pseudopolybia Apoica Agelaia P. langi Angiopolybia Parachartergus Chartergellus Leipomeles Nectarinela Marimbonda nest astelocyttarous nest mainly phragmocyttarous (or envelope flat)

(or envelope flat)

*

(oneof several forms)

?

1

2 3

Fig.5. PhylogeneticrelationshipsforthegeneraofEpiponini,adaptedfromWenzelandCarpenter(1994);omittingOccipitaliaandSynoecoides;Marimbondaismaintainedand representedassister-groupofLeipomeles;P.langiaddedassister-groupofotherPseudopolybiaspecies(terminalmarkedwithan*).Schematicrepresentationsofarchitectural typesadaptedfromWenzel(1991).“astelocyttarous”:sessilecombwithcellsconstructeddirectlyonsubstrate,coveredbyanenvelope;and“phragmocyttarous”:multiple stackedcombswithcellsofsecondarycombsconstructedontheenvelopeofprecedingcomb(seeRichards,1978;Wenzel,1998);aquestionmark(?)indicatesuncertainty ontheshapeandpositionofnestentranceofthe“Cajarinestspecimen”ofP.langi.

Acknowledgements

WearegratefultothePPBioBiodiversityResearchProgramand toIEPAforfacilitatingthelogisticsoftheexpeditiontothe FLONA-Amapá.Wealsothanktwoanonymousreviewersforcorrections andimprovementstotheoriginalmanuscript.

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