Ant fauna associated with Microgramma squamulosa (Kaulf.) de la Sota (Polypodiaceae) fern galls

RevistaBrasileiradeEntomologia63(2019)101–103

REVISTA

BRASILEIRA

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Entomologia

Short

Communication

Ant

fauna

associated

with

Microgramma

squamulosa

(Kaulf.)

de

la

Sota

(Polypodiaceae)

fern

galls

Marcelo

Guerra

Santos

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_Gabriela

_Fraga

_Porto

_,

_Isabella

_Rodrigues

_Lancellotti

_,

_Rodrigo

_M.

_Feitosa

b_{UniversidadeFederaldoParaná,DepartamentodeZoologia,LaboratóriodeSistemáticaeBiologiadeFormigas,Curitiba,PR,Brazil}

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Articlehistory:

Received18September2018 Accepted26February2019 Availableonline26March2019 AssociateEditor:RicardoSolar Keywords: Ecosystemengineers Fern–insectinteractions Myrmecophily Pteridophytes

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Gallsareneoformedplantstructurescreatedbycellhyperplasiaandhypertrophyinducedbyanumber oforganisms,especiallyinsects.Afteradultinsectshatch,senescentgallsmayremainonthehostplant andbeoccupiedbyasuccessionoffauna,themostimportantanddominantbeingants.Thisstudyaimed atcharacterizingtheantfaunasuccessorofstemgallsinducedbymicrolepidopterainMicrogramma squamulosa(Kaulf.)delaSota(Polypodiaceae).Fourcollectionswerecarriedoutinthemunicipalityof NovaFriburgo,RiodeJaneirostate,Brazil.Thegallswerepackedinplasticbagsandtakentothe labora-tory.Antswereeuthanizedandconservedin70◦GLalcoholandlateridentified.Atotalof49stemgalls werecollectedandanalyzed,15containingmicrolepidopteragallerlarvae,oneaparasitoidwaspand 33withoutthemicrolepidopteraorparasitoid(67%).Twelveofthesegalls(39%)containedants.Sixant specieswererecorded(Camponotuscrassus,Crematogastercurvispinosa,Crematogastersericea, Procryp-tocerussampaioi,Tapinomaatriceps,andWasmanniaauropunctata),allnativetoBrazil.Antoccupation inM.squamulosaseemstobeassociatedwithsenescentgallsduetohatchingofthegallerinsect,which leavesaholethatallowsantstocolonizeit,inotherwords,anopportunisticdomatia.Senescentgalls resultingfromthedeathofgallerinsectsdonotseemtofacilitateantoccupation.

©2019PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeEntomologia.Thisisan openaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/

).

Gallsareneoformedplantstructurescreatedbycellhyperplasia andhypertrophy.Theycanbeinducedbyorganismssuchasfungi, bacteria,nematodes,mitesandinsects;however,thelasttwostand outforthegalldiversitytheyinduceinplants(Mani,1964;Raman, 2007;Shorthouseetal.,2005).Inducersestablishaparasitic rela-tionshipwiththehostplant,manipulatingitsmetabolism(Mani, 1964;Raman,2007).

Galler insects are among themost specialized and sophisti-cated herbivores,considered ecosystem engineers,due to their abilitytostructurallyalterleaves,stems,roots,flowersorfruits andformnewhabitats(Jonesetal.,1994;WrightandJones,2006; Cornelissenetal.,2016).Insectgallsareinducedbyoviposition and/ordevelopmentoftheirlarvaein planttissues (Shorthouse etal.,2005).Afteradultinsectshatch,senescentgallsmayremain onthehostplantandbeoccupiedbyasuccessionoffauna,themost importantanddominantbeingants(Mani,1964;Almeidaetal., 2014).Senescentgallsprovideshelterandanestingsiteformany

∗ Correspondingauthor.

E-mail:marceloguerrasantos@gmail.com(M.G.Santos).

antspecies,mainlyarborealants(Santosetal.,2017;Almeidaetal., 2014).However,inthegaller-fern-antsystem,theimportanceof antstothegall/plantremainsunclear.

Inadditiontoshelter,somegallsareafoodsourceformany ant species. Moreover, certain galls induced by Eriophyidae, Homoptera,Hymenopteraand Dipteramayproducehoneydew, which attracts flying insects and ants (Mani, 1964; Washburn, 1984).

Because ferns do not have flowers, most researchers have longignoredthepotentialoffern-animalinteractions(WatkinsJr. etal.,2008).However,theseinteractionsmayoccurviaherbivory (Mehltreter,2010),withthepresenceofdomatia(Gómez,1974), leafnectaries(Kopturetal.,1982), crypticity(SantosandWolff, 2015)andgalls(Santosetal.,2019).

Although they are more frequent in spermatophytes, galls canalsobefoundin fernsandlycophytes (Santoset al.,2019). In Brazil, galls have been recordedon 16 fern species induced by mites (Eriophyidae) and insects of the orders Lepidoptera, Thysanoptera, Hemiptera and Diptera, the last being the most frequentgallerrepresentedbytheCecidomyiidaefamily(Santos andMaia,2018).

https://doi.org/10.1016/j.rbe.2019.02.004

0085-5626/©2019PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeEntomologia.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

102 M.G.Santosetal./RevistaBrasileiradeEntomologia63(2019)101–103 2 cm 0.5 cm 0.5 cm 0.5 cm

A

B

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Fig.1. (A)StemgallonMicrogrammasquamulosa(arrow);(B)Ecdyseofthemicrolepidopteragallerthatemergedfromthegall(arrow);(C)holeleftbytheexitinggaller (arrow);(D)sectionedgallexhibitingantslivinginside.

GallshavebeenrecordedinthreeMicrogrammaC.Presl (Poly-podiaceae) species, M. squamulosa (Kaulf.) de la Sota and M. vacciniifolia(Langsd.&Fisch.)Copel.inBrazil(Santosand Maia, 2018),andM.percussa(Cav.)delaSotainCostaRica(Santosetal., 2019).Moreover,severalspeciesofthisgenusofferncontain doma-tia(Mehltreter,2010).

TwogallmorphotypeswererecordedinMicrogramma squamu-losa,aneotropicalepiphytefern(Rochaetal.,2014).Oneisastem gall(Fig.1A)inducedbyTortrimosaicapolypodivoraBrown& Baix-eras,2004(Tortricidae:Lepidoptera) (Krausetal., 1993;Brown etal.,2004),andtheotheraconicalleafgallinducedbya yet-to-be-identifiedCecidomyiidae(Diptera)(SantosandMaia,2018).Both morphotypesoccurinthestatesofRiodeJaneiroandSãoPaulo, Brazil(SantosandMaia,2018).Earlierfieldworkfoundants occu-pyingsenescentgallsofM.squamulosa(Fig.1D).Assuch,thisshort communicationaimsatcharacterizingtheantfaunasuccessorof stemgallsinducedbyTortrimosaicapolypodivorainM.squamulosa. ThegallswerecollectedinaforestareaoftheNovaFriburgo Coun-tryClub(22◦1731.6S42◦3225.1W)andPrac¸adoSuspiro(Suspiro Square)(22◦1645.8S42◦3208.9W),bothlocatedinthe munic-ipalityof NovaFriburgo,Rio deJaneirostate,Brazil.Collections werecarriedoutinthedry(April2016andJune2017)andrainy seasons(October2017andFebruary2018),accordingtoBarbieri’s classification(2005)fortheBrazilianSoutheastregion.

We performed an active search of trees at the two col-lection sites and all galls found were packed in plastic bags and sorted in the laboratory. All biological voucher material wasdeposited in theherbariumof theFaculdadede Formac¸ão de Professores da Universidade do Estado do Rio de Janeiro (RFFP)and the Padre Jesus Santiago Moure Entomological Col-lection,UniversidadeFederaldo Paraná,DepartmentofZoology (DZUP).

Thegallsweresectionedinthelaboratoryandallants euth-anizedandfixedin70◦ GLalcohol. TheywereidentifiedbyDr. RodrigoM.Feitosa,intheLaboratoryofSystematicsandAntBiology atUniversidadeFederaldoParaná.

Atotalof49stemgallsfromM.squamulosawerecollectedand analyzed,15containingmicrolepidopteragallerlarvae,onea par-asitoidwaspand 33withoutthemicrolepidoptera orparasitoid (67%).Twelveofthesegalls(36%)containedantsandtwenty-one wereempty.

Six ant species, belonging to five genera were recorded (Crematogaster, Camponotus, Procryptocerus, Tapinomaand Was-mannia), allnativetoBrazil (Table1).Except forCrematogaster sericea,alltheantspeciesestablishednestsinsidegalls,withboth immatureandsexualindividualspresent,indicatingtheyarebeing usedbycoloniesforshelter.Furthermore,allantsthatoccupied gallsarearboreal,whichwasexpectedbecausethegallswerefound inan epiphyticfern(M.squamulosa).Inrelationtofoodhabits, alltheantspecies observedhere canbeconsideredgeneralists (Baccaroetal.,2015).

ThegeneraCamponotusandCrematogasterareamongthemost frequent gall successors in angiospermgalls (Mani, 1964) and inhabitantsofMicrogrammaspp.(Gómez,1974)andLecanopteris spp.domatia(Gay,1993),bothgenerabelongingtothefamily Poly-podiaceae.

The species with the highest frequency in galls were Camponotus crassus and Procryptocerus sampaioi, occurring in three galls each, and those with the greatest density were Tapinoma atriceps and Wasmannia auropunctata (Table 1). Cre-matogastercurvispinosa was only recordedin therainy season, C. sericea and W. auropunctata only in the dry season, and C. crassus, P. sampaioi and T. atriceps were found in both seasons(Table1).

M.G.Santosetal./RevistaBrasileiradeEntomologia63(2019)101–103 103

Table1

AntsrecordedinsenescentstemgallsofMicrogrammasquamulosa(Kaulf.)delaSota.Numberofgallswithants(n=12).Numberofants(n=399).

Species Origin Occurrence

(No.ofgalls) Absolute frequency(%) Numberofants pergall Absolute density Relative density(%) Season Crematogastercurvispinosa Mayr,1862

Native(Longino,2003) 2 16.67 29.5±14.8 59 14.79 Rainy

CrematogastersericeaForel, 1912

Native(Longino,2003) 1 8.33 4 4 4 Dry

CamponotuscrassusMayr, 1862

Native(Fernández&Sendoya,2004) 3 25.0 14.6±6.7 34 8.52 Dryandrainy Procryptocerussampaioi

Forel,1912

Native(Baccaroetal.,2015) 3 25.0 8.6±6.7 8.6±6.7 6.52 Dryandrainy

TapinomaatricepsEmery, 1888

Native(Shattuck,1994) 2 16.67 67.5±88.4 135 33.83 Dryandrainy

Wasmanniaauropunctata (Roger,1863)

Native(LonginoandFernández,2007)1 8.33 141 141 35.34 Dry

AccordingtoMehltreter,2010,interactionsbetweenfernsand ants canbe neutral ormutualistic. Thepresence of domatia in epiphyticfernsofthegenusMicrogramma,subgenusSolanopteris (Gómez, 1974; Lellinger,1977), aswellas inLecanopteris (Gay, 1993),mayestablishamutualisticrelationwithanumberofant species.However,insomesituations,antscanbeopportunistsand inhabitorgancavities(primarilystemsandpetioles)offerns pro-ducedbytheactionofherbivores,whichMehltreteretal.(2003) referredtoasopportunisticdomatia.

Thepossiblenutritionalbenefitsforplantspromotedbythese ants,especiallynitrogen,remainstobeassessed.Forexemple,in thetissuesofanepiphytefern[Antrophyumlanceolatum(L.)Kaulf. –Pteridaceae],WatkinsJr.etal.(2008)foundhighlevelsof nitro-genfromwasteproducedbythenestsofantsassociatedwiththis plant.Theseauthorssuggestthatanimalsmayprovide substan-tialnutritionalbenefitstoplantswithlittleornoinvestment,not requiringspecializedstructuressuchasdomatiaorleafnectaries. Thus,thehypothesisthatthenestsofgall-dwellingantssupply nutritionalsupporttotheepiphytefernM.squamulosahasyetto betested.

InM.squamulosa,antoccupationseemstobeassociatedwith senescentgallscausedbygallerinsecthatching(Fig.1B),which leavesa hole(Fig.1C)thatallows antstoenter andcolonizeit, inotherwords,anopportunisticdomatia(sensuMehltreteretal., 2003).Senescentgallsduetodeathofgallerinsectsseemnotto facilitatethisoccupationbyants.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

TheauthorswouldliketothankTheNationalCouncilfor Scien-tificandTechnologicalDevelopment(CNPq),CarlosChagasFilho ResearchSupportFoundationofRiodeJaneirostate(FAPERJ),and IncentiveProgramforScientific,TechnicalandArtisticProduction ofRiodeJaneiroStateUniversity(PROCIENCIA-UERJ)forfunding. WearealsogratefultoAndersondosSantosPortugal,ArthurFlores RibeiroandMarianaFernandesdaRochafromtheUERJBiodiversity TeachingandResearchLaboratoryforhelpindatacollection.

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