Sharing of termites (Blattodea: Isoptera) between sugarcane matrices and Atlantic Forest fragments in Northeast Brazil

RevistaBrasileiradeEntomologia63(2019)108–111

REVISTA

BRASILEIRA

DE

Entomologia

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

Short

Communication

Sharing

of

termites

(Blattodea:

Isoptera)

between

sugarcane

matrices

and

Atlantic

Forest

fragments

in

Northeast

Brazil

Alane

Ayana

Vieira

de

Oliveira

Couto

_,

_Martín

_Alejandro

_Montes

_,

Rozzanna

Esther

Cavalcanti

Reis

de

Figueirêdo

Chaves

_,

_Alexandre

_Vasconcellos

a_{UniversidadeFederaldaParaíba,DepartamentodeSistemáticaeEcologia,LaboratóriodeTermitologia,JoãoPessoa,PB,Brazil} b_{UniversidadeFederalRuraldePernambuco,DepartamentodeBiologia,Recife,PE,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Received14October2018 Accepted4February2019 Availableonline18February2019 AssociateEditor:M.ElianaCancello Keywords: Conservation Feedinggroups Isolation Speciesdispersal Speciesrichness

a

b

s

t

r

a

c

t

TheAtlanticForestofSouthAmericaisoneofthemostdegradedtropicalforestsandthecultivationof sugarcaneisconsideredoneofthemaincauses.Inhumidforeststermitesstandoutwithregardtotheir abundanceandfunctionalimportance.Thepresentstudyaimedtocomparetermiteassemblagesof frag-mentsoftheAtlanticForestwiththatofthesugarcanematricesthatsurroundthem.Collectionswere performedintwosugarcaneplantationsinNortheastBrazil.IneachplantationafragmentofAtlantic For-estandanadjacentsugarcanefieldweresampledusingastandardizedtermitesamplingprotocol.Atotal of39speciesand302encounterswererecorded.Speciesrichness,relativeabundanceandcomposition differedsignificantlybetweenforestsandthematrices,withthepresenceofexclusivespeciesineach environment—25intheforestsandseveninthematrices.Soilfeedingspeciesofthesubfamily Apicoter-mitinaeandspeciesofopenareaswerefoundinthematrices.Therewasamarkeddifferencebetween theassemblagesofthematrices,possiblyduetosoilcharacteristics.Themajorityofthespeciesfoundin thematricesdonotcausedamagetothecrop,butinsteadactintheprocessesofsoildecompositionand formation,therebycontributingtoincreasedproductivity.

©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

TheAtlanticForestofSouthAmericaisconsideredoneofthe

largest biodiversity repositories on the planet and one of the

mostdegradedtropicalforests(Galindo-Lealand Câmara,2005;

Marchese,2015).ItisestimatedthatthecurrentareaoftheAtlantic

Forestrepresentsjustover 11%of itsoriginalcoverage(Ribeiro

etal.,2009)andsugarcaneisoneofthecropswhoseexpansion

hasbeen identified asa main causeof the current scenario of

degradation.IntheNortheastBrazil,sugarcanematrices

surround-ingremnantsofAtlanticForestcompriseacommonfeatureofthe

landscape(Rantaetal.,1998).Atotalof866.5thousandhectares

ofsugarcanewasharvestedinthisregionin2016/2017(CONAB,

2017).

Inhumidforests,suchastheAtlanticForest,termitesstandout

withregardtotheirabundanceandfunctionalimportance.Theyare

importanteusocialorganismsinthedynamicsoftheecological

pro-cessesrelatedtoenergyflowandthenutrientcyclingofvegetable

necromass(Vasconcellos,2010;Vasconcellos andMoura,2010).

Theconversionofnaturalareastomonoculturesandtheselective

∗ Correspondingauthor.

E-mail:[email protected](A.A.Couto).

cuttingof treesarerecognizedasbeingresponsibleforreduced

speciesrichnessandabundanceoftermites,aswellaschangesin

theproportionoffeedinggroups,withsoilfeedingspecies(feeding

groupsIIIandIVaccordingtotheclassificationofDonovanetal.,

2001)beingthemostsensitivetoenvironmentalchanges(Bandeira

andVasconcellos,2002;Eggletonetal.,1996).

Inthiscontext,theobjectiveofthisstudywastocompare

ter-mite assemblagesof AtlanticForest fragments withthat ofthe

sugarcanematrices that surroundthem, seekingtoevaluate(i)

speciesrichness,relativeabundanceandthecompositionand

dis-tributionoffeedinggroupsinmatricesandforestfragments;and

(ii)thehabitsandpest-status,basedonliteraturerecords,ofthe

termitespecieslivinginthesugarcanematrices.

Theresearchwascarriedoutintwosugarcaneplantationsin

NortheastBrazil.Thefirst,UsinaSãoJoão,islocatedinthe

munici-palityofSantaRita,LitoralCentrooftheParaíbastate(07◦0945.8S,

35◦0351.5W),wherecollectionswerecarriedoutbetween

Octo-ber2014andApril2015.Themeanannualtemperatureis25.2◦C,

themeanrelativehumidityoftheairis83%andannualrainfallis

2193.6mm.Duringthefieldworktherainfallvariedbetween13.3

and40.7mm(INMET,2019).Thesoiloriginatesfromclay-sandy

sedimentsandis classifiedas Red-yellowArgisolwithsandyto

https://doi.org/10.1016/j.rbe.2019.02.001

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

A.A.Couto,M.A.Montes,R.E.Chaves,etal./RevistaBrasileiradeEntomologia63(2019)108–111 109

loamysandytexture,andisdeepandwithlowfertility(Santana,

1987). The vegetation of the forest fragments is classified as

semideciduousseasonalforestcharacterizedbyamixtureof

sec-ondaryAtlanticForestwithisolatedareasofopenCerradocalled

‘tabuleiros’(Rodriguesetal.,2013).Thesecondplantation,Usina

SãoJosé,islocatedinthemunicipalityofIgarassu,MataNorteof

thePernambucostate(7◦497S,35◦0045W),wherecollections

werecarriedoutbetweenSeptember2015andJanuary2016.The

meanannualtemperatureis26.3◦C,themeanrelativehumidityof

theairis83.9%andannualrainfallis1455.6mm.Duringthefield

worktherainfallvariedbetween16.6and91.8mm(INMET,2019).

ThesoiloriginatesfromsedimentsoftheBarreiraGroupandis

clas-sifiedasRed-yellowLatosolwithtexturevaryingfromsandyclay

toclayey,andisdeepandwithlowtomediumfertility(Koffler

etal.,1986).Thevegetationofthestudiedfragmentisclassified

asSemidecidualSeasonalLowlandForest(ThomasandBarbosa,

2008).Thesugarcanevarietycultivatedinthestudyareasofthetwo

plantationswasRB92579.Theareashadnotbeenreceiving

pesti-cidesforatleast18monthsandhadnotexperiencefiresforatleast

sixmonths.

ThecollectionprotocolproposedbyCancelloetal.(2014)was

applied in each area, which consistsof the demarcation of six

65m×2mtransectscontainingfive5m×2mplotsspacedat10m.

The transects were established at least 30m from the

planta-tion/forestborders.Thecollectiontimeateachplotcorresponds

toasamplingeffortof1hourbyperson.Duringthistime,termites

weresearchedforinallpossiblemicrohabitatsandthenspecimens

werecollectedforspeciesidentificationandclassificationby

feed-inggroupaccordingtotheproposalofDonovanetal.(2001).This

protocolwasoriginallydevelopedforthecollectionoftermitesin

tropicalforests,buthassincebeenappliedinopenecosystemssuch

asCaatinga(Vasconcellosetal.,2010;Vianaetal.,2014).Voucher

materialwasdepositedintheColec¸ãodeIsopteraofUniversidade

FederaldaParaíba.Theobservedspeciesrichnessandnumberof

encounterswereobtainedforeachforestfragmentandsugarcane

area,thelatterofwhichwasusedasanindicatorofrelative

abun-dance(Cancelloetal.,2014).

Assemblageswereorderedusingnon-metricmultidimensional

scaling(nMDS)withJaccardsimilarity.Differencesinthe

compo-sitionofspeciesandfeedinggroupsbetweenforestandadjacent

Table1

Observedspeciesrichness,numberofencountersandfeedinggroupinAtlanticforestfragmentsandsugarcanefieldsinNortheastBrazil.N,numberofplotsinwhicha specieswasencountered;Sobs,observedrichness;Us.,Usina.AF,AtlanticForest;S,sugarcanefield;FG,feedinggroup.

Family/subfamily/species Us.SãoJoão Us.SãoJosé

NAF NS NAF NS FG

Rhinotermitidae

Heterotermeslongiceps(Snyder,1924) 4 – 3 – I

Termitidae Apicotermitinae Apicotermitinaesp.1 – – 1 – III Apicotermitinaesp.2 – – 2 – III Apicotermitinaesp.3 – – – 1 III Apicotermitinaesp.4 – – – 1 III Anoplotermessp.1 – – 16 – III Anoplotermessp.2 10 – 5 9 III Anoplotermessp.3 1 – 8 2 III Aparatermessp.1 – – – 4 III Aparatermessp.2 1 – – – III Aparatermessp.3 – – – 4 III Grigiotermessp. 1 – 1 – IV Tetimatermessp. – – 1 – IV Nasutitermitinae Atlantitermessp. 1 – – – IV

Diversitermesdiversimiles(Silvestri,1901) 6 – 3 – II

Nasutitermescallimorphus(Mathews,1977) 10 – 10 – II

Nasutitermescorniger(Motschulsky,1855) 7 – 8 – II

Nasutitermescoxipoensis(Holmgren,1910) – – – 10 II

Nasutitermesephratae(Holmgren,1910) – – 10 – II

NasutitermesgaigeiEmerson,1925 – – 2 – II

Nasutitermesjaraguae(Holmgren,1910) 1 – – – II

Nasutitermesmacrocephalus(Silvestri,1903) 2 – – – II

Nasutitermesobscurus(Holmgren,1906) 3 – – – II

Nasutitermessp. – – 1 – II

Velocitermesvelox(Holmgren,1906) 1 – 4 – II

Syntermitinae

Embiratermesneotenicus(Holmgren,1906) 6 – – – II

EmbiratermesparvirostrisConstantino,1993 7 – – – III

Labiotermeslabralis(Holmgren1906) 7 – 4 – IV

Silvestritermesholmgreni(Snyder,1926) 3 – 3 – II

Syntermesgrandis(Rambur,1842) – – – 4 II

SyntermesnanusConstantino,1995 – – – 2 II

Termitinae

AmitermesamiferSilvestri,1901 7 2 1 – II

AmitermesnordestinusMélo&Fontes2003 – 16 – – II

Cavitermestuberosus(Emerson,1925) 1 – 1 – III

CylindrotermessapirangaRocha&Cancello,2007 1 18 – 4 II

MicrocerotermesindistinctusMathews,1977 23 – 15 1 II

NeocapritermesopacusHagen,1858 2 – 2 14 III

Orthognathotermessp. 1 – – – IV

TermesmedioculatusEmerson,1949 3 – – – III

Sobs 24 3 21 12

110 A.A.Couto,M.A.Montes,R.E.Chaves,etal./RevistaBrasileiradeEntomologia63(2019)108–111 0.2 0.0 -0.2 -0.2 -0.4 -0.2 0.0 0.2 -0.2-0.1 -0.1 0.0 0.0 0.1 0.1 0.2 0.2 0.3 Stress:0.11 Stress:0.28 nMDS axis 1 nMDS axis 2 nMDS axis 2 nMDS axis 1

A

B

Fig.1.Non-metricmultidimensionalscalingfortermiteassemblagesoftwoAtlantic Forestfragmentsandadjacentsugarcaneplantations.UsinasãoJoão(A)andUsina SãoJosé(B).䊉,AtlanticForest.,sugarcanefield.

24 20 16 12 8 4 20 40 IV III II I 60 80 100 120 Number of encounters Species r ichness 0 AF AF AF AF

Us. São João Us. São José Us. São João Us. São José

S S S S

0

A

B

Fig.2.Speciesrichness(A)andnumberoftermiteencounters(B)perfoodgroupof twoAtlanticForestfragmentsandadjacentsugarcanefieldsoftwoplantationsin NortheastBrazil.Us.,Usina;AF,AtlanticForest;S,sugarcanefield;I,feedinggroupI; II,feedinggroupII;III,feedinggroupIII;IV,feedinggroupIV(Donovanetal.,2001).

matrixweretestedthroughnon-parametricpermutationanalysis

ofvariance(PERMANOVA)with9999permutations.Allofthese

analyseswereperformedusingPASTv.3.20 software(Hammer

andHarper,2006).

Atotalof39speciesand302encounterswererecorded,with31

speciesand210encountersrecordedfortheAtlanticForest

frag-ments,14 speciesand 92encountersin thesugarcaneareas. In

UsinaSãoJoão(fragment+matrix)wererecorded25speciesand

145encounters(Table1).Atotalof109encountersand24species

wererecordedintheAtlanticForestfragment,22ofwhichwere

exclusivetothisenvironment,while36encountersandonlythree

specieswererecordedin thesugarcanematrix,withAmitermes

nordestinusSilvestri,1901,beingexclusivetothisenvironment.In

UsinaSãoJosé(fragment+matrix),29speciesand157encounters

wererecorded(Table1).Atotalof101encountersand21species

wererecordedintheAtlanticForestfragment,ofwhich17were

exclusivetothisenvironment,while56encountersand12species

wererecordedinthesugarcanematrix,eightofwhichwere

exclu-sivetothisenvironment.

ThenMDSindicatedthatthestructure oftheassemblagesof

theforestfragmentandthematrixdifferedinthebothplantations

(Fig.1).ThePERMANOVAshowedthatthespeciescomposition

dif-feredsignificantlyinthetwoplantformations,bothforUsinaSão

João(F=20.2,p<0.05),andforUsinaSãoJosé(F=9.93,p<0.05).

TheAtlanticForestfragmentshadsimilarresultsregardingthe

structureofthefeedinggroups,withagreaternumberofspecies

andencountersrecordedforfeedinggroupII,followedbyfeeding

groupsIII,IVandI.However,inthematrixofUsinaSãoJoãoonly

feedinggroupIIwasrecorded,whileinthematrixofUsinaSãoJosé

feedinggroupsIIandIIIwererecorded(Fig.2).

Thisis thefirstrecordofspecies belongingtothesubfamily

ApicotermitinaeinsugarcanefieldsinNortheastBrazil.Thereis

arecordofthissubfamilyintheSoutheastBrazil,butthespecies

wasonlyidentifiedtothesubfamilylevel(Junqueiraetal.,2015).

AllofthespeciesfoundinsugarcanefieldsofUsinaSãoJoãobelong

togenerathatwerepreviouslyassociatedwithsugarcaneinthe

NortheastBrazil(Guagliumi,1972/73;NovarettiandFontes,1998;

Mirandaetal.,2004).

InUsina SãoJoão,thespeciesrichness oftheAtlanticForest

fragmentwaseighttimesgreaterthanthatrecordedinthe

sugar-canefield,whileinUsinaSãoJoséthespeciesrichnessintheforest

fragmentwasapproximately1.7timesgreater.Itisimportantto

notethattheassemblagesfoundinthematricesdonotcorrespond

exactlytoasubgroupoftheassemblagesfoundin theadjacent

forestfragments,andpossessaconsiderablenumberofexclusive

species,which,onalandscapescale,representsanincreaseintotal

speciesrichness.Otherstudiescomparingassemblagesoftermites

betweenforestfragmentsandnearbyplantationsalsorecordeda

decreaseinspeciesrichnessandabundance,aswellasdifferences

intaxonomicandfeedinggroupcomposition(Attignonetal.,2005;

Bassetetal.,2016;Eggletonetal.,1996).Anotherfactorthatmay

havecontributedtothedecreaseintermitespeciesrichnessinthe

sugarcanematrixisthetypeofmanagementperformed.The

prac-ticeofpreharvestburningisstillcommoninsugarcanecultivation

andreducestheamountoforganicmatterinthesoilcomparedto

greenormechanizedharvest,aswellassignificantlyreducingthe

abundanceofarthropods(Sajjadetal.,2012;Wiedenfeld,2009).

Thelowerspeciesrichnessandabundance, coupledwiththe

simplificationofthestructureofthefeedinggroups,inthematrices

inrelationtothoserecordedintheAtlanticForestfragments

indi-catesthatthematrixfunctionsasafilterforthegreatmajorityof

speciesbutfavorsthepermanenceofotherpopulations,especially

species of openareas suchas Amitermes nordestinus,

Nasutiter-mes coxipoensis (Holmgren, 1910), Syntermes grandis (Rambur,

1842)andSyntermesnanusConstantino,1995(Alvesetal.,2011;

Constantino,1995;Cunha andMorais,2010;Garcia etal.,2006; Mathews,1977).

InthesugarcanefieldofUsinaSãoJoão,allofthespecieswere

includedinfeedinggroupII,whileinthesugarcanefieldofUsina

SãoJosé,ofthe12speciesrecorded,sixofthesubfamily

Apicoter-mitinaeand thespecies Neocapritermesopacus (Termitinae)are

includedinfeedinggroupIII.ThespeciesS.grandisandS.nanus,

despitebeinginfeedinggroupII,haveastrongconnectionwith

thesoilsincetheirnestsaresubterranean(Constantino,1995).

Thespeciescompositionsofthetwosugarcanefieldswerequite

different.Thisdifferencemayberelatedtoagreateramountof

clayinthesoilofUsinaSãoJosé(seethedescriptionoftheareas).

Clayis akeycomponent forensuringstructuralstability of

ter-mitenests(Jouquetetal.,2004).Therefore,sandysoilsmakenest

buildingdifficult and decreasegallery stability (Lee and Wood,

1971).ThetermiteassemblagesoftworestingaareasintheParaíba

state,whosesoiltextureresemblesthatofthesoiloftheUsinaSão

Joãosugarcanefield,hadalowoccurrenceofspeciesofthe

sub-familyApicotermitinae,whichwasassociatedwithsoilproperties

(Vasconcellosetal.,2005).Thus,thedifferencesfoundindicatethat

evenmatricesformedbythesamemonoculture,includingthesame

varietyofsugarcaneandmanagementpractices,cansupportvery

differentassemblages.

Althoughtermitesareconsideredimportantpestsofthe

sug-arcane crop in Northeast Brazil (Novaretti and Fontes, 1998),

publications thatstudytermiteassemblages insugarcanefields

inthisregionaregenerallyscarceandrelativelyold(Guagliumi,

1972/73;Mirandaetal.,2004;NovarettiandFontes,1998).Inthe

presentresearch,thespeciesS.grandisandS.nanuswereobserved

damagingtheleavesofplantsstillindevelopment,whiletheother

specieswerenotobservedcausinginjuriestotheplantsandwere

feedingonstrawororganicmatterinthesuperficiallayersofthe

soil,thuscontributingtotheprocessofnutrientcycling.

Thereisadrasticsimplificationofthetaxonomicandfunctional

structuresoftermiteswiththeconversionofAtlanticForestinto

sugarcanefield.Ontheotherhand,thematrixisnotacompletely

inhospitableenvironmentforthepresenceoftermitesandisable

tomaintainspecies that arenot foundin theadjacentAtlantic

Appar-A.A.Couto,M.A.Montes,R.E.Chaves,etal./RevistaBrasileiradeEntomologia63(2019)108–111 111

ently,mostofthespeciesfoundinthematrixdonotdamagethe

crop,andinsteadfeedonstrawandorganicmattercontainedinthe

superficiallayersofthesoil,thuscontributingtonutrientcycling.

Variationinsoiltype,especiallytheamountofclay,ofthesame

monocultureapparentlycaninfluencethecompositionoftermite

assemblages,andalterthepermeabilityofthematrix.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

TheauthorsthankUsinaSãoJoãoandUsinaSãoJoséfor

autho-rizingthefieldactivitiesintheirfacilitiesandthetraineesofthe

termitologylaboratoriesofUFPBandUFRPEforassistanceduring

fieldactivities.

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