Morphological traits, allometric relationship and competition of two seed-feeding species of beetles in infested pods

REVISTA

BRASILEIRA

DE

Entomologia

Biology,

Ecology

and

Diversity

Morphological

traits,

allometric

relationship

and

competition

of

two

seed-feeding

species

of

beetles

in

infested

pods

Jessica

A.

Silva,

Angelo

B.

Monteiro,

Laís

F.

Maia,

Lucas

D.B.

Faria

UniversidadeFederaldeLavras,DepartamentodeBiologia,SetordeEcologiaeConservac¸ão,Lavras,MG,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received2February2017

Accepted11April2017

Availableonline25April2017

AssociateEditor:LucasKaminski

Keywords: Merobruchusterani Statormaculatopygus Senegaliatenuifolia Bruchinae Negativeallometry

a

b

s

t

r

a

c

t

Pair-wisecompetitionproducesasymmetricconsequencesfortheinteractingspecies,resultingin reduc-tionofspeciesfitnessattheindividualscale;however,littleisknownoftheeffectsofcompetitiononthe allometricpatternsofinsects.Inthisstudy,weexploredhowcompetition,bymeansofpodinfestation, affectsthedevelopmentoffemaleandmaleindividualsintheco-occurringbruchinebeetlesMerobruchus teraniandStatormaculatopygus.WefounddifferencesbetweenM.teraniandS.maculatopygusinall mor-phometrictraits,butnosignificantdifferencesbetweenmalesandfemalesineitherspecies.Wealso found,withanincreasingdegreeofpodinfestation,apositivetrendinthepronotum,elytronandbody weightofM.teraniandanegativetrendinmorphologicaltraitsandbodyweightofS.maculatopygus. Anegativeallometrywasmaintained,suggestingthatwithincreasingbodyweight,thebodystructures didnotincreaseproportionally.Ontheotherhand,wefoundthatincreasingthedegreeofpod infesta-tionproducedawidervariationintheindividuals’bodysizethaninlowlevelsofinfestation.Finally,we discusshowpodinfestationcantriggercompetitionbetweenspecies,withbothpositiveandnegative impacts,eventhoughthespeciesfunctionsimilarlyinresourceexploitation.

©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

The role of competitive interactions between herbivorous

insects asan importantcommunity-structuring factorhasbeen

debatedfor50 years(KaplanandDenno,2007).Theconceptof

competition asa centralorganizing force that prevailedin the

early1960sand1970s(Dennoetal.,1995)changedinthe1980s

toconsideringcompetitionasaweakandinfrequentstructuring

process(LawtonandStrong,1981;Strongetal.,1984),andmore

recently tothe perspective that herbivorous insects frequently

compete(Dennoetal.,1995;KaplanandDenno,2007).Pair-wise

interactionsproduceasymmetricconsequencesfortheinteracting

species(Dennoetal.,1995; KaplanandDenno, 2007),resulting

inspeciesexclusionsatthepopulationleveland/orfitness

reduc-tionattheindividuallevel.Consequencesatregionalorlocalscales

resultfrommortality,nicheshiftingandavoidance;whilefitness

reductionresultsfromdecreasingsurvival,fecundityandbodysize

(Dennoetal.,1995).

Bodysizeregulatestheorganism’s formunder

developmen-talmechanisms (Cariveau et al.,2016; Shingletonet al., 2008),

∗ Correspondingauthor.

E-mail:lucasdbf@gmail.com(L.D.B.Faria).

sincemostmeasurableaspectsofmorphologicaltraitscovarywith

body size(Emlenand Nijhout, 2000).Therelationship between

thesizeofonemorphologicaltraitandthesizeofanother

mor-phological traitorthebody sizeistermedallometry, aconcept

widelyapplicabletoecologyandevolution;andisameasurement

employedtoinvestigatecharacteristicsofinsectsandtheirsexes

(ColgoniandVamosi,2006;Foxetal.,2003).Still,littleisknown

oftheeffectsofcompetitionontheallometricpatternsofinsects

(EmlenandNijhout,2000;Shingletonetal.,2008;SternandEmlen,

1999).

MembersofthecoleopteransubfamilyBruchinaeareimportant

seed-feeders,capableofdamagingedibleleguminous seedsand

seedstocksusedinreforestationprograms(HegazyandEesa,1991;

Southgate,1979;Venkataramanaetal.,2016).Immaturestageslive

insideseedsthathavebeenexcavatedbythefeedinglarvae,while

adultslivefreeandfeedonpollenandnectar(Southgate,1979).

Usually,seed-feeding,miningandgallinginsectsexperiencehigher

levelsofcompetition,sincetheirmobilityisconstrainedbytheir

life-historyandresourcetraits(Dennoetal.,1995).

Merobruchusterani(Kingsolver,1980)(Chrysomelidae:

Bruchi-nae) and Stator maculatopygus (Pic, 1930) (Chrysomelidae:

Bruchinae)arebruchinespeciesthatconsumeseedsofa

climb-ing acaciaspecies, Senegaliatenuifolia (L.) Britton &Rose, 1928

(Fabaceae:Mimosoideae),andshowsimilarseed-predation

behav-ior, although M. terani hasa larger body and occurs in higher

http://dx.doi.org/10.1016/j.rbe.2017.04.003

0085-5626/©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://

abundancesthanS.maculatopygus(Tulleretal.,2015).Bothlarval

andpupalstagesliveinsidetheseeds,consumingtheseedsasthey

develop(KingsolverandJohn,2004;JohnsonandRomero,2004;

Tulleretal.,2015).Intermsofresourcelimitation,weobservedthat

onlyoneseedwassufficientfortheimmaturestagestodevelop,and

twoconsiderationsarose:thelarvaehadnoaccesstootherseeds

whenconsumingtheoriginalone,andalaboratoryexperimenthad

shownthatM.teranicancompleteallstagesoflifeinsideasingle

seed(Tulleretal.,2015;Maiaetal.,2017).Indeed,thesetwobeetle

speciesarefoundattackingthesamefruit,butnotthesameseed

(Maiaet al.,2017), whichsuggeststhattheyarenotcompeting

directly,i.e.,interferencecompetition,butrather arecompeting

indirectly,i.e.,exploitativecompetition.Finally,asignificant

dif-ferencebetweenthespeciesinconsumingseedsisrelatedtothe

timewhenthefemaleslaytheireggs.M.teraniarrivesfirst,whileS.

maculatopygusreachesthefruitjustbeforethepodsstarttoopen

andaftertheseedsarereleased(JohnsonandRomero,2004;Tuller

etal.,2015).

Theseaspectsofthebiologyofthetwobruchinespeciesmake

themaninterestingmodeltobetterunderstandtheeffectsofpod

infestation(hereusedasanestimateofindirectcompetition)on

morphologicaltraitsandallometry.Weexaminedhow

competi-tion,throughpodinfestation,affectstheindividualmorphological

traitsofM.teraniandS.maculatopygus.WehypothesizedthatM.

terani,asasuperiorcompetitor,wouldhaveanegativeimpacton

themorphologicaltraitsofS.maculatopygus,andthegreaterthe

degreeofinfestation,thegreatertheimpactwouldbe.Specifically,

wemeasuredmorphologicaltraitsincludingthepronotum,both

elytra,andbodysize,andevaluatedvariationsbetweenspecies,

malesandfemales,andinfestationcategories.Finally,we

exam-inedtheallometricrelationshipsofthesemorphologicaltraitswith

respecttothedegreeofinfestationofthepod.

Methods

Fieldsamplesandbeetlemeasurement

We sampled once a month in July and August 2014 (the

ripening period) to collect fruits of S. tenuifolia. As S.

tenuifo-lia is a liana species, the identification of an individual plant,

fromitsrootstoitsfruits,isdifficultbecauseeachplantspreads

over other plants, making it difficult to distinguish the

num-ber of individuals at a site. We therefore opted to collect the

fruitscasuallythroughthesubareas. We collected25 fruitsper

subareaineach samplingevent, totaling 350fruits.The7

sub-areaswereat least400mdistantfromeach other,and located

intwomunicipalities(LavrasandLuminarias)insouthernMinas

Gerais,Brazil:Aero-2(S21◦145.71W044◦578.66),Aero-3(S

21◦14787W044◦58006),Lav-1(S21◦183.46W044◦580.53),

Lumi-1(S21◦311.36W044◦531.78),Lumi-2(S21◦315.13W

044◦526.32),Lumi-3(S21◦315.31W044◦523.84)andLumi-4

(S21◦315.13W044◦5140.80).

Westoredthepodsinlabeledpaperbagsandbroughtthemto

thelaboratory,whereweplacedeachpodinanindividualPVCtube,

sealingtheendswithvoileattachedwithrubberbands,toallowair

exchange.Weleftthecollectedpodsonaworkbenchinthesame

temperatureandphotoperiod(12:12h).Afterthreemonthsof

stor-age,weopenedthefruits,identifiedtheattackedseedsbyspecies,

sex,andlarvalconsumptiontraits(adultsofbothspeciesleavea

typicalholewhenemergingfromtheseeds,whileotherspecies

thatconsumetheseedsleavenodefinitevisualpattern).By

select-ingpodscontainingonlyattackedseedswithahole,weensured

thatonlybruchinespecieswerepresent,andwecouldestimatethe

degreeofbruchineinfestationasanindirectestimateof

competi-tionbetweenspecies.Further,allattackedseedsheldonlyasingle

beetle,andwecommonlyfoundbothspeciesoccupyingthesame

fruit,butindifferentseeds(Maiaetal.,2017).Thebruchineswere

storedin1.5-mLlabeledplasticmicrotubescontaining70%ethanol.

Tomeasurethedryweight,hereafterbeetlebodyweight,ofboth

beetlespecies,adultsemergedorun-emergedfromseedscollected

inthefield(wedissectedtheun-emergedindividualsfrominside

theseeds)wereplacedinindividualpaperbags,driedat40◦Cfor

48h,andweighedusingaprecisionanalyticalbalance(Shimadzu

AY220).

Inordertoestimatetheeffectsofpodinfestationonbodysize,

we selected three morphological traits that best explained the

bodysizevariationinsomespeciesofbruchinebeetles(Colgoni

andVamosi,2006):pronotumlength,leftelytronlength,andright

elytronlength.Thesemeasurementsweretakenwithindividualsin

dorsalview,usingaLeicaM205Astereomicroscopeequippedwith

aLeicaDFC295digitalcamera.Sinceallthebeetlesfoundbelonged

tothesubfamilyBruchinae,wesexedthembyexaminingthewidth

ofthelastabdominalsegment.Wedepositedvoucherspecimens

intheEntomologicalCollectionoftheLaboratoryofEcologyand

ComplexityattheFederalUniversityofLavras,MinasGerais,Brazil.

Statisticalanalysis

Toperform thestatistical analysesand isolate theinfluence

ofnon-bruchidcompetitors,weconsideredonlypodsthatwere

infestedexclusivelybybruchines(pleaseseeTulleretal.,2015for

moredetailsaboutthefoodweb).Laboratorymeasurementsafter

thesamplingshowlowerspeciesabundancesthanthenumbers

ofseedspredatedperpod.Thatisbecausesomeindividualshad

alreadyemergedfromtheseedsbeforethesamplesweretaken.

Sinceallattackedseedsheldonlyasinglebeetleandwecommonly

foundbothspeciesoccupyingthesamefruit,butindifferentseeds,

weassessedthecompetitionasthedegreeofinfestation,i.e.the

numberofpredatedseedsinrelationtothenumberofseedsinthe

pod.Wedefinedthreeinfestationcategories:(G1)low,from0to

0.30;(G2)medium,from0.31to0.60;and(G3)high,from0.61to

0.90.Noinfestationlevelabove91%wasfound.

Weevaluatedthevariationinmorphometrictraits(leftelytron,

rightelytron,andpronotum)betweeninfestationcategoriesand

betweenmalesandfemales.Weusedgeneralmixedmodelswith

alog-normaldistribution,andsamplingdateasarandomfactor,

toreducetheeffectsofsamplingandrepeatedmeasures.Wealso

evaluatedallometricrelationships,estimatingthevariationrateof

thepronotum,leftelytron,andrightelytroninrelationtothe

indi-vidualbodyweight.Inthisanalysis,weusedmajoraxisregressions

(i.e., geometricmean), which are considered more appropriate

whenbothxandyvariablesaremeasuredwitherror(Sokaland

Rohlf,1995).Thevaluesofslopesandconfidenceintervalsfrom

theanalyseswereusedinasingleplottoillustratetheallometric

relationshipsbetweenspeciesandbetweeninfestationcategories.

AllanalyseswereperformedusingR2.15.3(RDevelopmentCore

Team,2013).

Results

Weevaluated152individualsofM.terani:38inG1,81inG2and

33inG3,totaling78femalesand74males.Thebodyweightranged

from0.4mgto3.8mg,pronotumfrom0.56mmto1.70mm,left

elytronfrom1.45mmto2.65mm,andrightelytronfrom0.96mm

to2.60mm.Wealsoevaluated24individualsofS.maculatopygus:

18inG1and6inG2,totaling5femalesand19males.Wedidnot

findindividualsofS.maculatopygusininfestationcategoryG3.The

bodyweightrangedfrom0.4mgto2mg,pronotumfrom0.53mm

to86mm,leftelytronfrom1.39mmto1.87mm,andrightelytron

Table1

Femaleandmalespeciesabundance,theabundanceofeachspeciesforeach

infes-tationcategory,andestimatesofbodyweightandmorphologicaltraits.

Merobruchus terani Stator maculatopygus Femaleabundance 78 5 Maleabundance 74 19 G1abundance 38 18 G2abundance 81 6 G3abundance 33 0

Bodyweight(min–max,mg) 0.4–3.8 0.4–2

Pronotum(min–max,mm) 0.56–1.70 0.53–86

Leftelytron(min–max,mm) 1.45–2.65 1.39–1.87

Rightelytron(min–max,mm) 1.40–2.60 1.39–1.84

G1,G2andG3abundance,abundanceforeachcategoryofpodinfestation;G1, lowinfestation(0–0.30%ofattackedseeds);G2,mediuminfestation(0.31–0.60% ofattackedseeds);G3,highinfestation(0.61–0.90%ofattackedseeds);min–max, minimumandmaximumvalue.

leftandrightelytra(Spearmancorrelationof0.97forM.teraniand

0.98forS.maculatopygus).Thus,belowwediscussonlytheresults

fortheleftelytron(Table1).

WefoundasignificantvariationbetweenM.teraniandS.

macu-latopygusforallmorphometrictraits.However,wedidnotobserve

asignificantvariationbetweenmalesandfemalesforeitherspecies

(Fig.1).Thebody weightofM.teraniwassignificantlylargerin

thehigher-infestationcategories(T=−3.47,D.F.=170,p<0.01).The

estimateddifferencewas0.27mg±0.07mgbetweenG1andG3.

Wedidnotfindsignificantvaluesforthepronotumandelytron.

Wedidnotobservesignificantvariationsinmorphometrictraitsof

S.maculatopygusbetweeninfestationcategories(Fig.2).

Regarding allometric relationships, our resultsshowed

neg-ative allometry for all relationships investigated. The slope of

variationwas0.257inG1,0.258inG2,and0.541inG3betweenthe

pronotumandbodyweight(pronotumallometry)inM.terani

indi-viduals.However,weobservedconfidenceintervalsrangingtozero

inG3,indicatingalackofrelationshipbetweenthese

morphomet-rictraits.Wefoundasimilarpatternforthepronotumallometry

ofS.maculatopygus.However,apartfromthelackofindividualsin

G3,wefoundinG2confidenceintervalsrangingtozero(Fig.3).

Theresultsforallometricrelationshipsbetweentheelytronand

bodyweight(elytronallometry)wereidenticaltotheresultsfor

pronotumallometry.Weobservedslopesofvariationof0.19,0.15,

and0.40inG1,G2,andG3respectivelyforM.terani;and0.09in

bothG1andG2forS.maculatopygus.Again,weobserved

confi-denceintervalsrangingtozerointhehigherinfestationcategories

(Fig.3).

Discussion

We have demonstrated some consequences frompod

infes-tation for the morphological traits, sexes and their allometric

relationships, of theseed-feeding beetlesM. teraniand S.

mac-ulatopygus. Males and females of both species showed similar

morphologicaltraits.ForM.terani,thehigherwastheinfestation

level,thelargerthebodypartsandbodyweight.S.maculatopygus

showedtheoppositetrend,i.e.,thehighertheinfestationlevel,the

smallerthebodypartsandbodyweight.Last,anegativeallometry

patternwasestimatedforbothspeciesregardlessofthelevelof

infestation,althoughincreasesintheinfestationlevelresultedin

significantvariationinbodysizeandmorphologicaltraits.

Although males are larger than females, we found no

sta-tisticallysignificantsexualdimorphismsformorphometrictraits

(e.g.,pronotumandelytron)ineitherspecies.Sexualsize

dimor-phismreflectsdifferentmaleandfemaleadaptations(Fairbairn,

a MF 0.0035 1.2 _2.6 2.4 2.2 2.0 1.8 1.6 1.4 1.1 1.0 0.9 0.8 0.7 0.6 0.0030 0.0025 0.0020 0.0015 0.0010 0.0005 MM

Body weight Pronotum

Elytra

SF SM MF MM SF SM MF MM SF SM

a b b a a b b a a b b

Fig.1. Variationsinbodyweight,pronotumandelytronlengthbetweenMerobruchusteraniandStatormaculatopygusandformalesandfemales.Theanalysesusedalinear

mixedmodelwithalog-normaldistributionandTukey’spairwisecomparison.MF,M.teranifemales;MM,M.teranimales;SF,S.maculatopygusfemales;SM,S.maculatopygus

a ab a a a a a a 0.0035 1.2 2.6 2.4 2.2 2.0 1.8 1.6 1.1 1.0 0.9 0.8 0.7 0.6 0.0030 0.0025 0.0020 0.0015 0.0010 0.0005 b MG1 MG2 MG3 SG1

Body weight Pronotum

Elytra

SG2 SG3 MG1 MG2 MG3 SG1 SG2 SG3 MG1 MG2 MG3 SG1 SG2 SG3

b b b b

c c

Fig.2.Variationsinbodyweight,pronotumandelytronlengthforMerobruchusteraniandStatormaculatopygusineachinfestationcategory.Theanalysesusedalinear

mixedmodelwithalog-normaldistributionandTukeypairwisecomparison.M,M.terani;S,S.maculatopygus.G1,lowinfestation(0–0.30%ofattackedseeds);G2,medium

infestation(0.31–0.60%ofattackedseeds);G3,highinfestation(0.61–0.90%ofattackedseeds).

1.5 1.2 1.0 0.8 0.6 0.4 0.2 0.0 1.0 M. terani S. maculatopygus 0.5 0.0 G1 G2 G1 G2

Pronotum allometry Elytra allometry

G3 G3

Fig.3.Negativeallometrydepictedbytheslopesandtheirconfidenceintervalsforthepronotumandelytronallometry(pronotumlengthandelytronlengthinrelation

tobodyweight)betweeninfestationcategoriesforbothbruchinespecies.G1,lowinfestation(0–0.30%ofattackedseeds);G2,mediuminfestation(0.31–0.60%ofattacked

seeds);G3,highinfestation(0.61–0.90%ofattackedseeds).

1997). It is a common pattern for females to be larger than

males; larger females are able to produce and lay more eggs,

whichresultsinhigherfecundity (Honek, 1993).However,

sex-ualdimorphism is contingent on environmentaland biological

conditions.Environmentalconditionssuchasthehost’sdefense

mechanisms,temperature,sizeofthehostseed,andfood

short-agesaffectthelarvaldevelopmentandpromotethedevelopment

ofadaptivestrategies,suchasreductioninbodysize(Carrolland

Hoyt,1986;CenterandJohnson,1974;Honek,1993).Ontheother

hand,femalesmaybesmallerthanmalesinresponsetobiological

factors, suchas male–male competition for sexual selection of

females(Foxetal.,2003;SavalliandFox,1998).

Tulleretal.(2015)foundthatM.teraniwasfivetimesmore

abundantthanS.maculatopygusinpodsofS.tenuifolia,and

pro-posedthatM.teraniiscompetitivelydominant.Maiaetal.(2017)

observeddominantspecies witha positive relationshiptotheir

resourcequantity,whereasS.maculatopygusdidnotshowsucha

relationship.Ourresultsconcordwiththesefindings.Thehigher

bodyweightandthemorphometrictraitsofM.teranicouldprovide

whiletheincreaseofbodyweightwithinfestationlevelsindicates

thatM.teranimaynotbelimitedbycompetitiveintra-and

interspe-cificinteraction.Ontheotherhand,S.maculatopygusmaybelimited

byinterspecificcompetition,sincethisspecieswasnotobservedat

thehighestlevelofpodinfestationanditsbodypartsandweight

becamesmaller.Therefore,S.maculatopygusmayreduce

competi-tionbyavoidingpodswithhighlevelsofinfestation,orevenfailto

surviveinthiscondition.Bruchinebeetleshavemodified

develop-mentalstrategies,suchasalteredfeedingandpupatingbehaviors,

andreductioninbodysize(CenterandJohnson,1974).Additionally,

theyshowtemporaldifferentiationinovipositionandhost

special-ization(CenterandJohnson,1974).Thesebehavioralresponsesto

selectivepressuresacttoreducetheeffectofcompetitivepressures

between species, such as the effects on development time,

weightandprobabilityofemergence(Foxetal.,2003;Messina,

1991).

Inordertounderstandtheproblemofhowbodypartsvarywith

totalbodyweightorotherpartsinrespecttopodinfestation,we

employedtheallometricapproach.Wechosethemorphological

traitsthatbestcapturetheeffectsofbodyvariation(elytronwidth

andlengthandpronotumlength)asrepresentativemeasurements,

commonly used to investigate thedevelopment of insects and

theirmorphologicalcharacteristics(ColgoniandVamosi,2006;Fox

etal.,2003).Thegeneraloutcomesdemonstratethatthenegative

allometry,maintainedthroughthedifferentinfestationlevels,

sug-geststhatincreasingbodyweightdidnotincreaseproportionally

withthebodystructures.However,thehighestlevelofinfestation

experiencedbyM.teraniincreasedtherelationship(slopevalueis

larger),increasingthesizeofmorphologicalstructureswithrespect

tobodyweight.Ontheotherhand,weshowedthatincreasingthe

degreeofpodinfestationproducedawidervariabilityinthe

indi-viduals’bodysize,makingthepopulationsofbothspeciesmore

heterogeneousintermsofmorphologicaltraits.Further,thestress

causedbytheinfestationlevelsmayincreasetheinstabilityofthe

developmentoftheindividuals,affectingtherelationshipamong

bodyparts.

In conclusion, we tested the hypothesis that M. terani is a

superiorcompetitor,negativelyaffectingS.maculatopygus;andan

increasein thedegreeofpodinfestationaugmenteditsimpact.

Ingeneral,wecorroboratedthehypothesiseventhoughthe

sta-tisticalanalysesdidnotsupportit.M.teraniseemsnottohave

beenaffectedbyintraspecificandinterspecificcompetitioninour

system,whileS.maculatopygusisimpactedbyinterspecific

com-petition,decreasingitsmorphologicaltraitsandbodysize.Wealso

observedthattheallometryapproachappliedtoinfertheeffects

ofcompetitiononthesespeciesdidnotshowconsistentpatterns,

despitetheincreasesinthesizeheterogeneityofindividualsofthe

populationsofbothspecies,insomelevelsofinfestation.Finally,

we demonstrated that interspecific competition affects these

species differently,although theyplay similarrolesin resource

exploitation.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

Wethanktheanonymousrefereesfortheirvaluablecomments

onthisstudy.Faria,L.D.B.thankstheMinasGeraisResearch

Foun-dation(FAPEMIG)andtheBrazilianNationalCouncilforScientific

andTechnologicalDevelopment(CNPq)andCoordinationforthe

ImprovementofHigherEducationPersonnel(CAPES)forfinancial

support.

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