The composition of spider assemblages varies along reproductive and architectural gradients in the shrub Byrsonima intermedia (Malpighiaceae)

2011·2.6 MB·English

by  Augusto Cesar De Aquino Ribas

2011.TheJournalofArachnology39:537-540
SHORT COMMUNICATION
Thecomposition ofspider assemblagesvaries alongreproductive and architectural gradientsIn theshrub
Byrsonima intermedia (Malpighiaceae)
AugustoCesardeAquinoRibas: GraduatePrograminEcologyandConservation,UniversidadeFederaldeMatoGrosso
do Sul, Campo Grande, MS, Brazil. E-mail: [email protected]
AntonioDomingosBrescovit: LaboratoriodeArtropodes,InstituteButantan,Av.VitalBrasil, 1500,Butanta,SaoPaulo,
SP, Brazil
JosueRaizer: SchoolofBiologicalandEnvironmentalSciences,UniversidadeFederaldaGrande Dourados,Dourados,
MS, Brazil
Abstract. Thepresenceofbuds,flowers,andfruitsincreasesstructuralcomplexityinplants,butcanalsoattractpotential
preyforpredators,thusdeterminingfaunisticcomposition. To understandhowaspiderassemblagelivingintheshrub
Byrsonimaintermedia(Malpighiaceae)varieswithhabitatstructureintermsofreproductiveelementsandheightofplant,
wecollectedspiderspecimensandmeasuredbud,flower,fruit,andleafmassesof44plants,aswellastheirheight.Spider
familycomposition was found to depend on habitat structure, followinga pattern offamilyturnover occurringalong
gradientsofreproductiveplantelementsandheight,regardlessofplantbiomass.Theridiidaeoccurredinsampleswiththe
major proportions ofbuds and flowers, while Oxyopidae occurred only in samples with major proportions offruits.
Multiplelinear regression revealed thestrongrelation between thecomposition in reproductiveplantelementsand the
compositioninfamiliesofspidersandarelationbetweenshrubheightandspiderfamilycomposition.Theseresultshelpus
tounderstandthetemporaldynamicsbetweenstructuralcomplexityofvegetationandspiderassemblages,becauseduring
plantphenologytheproportionsofreproductiveelementsarealsovarying.
Keywords: Araneae,assemblagecomposition,assemblagediversity,habitatstructure,habitatheterogeneity,reproductive
phenology
The influence ofplant structural traits on microhabitat selection Data were collected from an area of the Brazilian savanna
has been demonstrated for spiders around the world. The spiders’ (“cerrado stricto sensu”) in Campo Grande, Mato Grosso do Sul,
preferencesforparticularmicrohabitatsresultinvariationofspider southwestern Brazil (Embrapa Gado de Corte, 20°26'36.6"S,
diversityrelatedtoboththestructureofvegetativeparts(Halajetal. 54°43'30.6"W). The area, now undergoing regeneration, harbors a
2000;Souza2005)andthepresenceofreproductivestructures(Souza largenumberofB. intermediaspecimenswithasynchronicflowering.
&Modena2004;Souza&Martins2004). The species has entomophilous flowers that last for one day on
Inflorescence-bearing branches are structurally distinct from averageanddevelopintoadrupe(Oliveiraetal.2007).
vegetative branches and may constitute microhabitats that offer a From 17 October to 4 December 2008, a total of 44 shrubs
range ofattractive traits forspiders. Floral structuresmay provide (typically sixeach week) was sampled. To randomize thechoice of
refuge from predators and harsh environmental conditions, facili- shrubs,thepostsofanadjoiningfencewerenumbered. Afencepost
tating camouflaging for prey capture and serving as breeding sites andaperpendiculardistanceinmeters(integersfrom0to 100)were
(Johnson 1995). Abundanceofpotential prey forspiders is high in thenchosenbydraw.Fencepostanddistancedeterminedaspotfrom
budsandflowers,asthesestructuresareoftenvisitedbyherbivores whichthenearestB. intermediashrubwasselected.Whileuncut,the
and pollinating insects (Louda 1982). Furthermore, fruits attract plants were individually wrapped in plastic bags of 100 1 capacity,
insects andmay depend on these tocomplete their lifecycles (e.g., then cut at ground level using pruning shears before taken to the
Kolesik et al. 2005; Burkhardt et al. 2009). Plant phenological laboratory, whereeach shrub (mean height = 1.24 m, SD = 0.25;
variationisthereforeexpectedtodeterminevariationsinthestructure biomass = 461.2 g, SD = 252.3)was inspected forthepresenceof
ofspiderassemblages. arthropods. The spiders thus collected were stored for identifica-
The presence and succession ofreproductive elements ofplants tion at the family level. Voucher specimens were deposited in the
mask theeffects ofplant structural complexity on spiderdiversity, ArachnidacollectionofInstitutoButantanofSaoPaulo, Brazil.
because reproductive structures not only modify plant architecture Afterremovalofthearthropods,allthebuds, flowers,fruits, and
(bychangingbiomassspatialarrangement),butalsoamplifythelocal leavesfromeachshrubwerecollected,andthefreshmassofeachof
preyavailability, beingattractivetospidersformany reasons(e.g., thesetypesofstructurewasweighedusingabalanceof0.01gprecision
Finke&Denno2006;Schmidt&Rypstra2010). rightaftertheremovalofthearthropodsinthesamedayofsampling.
We desired to know ifthe relative amount ofeach reproductive AsB.intermediaisaspecieswithanasynchronousfloweringperiod
element (buds, flowers and fruits), height (plant architecture), and (Filho & Lomonaco 2006). The44 plant specimenswere randomly
biomass (habitat size) ofthe shrub Byrsonima intermedia A. Juss grouped,takingintoaccount thefrequencyofspiderfamilies,mean
(Malpighiaceae)mightexplainvariationinthecompositionofspider plantheight,andtotalbiomassofshrubs,leaves,buds,flowers,and
assemblages.Thearchitectureofthisshrubspeciesvarieswithheight fruits,resultingin 11 samplesoffourspecimenseach,allowingusto
(Oliveiraetal.2007),becausethetallerthespecimen,thefurtherapart makeordinationsofthevariableswithoutlosingtherelationbetween
itsbranchesarearranged,facilitatingtheconstructionofwiderwebs. them.
537
538 THEJOURNALOFARACHNOLOGY
-1IbIlllll Fruits
iiiIIIIIIII Flowers
il.illI-..B Buds
lllliilllll Leave
NMDSordinatedsamples -0.3 -0.2 -0.1 0.0 0.1 0.2
Reproductive elements composition
B
Oxyopidae
Araneidae
Sparassidae
Anyphaenidae
Miturgidae
III
Dictynidae
Salticidae
Thomisidae
Theridiidae
NMDSordinatedsamples -0.1 0.0 0.1 0.2
Figure 1.- Ordinationsofthesamplesbynon-metricmultidimen-
sional scaling (NMDS). (A) Phenological variation: ordination Plant height
obtained using relative biomass ofleaves, buds, llowers and fruits —
csinpoimBdpyeorrssioftnaimioiDlnii:aesi.onrledniiniaetdiioanspoebctiamiennesd(Muaslipnigghriealcaetaieve).f(rBe)quSepnidceyroffamitlhye mvaoldFueielgs.uroeNftM2h.DeSdPeaprsetcniodarleesntrfevograrreirsaeslbialotenivaenpdlforNtesqMueDonfcSietsshceoorfemsuslpotifidperlerleaftairmveieglrimeeasssssiaeorsne
of reproductive elements (A) and height of Byrsonima intermedia
(Malpighiaceae) shrubs (B) are the independent variables. Lines
Ordination by non-metric multidimensional scaling (NMDS) was represent the linear function obtained in the multiple regres-
employedtorepresentthevariationinrelativeamountsofleaves,buds, sionmodel.
(lowers, and fruits across plant samples. Weconsidered the relative
biomassofvegetativestructures(leaves)and reproductivestructures
(buds, flowers, and fruits), employing a Bray-Curtis dissimilarity families. Rsoftware(R DevelopmentCoreTeam2010)wasusedfor
matrixforthisordination. NMDSwasalsoused torepresentspider dataanalysis.Thevegansoftwarepackage(Oksansenetal.2010)was
family composition. A Bray-Curtis dissimilarity matrix based on additionallyemployedfordiversitycalculationsandforordinations.
relativefrequencieswasalsoemployedforthispurpose. Ordination of B. intermedia samples using the relative mass of
Amultiplelinearregressionmodelwasusedtoevaluatetheeffectsof leaves, buds, flowers, and fruits usingNMDS (n = 11, = 0.94)
reproductiveplantelements(NMDSscores),height,andbiomassonthe revealed variation in composition of the reproductive elements
diversity(Shannon index)andcomposition(NMDSscores)ofspider (Fig. IA). Samples with more buds remained on the left in the
RIBASETAL.—SPIDERASSEMBLAGESIN SHRUBS 539
gradientofordination,whileflowersdecreasedand fruits increased protectionduetopredationonherbivores),isnecessarytounderstand
alongthisgradient.Leaveswereabundantinallsamplesthroughout the structure ofa spider assemblage and help to predict potential
thisgradient,irrespectiveofreproductiveelements. responses to indirect interactions between spiders and plants
A total of 195 spiders from nine families was collected from 44 (Wootton2002).Itcanbeconcludedthatspidercompositiondepends
shrubs. Salticidae(62specimens),Anyphaenidae(33),andThomisi- on habitat structure, with a pattern of family turnover occurring
dae(21)werethemostabundantfamilies.AmeanShannon’sindexof alonggradientsofcompositionofreproductiveelementsandheight,
1.49wasfoundforfamilydiversity,rangingfrom0.67to 1.86forthe irrespectiveofplantbiomass.
h1e1igshatm,palnesdbainodmavsarsyiinngarmualntdiopmlelyrewgirtehssiroenprmoodducetliv(/e;=pla1n1t;Ee"le=me2n.t6s3,; ACKNOWLEDGMENTS
R- = 0.68;P=0.35). WethankF.O.Roque,J.C.Voltolini,S.Pekarandtwoanonymous
Sampleordination by NMDS {n = 11; = 0.73) usingrelative reviewersfortheirhelpfulsuggestionsandcomments.V.L. Landeiro
frequenciesofspideroccurrence,revealedagradientinspiderfamily provided R functions for the graphs in Fig. 1. This research was
composition (Fig. IB). Spiders ofthe family Salticidae were found supportedbythe FUNDECT, agovernmental foundation ofMato
throughout this gradient; Theridiidae and Thomisidae were more Grossodo Sul State(process 23/200.327/2008 and 23/200.384/2008)
likely to occur at the beginning of the gradient; Araneidae and and by Conselho Nacional do Desenvolvimento Cientifico e
Oxyopidae, at the end. Other families occurred in intermediate Tecnologico(CNPqgrant301776/2004-0toADB).
portionsofthegradient.
2ceviart0Pfn.ah0eloun0reg0enmAd=I4tia4cmpnl)hefr;teo,itsefd0ianrsrh.lSsoNtwusi0teonomisip1tsMutuu)titsis(lg,dzohooDbtheafnhbiadroS=apuaef&Noqltvasmfueses1soMaMan.ocsrnnr6aobcoDebes8tetrriomep;tigeaStvbretrrostiteolaneaifndtsag=fotssuisgborndecivcresioe2o2oet.oshur0nsib7(cme0mnopv7Fers4aeidmi;ewti)sdgaowb,.Pesefsdteerobluehtde2r(ie=erh)lfnPom.eeaimcec0nm(s=apno.oo«iprst0mmftlie3sspp0=hdysc),.ooeeeeo5scrsanxm71sioiltn3pBp1itmt).;dlaotipsi.aensRotoohiridTniu"senanthndtiieciiutygo=tdoeroeshfirfeinrt6ots0fma,an.8({iroei6thSnsedf%n8vopdipo;=atiiarutoorhdnoyzFfieu^eg0dpaer.rtuerd=3rhsceh8k&aeetep;avnso4iirseovs.fvgtoaMa7weehald(=r9olmtsu;liebldcopa3idltteltwP.anhgaiaie4neanegvnor6ta=ad,etnes;,r FFBiaulrrsactitBBhikeonabuyoiahrtr,o,robapaltr.lp,oorhstRoolrLdaoigF.lpe.tgnoiyoRsueC,innrc.ln.mae6maeARtano8i.&ngi.cn:c,snoei2igisen2TdlL,s,&tsa9a..ers-eFNarJve2.).dnnaaCe3,ielc.ddD2eqL-d.eipuietLinDleLihmaaapIrnoetaSv.fhiom.AiToinlu.oE&nrglt(2nfmahRR0JiiaaG-u0unuAcn.bssP8eecoesi.Talnc.el.anBctUi.ceteSsp(eRra:pt2OaMoniniE0tceeafadaa0h)clsele6C:pCocr,.rioslAeIengo.fvBTimafhgreVes.aiaigEacSzsateartDti2octoi.l0caego-.a10itaHfa6g9aiiesB1ot.(lv)rt:ee.ela8esdBoz7erewib(-nwmelDrf9seriiipea8fta.ln.nuishnloitcm(etzshJniePaHeoip.ayassaiunmanyccrdrceaednvheasanecoaeflroot)rsserpudutoiim-essatef
transiqaocerrado-vereda.Acta Botanica Brasiliense20:719-725.
a&erlcehMmieatnrettcsit,nusrierr2ae0ss0p4ae;cftuiFnvacertiioaofn&tootfaLlsiizpmelaainn2tf0l0bu8ie)on,mcaetsshsih.sabSiiintnvacetestcvioagmarptiliaeotxniionteyvian(lSupoalutazenadt Finpkree,daDti.oLn.:&implRi.cFa.tiDonesnnfoo.rp2r0e0y6.supSppraetisaslionreafnugdetrforpohmicicnatsrcaagdueisl.d
dthiesreigsaolradtiendgetfhfeectvaroifatairocnhidtuecetutroebbiyomamsesa,suwrhiincghswhrausbachehiigehvtedanbdy GonOceaclovleosg-iSaou1z4a9,:26T.5,-27P5..M. Omena, J.C. Souza & G.Q. Romero.
takingintoaccountthemultipleregressionmodel.Tallershrubshave 2008. Trait-mediated effects on flowers: artificial spiders deceive
rmeoprreesebnrtasncthheesamaonudntthoefsehaabrietatmoarvaeilasbplreeafdorosupti,dewrsh.ereas biomass Halpaojl,liJ.n,atDo.rsW.anRdosdsec&reaAs.eR.plMaontldfeintnkeess..2E0c0o0l.oIgmyp8o9r:t2a4n0c7e-2o4f1h3a.bitat
Several studies have demonstrated associations between plants structure to the arthropod food-web in Douglas-fir canopies.
aVansdcosnpicdeelrlso,s-mNoesttoo2f0t0e5n),ofbsuitngallesospeocfiemsul(tJiophlenssopnec1i9e9s5;(HRaloamjeretoa&l. HofOeirk,osH.90&:13A9.-D1.52B.rcscovit. 2001. Speciesand guild structureofa
2000;Raizer&Amaral2001;Souza&Martins2004).Thesestudies Neotropical spider assemblage (Arancae) from Reserva Ducke.
corroboratetheassumptionthathabitatarchitecturaltraitsdefinethe Amazonas, Brazil.Andrias 15:99-119.
compositionofspiderspecies. Johnson. S.R. 1995. Observations ofhabitat use by Sarinda hentzi
EachcomponentofthephenologyofB. intermediacan represent (Araneae, Salticidae) in Northeastern Kansas. Journal ofArach-
e(iRtohemreraon&inVcraesacsoencoerllaosd-eNcerteoas2e00i5n).spIindetrheapbruensdenatncsetudayn,dthdeivaedrsdietdy Kolneosliok,gyP2.3,:7R1.-J7.4.Adair & G. Eick. 2005. Nine new species of
effects ofleaf, bud, flower, and fruit biomass on spideroccurrence Da.sineitra (Diptera: Cecidomyiidae) from flowers of Australian
revealed a pattern offamily turnover in whichTheridiidae occured Acacia(Mimosaceae).SystematicEntomology30:454^79.
in samples with the major proportions ofbuds and flowers, while Louda, S.M. 1982. Inflorescence spiders: a cost/benefit analysis for
Oxyopidaeoccurredonlyinsampleswithmajorproportionsoffruits. thehostplant,Ilaplopappnsvenetii.sBlake(Asteraceae).Oecologia
This pattern suggests that niche partitioning is dependent on the 55:185-191.
reproductivephenologyofB. intermedia,morespecificallydependent Oksanen, J., F.G. Blanchet, R. Kindt, P. Legendre, R.B. O’Hara,
onthecompositionofreproductiveelements. G.L. Simpson, P. Solymos, M.H.H. Stevens&H. Wagner. 2010.
This response seen in the structure of the spider assemblage Vegan: Community Ecology Package. R package version 1.17-4.
possibly influences the indirect interactions between spiders and Onlineathttp://www.R-project.org
reproductive success (e.g., fruit-set and seed set) ofplants (Louda Oliveira,M.l.B.,C.A.Polido,L.C.Costa&W.S.Fava.2007.Sistema
1982; Goncalves-Souza et al. 2008; Romero et al. 2008). Different reprodutivo e polinizaqao de Byrsoiuitia intermedia A. Juss.
componentsofthereproductivestageofplantsareexpectedtohave (Malpighiaceae)emMatoGrossodoSul,Brasil.RevistaBrasileira
differenteffectsontheattractionofspidersofeachfamily(Souza& Biociencias5:756-758.
Martins 2004; Romero & Vasconcellos-Neto 2005), and general R DevelopmentCoreTeam.2010. R:ALanguageandEnvironment
patternssuchasthosedescribedinthisstudyareadditiveresponses forStatistical Computing. R Foundation forStatistical Comput-
resultingfromthesefamily-levelpatterns.Notonlyknowledgeofthe ing,Vienna,Austria.Onlineathttp://www.R-project.org
effect of each reproductive component of plant, but also of the Raizer,J.&M.E.C.Amaral.2001.Doesthestructuralcomplexityof
interaction between these components (e.g., decreased plant cross aquatic macrophytes explain the diversity of associated spider
pollination due to spiders predating on pollinators and fruit assemblages?JournalofArachnology29:227-237.
540 THEJOURNALOFARACHNOLOGY
Romero, G.Q., J.C. Souza & J. Vasconcellos-Neto. 2008. Anti- Souza,A.L.T. &R.P. Martins.2004. Distributionofplant-dwelling
herbivoreprotection bymutualistic spidersand theroleofplant spiders:inflorescencesversusvegetativebranches.AustralEcology
glandulartrichomes. Ecology89:3105-3115. 29:342-349.
Romero, G.Q. & J. Vasconcellos-Neto. 2005. The effects ofplant Souza, A.L.T. & E.S. Modena. 2004. Distribution of spiders on
structure on the spatial and microspatial distribution of a differenttypesofinflorescencesintheBrazilianPantanal.Journal
bromeliad-livingjumping spider (Salticidae). Journal ofAnimal ofArachnology32:345-348.
Ecology74:12-21. Wootton, J.T. 2002. Indirect effects in complex ecosystems: recent
Schmidt,J.M.&A.L.Rypstra.2010.Opportunisticpredatorprefers progress and future challenges. Journal of Sea Research 48:
habitat complexitythat exposes preywhile reducingcannibalism 157-172.
andintraguildencounters.Oecologia 164:899-910.
Souza,A.L.T. 2005. Foliagedensityofbranchesanddistributionof
plant-dwellingspiders. Biotropica37:416-420. Manuscriptreceived19December2010, revised18August2011.