Phytochemical cues affect hunting-site choices of a nursery web spider (Pisaura mirabilis) but not a crab spider (Misumena vatia)

2011·4.1 MB·English

by  Robert R Junker

2011.TheJournalofArachnology39:113-117
SHORT COMMUNICATION
Phytochemical cues affect hunting-site choices ofa nursery weh spider (Pisaura mirahilis)
but not a crab spider {Misitmena vatia)
RobertR.Junker’\ SimonBretscher',Stefan DotterFand NicoBliithgen': 'Department ofAnimal Ecology and
Tropical Biology, Biozentrum, UniversityofWurzburg, Germany. E-mail: [email protected];
^DepartmentofPlantSystematics, University ofBayreuth, Germany
Abstract. Predaceousarthropodssuchasspidersareoftenadaptedtohuntingsiteswheretheirhuntingsuccessisgreatest.
Weinvestigatedtheresponsesoftwospiderstophytochemicalcuesthattheypotentiallyexperiencewhilehuntingonleaves
orflowers,andhowthesecuescouldinfluencetheirdecisionswheretoforage.Wecomparedthebehavioroftwosit-and-
wait predators, Pisaura mirahilis and Misiimena vatia, which hunt predominantly in the vegetation or on Powers,
respectively. Inchoicetests, P. mirahilisfrequentlypreferred leavesandleafextractsto flowersand lloralextractsand
avoided substrates treated wMith the common floral scents (J-caryophyllene and nerolidol (sesquiterpenes) in natural
concentrations. Incontrast, vatiadidnotshowanypreferencesforanyofthesubstratesandtreatmentsoffered.The
lackofresponsesbyM. vatiacontrastswithearlierstudiesonanothercrabspiderspecies(Thomisitsspectahilis)thatused
phytochemicalcuesasaguidetorewardingflowers.Theavoidanceofmanyflowers,theirextracts,andthefloralscent
compoundsbyP.mirahilissuggeststhatthesecuesmaypreventthevisitationbythisandothergeneralisedpredatorsthat
potentiallydecreasethepollinationsuccessofaplant.
Keywords: Deterrence,optimalforaging,secondarymetabolites
Anunderlyingassumptionofmanyoptimalforagingmodelsisthat vegetation(oneindividualwascollectedfromanAchilleamillefoliitm
animals are behaviorally, morphologically and physiologically fiower).Wekeptthespidersindividuallyinsmallplasticcontainersin
adaptedtomaximizetheirnetrateofenergyintake(Schoener 1971; aclimatechamberunderlongdayconditions(day:night = 14:10h,
Cowie 1977). A behavioral adaptation ofpredaceous animals is to 26:19° C) and fed them with fiies twice a week and continuously
choose foraging patches that are frequently visited by prey or to provided waterasasmall drop. We picked the plants used forthe
which the animals are best adapted (Krebs et al. 1974; Shafir & laboratoryexperimentsinthesamearea.
Roughgarden 1998). Somecrabspiders, forexample, showadapta- In pair-wise choice tests, spiders were able to choose between
tionsas sit-and-wait predatorson flowers: they are able tochange different substrates including (lowers vs. leaves ofthe same plant
color forcamouflage and enhance the attractiveness offlowers for species (Experiment I), filter papers with extracts of (lowers vs.
pollinatorsduetotheirultravioletcontrastagainstpetals(Heilinget extractsofleavesofthesameplantspecies(ExperimentII)andfilter
al.2003). Thehighspecializationonflowersbycrabspiders isalso papers treated with synthetic floral scentcompounds vs. unscented
reflected in a relatively narrow prey spectrum, which is limited to controls(Experiment III). The principal setup oftheseexperiments
commonflowervisitortaxa(Nentwig1986).Othernon-web-building (I-III)wasthesame: weplacedindividualspidersonpiecesofcork
spiders hunt or ambush predominantly in the vegetation and thus representing“islands” (ca 30cm^) in water-filled bowls, preventing
captureabroaderspectrumofpreytaxa(Nentwig 1986).Tobenefit spiders from escaping. On each ofthese islands, we attached two
fromtheiradaptationstodifferentplantstructures(vegetativeversus wooden sticks (height = 140 mm, diam. = 3 mm) in an upright
reproductive)ortospecificvisitorsofthesestructures,spidersneedto positionandattachedthedifferentsubstratesusedintheteststothe
perceiveandthusrecognizethosestructures.Heilingetal.(2004)have tipofthesesticks.Thedistancebetweenthesubstrates(ca 1cm)was
shown that crab spiders (Thomisits spectahilis) use visual and chosen to be close enough that the spiders could freely change
olfactoryflowercuesforpatchchoice. between the substrates without descending to the islands but large
Weexperimentallytestedforsubstratechoicebehaviorandarole enoughthatspiderswereforcedtomakeachoice.Neonlampsfrom
of phytochemicals in two non-web-building spiders that utilize aboveilluminatedthewholesetup. Afterspiderswereplacedonthe
differentplantpartsashuntingsites:thecrabspiderMisitmenavatia islands,weobservedthemfor 1 h,recordingtheirpositiononeither
(Thomisidae), which typically sits and waits on flowers to catch substrateevery3min.Weusedindividualspidersforseveraltestsbut
flower visitors, and the nursery web spider Pisaura mirahilis notrepeatedlyforthesametreatment.
(Pisauridae), which hunts in the vegetation. In concordance with Experiment I: We placed freshly picked (lowers and leaves from
theirlifestyle, weexpected M. vatiato be attracted to flowercues, Achillea millefolium, Centaurea cyanits, Tanacetiini vitlgare (all
whileP. mirahilsmaypreferleaves. Asteraceae), Medicago sativa (Fabaceae) and Saponaria officinalis
BetweenJuneandAugust2008,wecaughtM. vatiaandP.mirahilis (Caryophyllaceae)insmallwater-filledvases.Thevaseswere 1.5ml
spiderson fallow lands in Wurzburg, Germany. Wecollected fifty- standard microcaps, and we attached them on top ofthe wooden
eight individuals of M. vatia on flowers of Achillea millefoliitm, sticks.Ineachpair-wisetest(fiowervs.leafofthesameplantspecies),
Aegopodiitmpocktgraria,Leucanthemitmvitlgare,Sapomtriaofficinalis, weadjustedthenumberofleavesandflowersorinfiorescencessothat
Solidago canadensis, Trifoliitm pratense, Tripleitrospermitm niariti- bothsubstratesrepresentedapproximatelythesamearea, providing
mum, while we collected all but one of41 P. mirahilis from the sufficientspaceforspiderstositon.
ExperimentII:Weusedthesamefiveplantspeciestoprepareleaf
^Currentaddress: Heinrich-Heine-UniversityofDiisseldorf,Depart- andflowerextracts.Weplacedfreshlychoppedplantmaterialintoan
ment Biology, Institute of Sensory Ecology, UniversitatsstraPe 1, extractionthimbleandcontinuouslyextracteditwith50ml//-hexane
40225Dusseldorf,Germany in a Soxhlet apparatus for three hours at a temperature of85° C
113
114 THEJOURNALOFARACHNOLOGY
Table 1.—Generalizedlinearmodels(GLMwithquasibinomialerrordistribution)oftheproportionalchoicesforflowers,flowerextractsor
syntheticcompounds in Pisaiiraminihilixand Misumena vatia: a) trials usingfreshplantmaterial (flowersversus leaves, Experiment I)and
extractsofdowersversusextractsofleaves(ExperimentII).Factor“treatment”referstotrialsusingfreshplantmaterialsorextractsthereof,b)
Trials using synthetic scent compounds versus the acetone-only treatment (Experiment III). Starting with the full model containing all
explanatoryparameters,eachreducedmodelwascomparedwiththepreviousonewitha testresultingindeviance,numberofdegreesof
freedom(dj)),residualdegreesoffreedom(r//^)andsignificance(P)foreachparameter.
Parameter Deviance df, df2 P
a)
Spiderspecies*plantspecies*treatment 4.53 9 288 0.58
Treatment 0.00 1 297 0.99
Spiderspecies*plantspecies 5.48 4 298 0.053
Plantspecies 7.95 4 302 <0.01
Spiderspecies 14.25 1 306 <0.001
Residualerror 199.85
Total 232.06
b)
Spiderspecies*substance*concentration 2.54 3 226 0.27
Concentration 0.08 1 227 0.73
Spiderspecies*substance 5.41 5 232 0.14
Substance 8.94 5 237 0.014
Spiderspecies 4.37 1 238 <0.01
Residualerror 163.61
Total 184.94
(Baysal & Starmans 1999). We removed thesolvent undervacuum testedwithP.mirahilisonly.Wedissolvedsubstancesinacetoneand
and resolved the extract in acetone. We determined the volume of appliedthemindifferentamountsstartingwith0.01 mMolperfilter
athceeteoxnteraacst0(.27050•pgi)droynwreoiugnhdtf•i2lt0e0rplpaapceertson(ediaanmdetaeprpl=ied35almimqu)ottshaotf pspaipdeerr.sIpnecciaessesinwhtheirseinaitsiaulbsctoanncceentrafafteicotne,dwtehescuhbosiecqeueonftloynereodfuctehde
were attached on top ofthe wooden sticks. Thus, the extract was the amount (0.005, 0.0025, and 0.00125 mMol per filter paper) in
appliedtofilterpaperswithamassof75%oftheplantdryweightto order to explore concentration-dependent effects. We attached the
accountforlossesoftheextractduringtheprocess.Wetestedflower scented filterpapers(treatment) and filterpapers treated onlywith
andleafextractsofeachplantspeciesagainpair-wise. acetone(controls)ontopofthewoodensticks.Afterapproximately
In order to determine those compounds in the extracts that 10min,afterthesolventhadevaporated,atrialstarted.
frequentlyoccurin flowerand leafscents(Knudsenetal.2006),we Each trial(1-h period)yielded upto20observationsfromwhich
analysed theextracts usinga Varian 3800gaschromatograph (GC) the proportion ofobservations on flowers (Experiment I), fiower
fittedwitha1079injectorandaZB-5column(5%phenylpolysiloxane; extracts(II)orscentedfilterpapers(III)wasobtained,disregarding
length, 60 m; inner diameter, 0.25 mm; film thickness, 0.25 pm; observationsduringwhichthespiderwasnotpresentononeofthe
Phenomenex)andaVarianSaturn2000massspectrometer.Weplaced substrates. Somespidersspenttimeontheislands,whileothersdid
sm1pelpiaitnovsfenottfhetwhaseasCmophplreeonsmeadin,ttooaPnardoqtbuheaerktiinztj(veAicatmloirirnwaatvshe&hieDnajategecdatonart1p49o09r°7t)C.ofTtohthefeliuGnsjhCecatnboyyr tnvahotetiapl:reoa7pv.eo3r%itt)i;dountr.hienWsgeetrhapereerenfetovierrnmetepsdewrgieeorndeer{naPol.itzmiierdnachlliiulndieesa:dr3imn.o0dt%ehelosfca(allGcluLtlrMaita)liso,wniMto.hf
air from the system. After2 min, thesplit vent wasclosed and the quasibinomial error distribution (accounting for the overdispersed
irnujne.ctTohrehesaptlietdvaten2t00w°aCsmagiani“n',otpheennehdeladftaetr246.05°mCinu.ntiElltehcetreonndicoffltohwe cdhaotiac)e.inWeoradnearlytsoedextphelotreeststhweithpafrraemsehtpelrasntimnaftleureinaclin(gExtpheerismpeidnetrsI’)
controlwasusedtomaintainaconstantheliumcarriergasfiowrate and extracts (Experiment II) in one GLM, with the proportionof
C(1,.0thmelnmiinlclr”e'a)s.eTdhbeyG6°CCovmeinn^t'emtpoe3r0a0t°urCe,waansdhheellddffoorr41.55mmiinnaattt4h0i°s sopbisdeerrvastpiecoiness,opnlafnitowseprescieosrafnidowterreaetxmteranctts(i.ae.s,rfreessphonpsleantvamraitaebrliealanodr
temperature.Massspectraweretakenat70eVwithascanningspeedof extracts)asexplanatoryvariables. IntheGLM fortestswithfloral
onescan per second from m/z30 to 650. We analyzed the data as scentcompounds(ExperimentIII),weusedspiderspecies,substance
describedelsewhere(Dottedetal.2009),andusedaninternalstandard andconcentration(mMol)asexplanatoryvariables. Beginningwith
(3-chloro-4-methoxytoluene)forquantification. thefullmodel,wereducedthemodelsstepwiseandcomparedthemto
Experiment III: Sinceweexpectedthatthephytochemicalcuesto thepreviousonewitha test(Crawley2005).Priortothestepwise
whichspidersrespondarenotspecifictocertainplantspecies,weused statisticalanalysis,wecomparedthefullmodeltoanullmodel(model
commonlyoccurringfiowerandleafscentcompoundsthatwerealso with no explanatory variables) to validate the overall effect ofthe
present in the extracts for subsequent bioassays. Among the combinedparameters.Wetestedindividualparametersonlyifthefull
compounds identified in the samples, we selected benzaldehyde modelhadsignificantlymoreexplanatorypowerthanthenullmodel
(benzenoid), 1-hexanol, r7.v-3-hexen-l-ol,c7.s'-3-hexen-l-ylacetate(all (seeMundry&Nunn2009).Additionally,weindividuallytestedthe
aliphatics),limonene,linalool(monoterpenoids),p-caryophylleneand proportionsagainstthenullhypothesis(assumingequalvisitationof
nerolidol (mixture of cis- and trans-isomers, sesquiterpenoids), bothtreatmentandcontrol;i.e.,proportion =0.5)withaWilcoxon
becausethesecompounds arecommon and widespread floral scent test. All statistical analyses were performed using R 2.4.0 (R
compounds (Knudsen et al. 2006). 1-hexanol, c7.s'-3-hexen-l-ol and DevelopmentCoreTeam2009).
c/.s'-3-hexen-l-ylacetatearealsocommongreenleafvolatiles(Pare& In 93.3 and 97.5% ofall trials with M. vatia and P. mirahilis,
Tumlinson 1999); r7.s-3-hexen-l-ol and c/.s-3-hexen-l-yl acetatewere respectively, the spiderchose one ofthe substrates within thefirst
JUNKERETAL.—PHYTOCHEMICALSAFFECTPATCHCHOICEINSPIDERS 115
Proportionofchoicesforflowers Proportionofchoicesforflowers
00 0.2 04 0.6 0.8 1 00 02 0.4 0.6 08 1C
Achilleamillefolium I- --H 9
L:l.a.a.fiF: h 10 T I H • 10
CH
Centaureacyanus I- -I 12
L:5.6F;1.4.5 U ]l 19
HD
Medicago-sal-iva I-1 -I 14 . 12
^ I i I- H 16 i 17
Saponariaofficinalis J 16 -1: 20
H 11 H: 20
Tanacelumvulgare 1 1 20 21
L:3.5F:3,i -I 19 -H 19
Proportionofchoicesforscentedfilterpaper Proportionofchoicesforscentedfilterpaper
00 02 04 06 08 1.0
(1)Benzaldehyde (----I | j- 1 10 h 1 1 1 ^0
(2)1-HeKanol I -j |i; [--I 10 [zzl:::: 1 1 10
(3)Limonene I •! II b '3 r~ \--i 14
(5)3-Car(y4o)pLhiynalllcexn5el It-( | | 1i 11 1 ^ < -9 11 1 11,;; 1_105
(6)Nerolidol i---| | 1 [ 1 • 40 Ir
Misumenavatia Pisauramirabilis
—
Figure 1. DualchoicesofPisauramirabilisandMisumenavatiabetweenflowersandleaves,extractsorsyntheticcompounds.Choiceswere
measuredasproportionofchoicesforflowersandtheirextracts(a.experimentsIandII)orscents(b.ExperimentIII)ofthetotaltimeonboth
treatments. Significant deviation from an equal proportion ofvisits on flowers and leaves, or scent and control (i.e., proportion = 0.5) is
indicatedbyasterisksusingpairedWilcoxonranksumtest{*P<0.05,**P<0.01,***P<0.001).Samplesizesaregivennexttoeachboxplot,
a)Whiteboxesshowtrialswithfreshplantmaterial(flowersvs.leaves),grayboxesfiowervs.leafextracts.Leaf(L)andflower(F)extractsoften
containedoneormoresubstancesusedinthebioassay,whicharelistedbeloweachspeciesname.Numberscorrespondtothesubstancecode
below (see b). Concentrations ofsubstances in plant materials are labelled as follows: plain numbers: MO^^-O.Ol niMol g“' dry weight;
underlinednumbers:0.011-10mMolg“';underlined,boldfacedanditalicnumbers:> 10mMolg^'.(b)Resultsoftrialsusingsyntheticfioral
scentcompoundstestedagainsttheacetone-onlycontrol.
8min.Onceaspiderclimbedupawoodenstick,itrarelydescendedto M. vatiawaslessselectivethan P. mirabilis(Table lband Fig. lb).
islandsagain.WhileM. vatiaoftenchangedthesubstratesduringthe M. vatiaavoidedfilterpapertreatedwithnerolidol,andP. mirabilis
trial (3.0 ± 0.2 times, mean ± SE), P. mirabilis was less likely to avoided both nerolidol and P-caryophyllene (Fig. lb). P. mirabils
switch, with only 0.8 ± 0.2changesofthesubstrate per trial. The behaviorwasnotaffectedbythegreenleafvolatilesc/.y-3-hexen-l-ol
responses to fresh plant material (Experiment I) were usually and m-3-hexen-l-y! acetate (V< 50.5, P > 0.37, Wilcoxon test).
consistent with responses to extracts of the same plant species LargeamountsofnerolidoloccurredinfloralextractsofS.officinalis,
(Experiment II) for both species ofspider, but the spiders’ choices and P-caryophyllene in A. millefolium. These substances may have
between leaves and flowers differed strongly between plants triggeredthepreferenceofP. mirabilisforleavesandleafextractsin
(Table la). P. mirabilis strongly preferred leaves over flowers (and S.officinalis,andforleafextractsofA.millefoliumovertherespective
theirextracts)inthreeoutoffiveplantspecies,whereasM. vatiadid flowers or floral extracts (Fig. 1). Living flowers ofA. millefolium
notshowanypreferences(Table laandFig. la). were not avoided by P. mirabilis, suggesting that some substances
Intrialswherespiderswereallowedtochoosebetweenfilterpaper were dissolved from the plant tissue and were thus present in the
treated with scent compounds and acetone-treated filter paper extractsthatwerenotemittedbyfreshplantmaterialorwereemitted
(Experiment III), thechoicesdepended on the particularsubstance inalesseramount.
andspiderspecies.Overall,theconcentrationofthecompoundsdid The results of our study imply that P. mirabilis perceive
notaffectthespiders’choices(Table lb).Similartotheprevioustests. phytochemical cues and use them to decide where to ambush for
THEJOURNALOFARACHNOLOGY
116
prey. InM. vatki,behavioralresponsestothesecuesweremuchless Chien,S.A.&D.H.Morse.1998.Therolesofpreyandflowerquality
pronounced, and the crab spiders only responded weakly to the inthechoiceofhuntingsitesbyadultmalecrabspidersMisumena
sesquiterpenenerolidol.WehadexpectedthatM. vatiawouldprefer vatia(Araneae,Thomisidae).JournalofArachnology26:238-243.
flowersandtheirextractsoverleavesandtheirextracts,sinceother Cowie,R.J.1977.Optimalforagingingreattits(Parusmajor).Nature
crab spiders (Thaniism spectahilis) positively responded to floral 268:137-139.
osdhoorwsn(tHoeilpirnefgeretfuall.ly2o00p4e)n. aCnrdabfusnpcitdieornsalinfcllouwdeirnsg(Ma.nthveastiisa)woevreer CraCwhliecyh,estMe.rJ,.U2K0.05. Statistics - An Introduction Using R. Wiley, :
senescentones(Chien& Morse 1998; Heiling& Herberstein2004a) Dotterl,S.,A.Jurgens,L.Wolfe&A.Biere.2009.Diseasestatusand ’
and therefore have the same preferences as pollinators and use populationorigineffectsonfloralscent:potentialconsequencesfor
olfactoryinadditiontovisualcues(Heilingetal.2004).However,we ovipositionandfruitpredationinacomplexinteractionbetweena
could notconfirm positive responses to floral odorsorcompounds plant, fungus, and noctuid moth. Journal ofChemical Ecology 1
thereofGrecoand Kevan(1994;2001)alsoreportednodiscrimina- 35:307-319.
tion between leaves and flowers by the same spider species. It was Dukas,R.2001.Effectsofperceiveddangeronflowerchoicebybees.
shownthatM. vatiaremainslongeronflowersthatarefrequentedby EcologyLetters4:327-333. ^
pollinators(Chien&Morse 1998;Morse2000a)andonflowersthat Dukas,R.&D.H. Morse.2003.Crabspidersaffectflowervisitation
theyhaveexperiencedbefore(Morse2000b).Weusedpickedflowers bybees.Oikos 101:157-163.
(i.e., notthepreferredstateoftheflowers)thatwerenotvisitedby Gershenzon,J.&N.Dudareva.2007.Thefunctionofterpenenatural
insects,whichmaycontributetoalackofpreferences. products in the natural world. Nature Chemical Biology 3:408-
The preference for leaves over flowers in P. inirabils may either 414.
result from an attraction to leaves or from an avoidanceofflower Goncalves-Souza, T., P.M. Omena, J.C. Souza & G.Q. Romero.
secondary metabolites. The trials with individual substances are 2008. Trait-mediated effects on flowers: artificial spiders deceive
consistent with the latter and suggest that floral scents or perhaps pollinatorsanddecreaseplantfitness. Ecology89:2407-2413.
othernon-volatilemetaboliteshaveadeterrenteffectonthisspider. Greco, F. & P.G. Kevan. 1994. Contrasting patch choosing by
Plantvolatilesemittedbyflowersandfeaveswereshowntorepelor anthophilous ambush predators: vegetation and floral cues for
d&UentseDircuvkdaearrrieoevtusaala.r2t020h07r0;9o;poJWduisnlk(lemPriecr&heetrsBaklly.ii&2t0hg0Ge9en;rsJ2hu0en0nk8ze;ornK&2a0nB0t2l;uteGthegrealsn.he220n01z00o9)n.; dZoefocoialsnoiognaysm7bb2yu:s1ah5c8r3ba-ub1g5s8p8{i.Pdleir'y(mMaitasuammeenraicvaantai)a.)aCnadnamdaileasnaJnodurfneamlaleosf
Therefore,itislikelythatthefloralrepellenceofthisspiderrepresents Heiling,A.M.,K.Cheng&M.C. Herberstein.2004.Exploitationof
atypicalresponseofabroadspectrumofgeneralisedpredatorsand floral signals bycrab spiders{Thomisusspectahilis,Thomisidae).
othertaxathatarenotspecificallyadaptedtoflowers. BehavioralEcology 15:321-326.
Crab spiders are predators that exploit the mutualism between Heiling,A.M.&M.E.Herberstein.2004a.Floralqualitysignalslure
flowers and pollinators and thereby have detrimental effects on pollinators and their predators. Annales Zoologici Fennici 41:
pollination and consequently reproduction ofplants (Dukas 2001; 421-428.
Dukas & Morse 2003; Heiling& Herberstein 2004b; Readeret al. Heiling, A.M. & M.E. Herberstein. 2004b. Predator-prey coevolu-
2006;Goncalves-Souzaetal.2008;Ings&Chittka2008;Brechbiihlet tion: Australiannativebeesavoidtheirspiderpredators. Proced- '
al. 2010). Chemical floral cues that prevented predators such as ingsoftheRoyalSocietyLondon271:196-198.
spiders and other floral antagonists from visiting flowers and Heiling, A.M., M.E. Herberstein & L. Chittka. 2003. Pollinator
simultaneously attracted pollinators would maximize the plants’ attraction - Crab-spiders manipulate flowersignals. Nature421:
reproductive success (Brown 2002; Irwin et al. 2004; Junker & 334-334. '
Bluthgen 2008). Animals that depend on floral resources (obligate Ings, T.C. & L. Chittka. 2008. Speed-accuracy tradeoffs and false
flowervisitors)areabletotoleratedefensivefloralscentcompounds alarms in bee responses to cryptic predators. Current Biology
and even use them as host-finding cues, while facultative flower 18:1520-1524.
visitorsarenotableto(Junker&Bluthgen2010).Theresultsofthe Irwin,R.E., L.S.Adler&A.K. Brody.2004.Thedualroleoffloral
presentstudysuggestsuchadichotomy,inwhichanobligateflower traits: Pollinator attraction and plant defense. Ecology 85:1503-
visitor{M. vatia)isadaptedtoflowersasaplacetositandwaitfor 1511.
prey,whichmayincludeatoleranceagainstotherwisedefensivefloral Junker, R.R. & N. Bluthgen. 2008. Floral scents repel potentially
compounds.Incontrast,P. inirahilisisadaptedtousethevegetative nectar-thievingants.EvolutionaryEcologyResearch 10:295-308.
plant parts as hunting sites and may not have been subjected to a Junker, R.R. & N. Bluthgen. 2010. Floral scents repel facultative
selectivepressuretotoleratethesamecompounds. flower visitors, but attract obligate ones. Annals ofBotany 105:
ACKNOWLEDGMENTS Kan7t7,7-7M8.2R.., P.M. Bleeker, M.V. Wijk, R.C. Schuurink & M.A.
WethankRichardBleilforperformingsomeofthebioassays.The Haring.2009.Plantvolatilesindefence.Pp.613-666.InAdvances
study wassupported by the Deutsche Forschungsgemeinschaft (BL inBotanicalResearch,Volume51.(L.C.vanLoon,ed.).Academic
960 1-1)andbytheEvangelischesStudienwerke.V.Villigst. Press, Burlington,Massachusetts.
LITERATURECITED Keviamnm,atPu.r&e Fa.mbGurescho.pr2e0d0a1t.orCso,ntarassptiidnegrp(aMticshucmheoniacevbaetihaa)viaonudrabny
Amirav,A.&S.Dagan. 1997.Adirectsampleintroductiondevicefor insect(Pliymataamericana).EcologicalEntomology26:148-153.
mass spectrometry studies and gas chromatography mass spec- Knudsen,J.T.,R.Eriksson,J.Gershenzon&B.Stahl.2006.Diversity
trometryanalyses. EuropeanMassSpectrometry3:105-111. anddistributionoffioralscent. BotanicalReview72:1-120.
Baysal, T. & D.A.J. Starmans. 1999. Supercritical carbon dioxide Krebs, J.R., J.C. Ryan & E.L. Charnov. 1974. Hunting by
extractionofcarvoneandlimonenefromcarawayseed.Journalof expectation or optimal foraging? A study of patch use by
SupercriticalFluids 14:225-234. chickadees.AnimalBehaviour22:953-964.
Brechbuhl,R.,C.Kropf&S.Bacher.2010.Impactofflower-dwelling Morse,D.H. 2000a. Flowerchoicebynaiveyoungcrabspidersand
crab spiders on plant-pollinator mutualisms. Basic and Applied theeffectofsubsequentexperience.AnimalBehaviour59:943-951.
Ecology 11:76-82. Morse,D.H.2000b.Theroleofexperienceindeterminingpatch-use
Brown,K.2002.Acompromiseonfloraltraits.Science298:45-46. byadultcrabspiders. Behaviour 137:265-278.
JUNKERETAL.—PHYTOCHEMICALSAFFECTPATCHCHOICEINSPIDERS 117
Mundry,R.&C.L.Nunn.2009.Stepwisemodelfittingandstatistical Schoener,T.W. 1971.Theoryoffeedingstrategies.AnnualReviewof
inference:turningnoiseintosignalpollution.AmericanNaturalist EcologyandSystematics2:369^04.
173:119-123. Shafir, S. &J. Roughgarden. 1998. Testingpredictions offoraging
Nentwig, W. 1986. Non-webbuilding spiders - prey specialists or theory for a sit-and-wait forager, Anolis gingivinus. Behavioral
generalists.Oecologia69:571-576. Ecology9:74-84.
Pare, P.W. & J.H. Tumlinson. 1999. Plant volatiles as a defense Unsicker, S.B., G. Kunert & J. Gershenzon. 2009. Protective
againstinsectherbivores.PlantPhysiology 121:325-331. perfumes: theroleofvegetativevolatilesin plantdefenseagainst
Pichersky,E.&J.Gershenzon.2002.Theformationandfunctionof herbivores.CurrentOpinioninPlantBiology 12:1-7.
plant volatiles: perfumes for pollinator attraction and defense. Willmer,P.G.,C.V.Nuttman,N.E.Raine,G.N.Stone,J.G.Pattrick,
ReaCduerrr,enTt.,OpAi.nDi.onHiigngPilnasnotn,BiCo.lJo.gyBa5r:n2a3r7d-,243F..S. Gilbert & B.E.F. 2K0.09H.enFlsoorna,lvPo.laSttiillelsmcaonn,trLo.llMicngllarnoty,beSh.aGvi.ouPro.ttFsun&ctJi.oTn.alKnEucdosleong.y
Course. 2006.Theeffectsofpredationriskfromcrabspiderson 23:888-900.
beeforagingbehavior. BehavioralEcology 17:933-939.
RDevelopmentCoreTeam. 2009. R: A languageandenvironment
forstatisticalcomputing.RFoundationforStatisticalComputing,
Vienna.Onlineathttp://www.r-project.org/ Manuscriptreceived15February2010, revised10October2010.