Review Foraging behavior of egg parasitoids exploiting chemical information

13 Pages·2008·0.22 MB·English

BehavioralEcology
doi:10.1093/beheco/arn011
AdvanceAccesspublication27February2008
Review
Foraging behavior of egg parasitoids exploiting
chemical information
Nina E. Fatouros,a Marcel Dicke,a Roland Mumm,a Torsten Meiners,b and Monika Hilkerb
aLaboratoryofEntomology,DepartmentofPlantSciences,WageningenUniversity,Binnenhaven7,6709
PD Wageningen, The Netherlands and bApplied Zoology/Animal Ecology, Institute of Biology, Freie
Universita¨t Berlin, Haderslebener Strasse 9, 12163 Berlin, Germany
Femaleparasiticwaspsseekhostsfortheiroffspringofteninadynamicenvironment.Foragingeggparasitoidsrelyonavarietyof
chemical cues originating from the adult host, host products, or the host plant rather than from the attacked host stage—the
insecteggitself.Besidespupae,insecteggsarethemostinconspicuoushoststageattackedbyparasiticwasps.Toovercomethe
problemoflowdetectabilityofhosteggs,eggparasitoidshaveevolvedseveralstrategiessuchasexploitinglong-rangekairomones
of the adult hosts, for example, host aggregation and sex pheromones, plant synomones induced by egg deposition or host
feeding, orshort-range contact cuesderived from the adulthost or thehost plant. Moreover,egg parasitoidshaveevolved the
abilitytousechemicalespionageincombinationwithhitchhikingontheadulthost(phoresy)tocompensatetheirlimitedflight
capabilityandtogainaccesstofreshlylaidhosteggs.Here,weprovideacomprehensiveoverviewonthevarietyofhost-foraging
strategies of egg parasitoids exploiting chemical signals. Furthermore, the use of such infochemicals is discussed with respect
to the wasps’ dietary breadth and their ability to learn. Key words: egg parasitoids, host-foraging behavior, infochemicals,
kairomones,phoresy,plantsynomones, sexpheromones. [BehavEcol19:677–689(2008)]
Egg parasitoids are specialized to develop in the eggs of completed with the oviposition in or on the host. This so-
other insects. Insect eggs are nutrient-rich enlarged cells called host selection is mediated by numerous stimuli, of
that do not feed and release feces and consequently lack in- which chemicals are known to play a major role (Vinson
tenselong-rangeodorsthatcanbeexploitedbytheirenemies. 1976).Ourreviewfocusesonchemicalcuesusedbyeggpara-
Additionally, many insect eggs develop rapidly, except when sitoids in the initial 2 stages of their host-selection behavior
theyenterdiapause,fromanutritionsourcetoacomplexem- beforehostcontacttakesplace,thatis,long-rangeandshort-
bryoandmightthereforebepresentonlyfor2–3days(Hinton rangehostlocation.Habitatlocationisgenerallymediatedby
1981).Manyeggsarewellprotectedphysicallyand/orchem- long-range cues, such as plant volatiles or herbivore phero-
ically(HilkerandMeiners2002a)becauseoftheirimmobility monesperceivedbyolfaction,whereascuesusedinthecloser
and exposure to enemies and environmental influences. vicinity are mostly short-range cues of herbivore products or
Some insects make their eggs less accessible by hiding them of theplant surfaceoftenperceived bygustatoryreceptors.
in plant tissue or by covering them with physical devices like Vet and Dicke (1992) stated that herbivore-foraging carni-
hairs, feces, scales, or secretion (Hinton 1981; Hilker 1994; vores face a reliability-detectability problem: infochemicals
Blum and Hilker 2002). Maternally incorporated or applied (sensu Dicke and Sabelis 1988; see Glossary) provided by
toxins provide protection against enemies (Hilker and the herbivore itself are reliable indicators of the herbivore’s
Meiners 1999; Blum and Hilker 2002; Bezzerides et al. 2004). presence, but their detectability is low due to 1) the small
Furthermore, insect host eggs are able to enhance transcrip- biomass of the herbivore relative to that of their host plant
tionofsomeimmune-relatedgenesinresponsetoparasitism and2)selectiononthehosttominimizetheemission.Onthe
(Abdel-latiefandHilker2008).Consequently,eggparasitoids other hand, plant-derived stimuli are supposed to be more
have to face many challenges when searching and finding detectable because they are available in larger quantities
theirsmall andinconspicuous hosts. and emitted over larger distances although they are not nec-
Female parasitoids are forced to optimize their host-selec- essarilyreliableindicatorsofthepresenceofthehost(Vetand
tionbehaviorbecauseitisdirectlylinkedtotheirreproductive Dicke 1992). It was assumed that the evolution of host loca-
success: the host is the only food source for their offspring tion is restricted by this reliability-detectability problem of
(Alphen van and Vet 1986). The parasitoids’ searching be- prey/host-derived infochemicals (Vet and Dicke 1992). The
havior can be divided into several phases (i.e., host habitat authorsproposed3solutionstothisproblem,namelyi)using
location, host location, and host acceptance), which are infochemicalsproducedbytheadulthoststage,suchaspher-
omones to locate eggs or larvae of the herbivore (termed
infochemicaldetour),ii)usingplantvolatilesinducedbyhost
feeding (termed herbivore-induced synomones or herbivore-
Address correspondence to N.E. Fatouros. E-mail: nina.fatouros@
wur.nl. induced plant volatiles), or iii) linking detectable cues with
Received 22 August 2007; revised 3 January 2008; accepted 7 reliable, host-derived cues through associativelearning.
January2008. Fromaneggparasitoids’pointofview,plantvolatilesinduced
byhostfeedingareindicatingthepresenceofthehostbutnot
(cid:1)TheAuthor2008.PublishedbyOxfordUniversityPressonbehalfof
theInternationalSocietyforBehavioralEcology.Allrightsreserved.
Forpermissions,pleasee-mail:[email protected]
678 BehavioralEcology
necessarily the presence of host eggs (coined ‘‘infochemical ulationortheproperhoststageisnotpresentanymore.Con-
detour’’ by Vet and Dicke 1992). However, a new example of sequently,eggparasitoidsneedtohaveaninnaterepertoireof
solution(ii)isavailable:eggparasitoidswererecentlyshownto responsestocuesassociatedwiththehosthabitat.Salt(1935)
use plant volatiles induced by egg deposition (Meiners and statedthatmostparasitoidsarefirstattractedtoacertaintype
Hilker 1997, 2000; Hilker et al. 2002; for reviews, see Hilker of environment and then to a particularhost. Vinson (1981)
andMeiners2002b,2006;Colazza,Fucarino,etal.2004;Mumm lists factors involved in habitat location such as sound, visual
and Hilker 2005, 2006). These oviposition-inducedplant cues cues, forms of electromagnetic radiation, and volatile chem-
were shown in laboratory bioassays to attract egg parasitoids, icals. Especially, plant volatiles may guide egg parasitoids to
whereas feeding-induced plant volatiles did not elicit any thehabitatoftheirherbivoroushosts(Weseloh1981;Vinson
behavioral response by the parasitoids. Thus, oviposition- 1991; Steidle and van Loon 2002). In general, infochemicals
induced cues are expected to be a more reliable solution for used by egg parasitoids forhost habitatlocation usually arise
theseeggparasitoidsthanplantcuesinducedbyhostfeeding. from sources associated with or connected to the host stage
Thisreviewcoversthediverseforagingbehaviorofeggpara- attackedratherthan from thehost egg itself.
sitoidswithrespecttotheuseofchemicalsignalsandoutlines
Volatilesfromundamaged plants
adaptive strategies that egg parasitoids employ to find their
A number of studies have shown Trichogramma spp. to re-
hosts. We divided the signals roughly into either category
spond to volatiles derived from undamaged plants or plant
long-rangeandshort-rangeinfochemicals.However,somecues
extracts (e.g., Bar et al. 1979; Altieri et al. 1982; Nordlund
mightnotfitintothe2categoriesbecausetheyareintermedi-
et al. 1985; Kaiser et al. 1989; Boo and Yang 1998; Reddy
ate orperceived bothovershort andlongdistances.
et al.2002;Romeisetal.2005)(Table1).However,itseems
that Trichogramma wasps and other egg parasitoids are gen-
LONG-RANGEINFOCHEMICALS erally arrested by plant volatiles after entering a habitat
rather than attracted from a distance (Romeis et al. 1997).
Plantcues
Due to their minute size, egg parasitoids like Trichogramma
When an adult egg parasitoid emerges from its host’s egg, it spp. are known to disperse passively by wind drifts rather
mayfinditselfinahabitatwhereinmostcasesthehostpop- thantoflydirectlytoanodorsource(Noldus,vanLenteren,
Table1
Responsetoplantcues
Eggparasitoid Host Source Response Reference
Scelionidae
Trissolcusbasalis Nezaraviridula Bean:infestedwithhost Attraction Colazza,Fucarino,etal.
adultsand3-to4-d-oldeggs (2004)andColazza,
McElfresh,andMillar
(2004)
Telenomuspodisi Euschistusheros Twolegumespecies: Attraction Moraesetal.(2005)
infestedwithhostadults
and/ornymphs
Eulophidae
Chrysonotomyiaruforum Diprionpini Pine:infestedwith3-d-old Arrestment Hilkeretal.(2002,2005)
hosteggmasses
Oomyzusgallerucae Xanthogalerucaluteola Elm:infestedwith3-hto5-d- Arrestment MeinersandHilker(1997,
oldhosteggmasses 2000)
Trichogrammatidae
Trichogrammasemifumatum Heliothisarmigera Tomato:plantsinfestedwith Increasedparasitism Baretal.(1979)
hosteggs inthefield
Trichogrammachilonis Helicoverpaarmigera Sorghumandpigeonpea: Arrestment Romeisetal.(1997)
uninfestedplants
Helicoverpaassulta Hotpepper:uninfested Arrestment BooandYang(1998)
plants
Plutellaxylostella Cabbage:syntheticgreen Attraction Reddyetal.(2002)
leafvolatiles
Trichogrammabrassicae(or Pierisbrassicae Brusselssprouts:leaves Arrestment Fatouros,
Trichogrammamaidis) infestedwith3-d-oldegg Bukovinszkine’Kiss,etal.
clutches (2005)
Ostrinianubilalis Maize:extractsin Arrestment Kaiseretal.(1989)
combinationwiththe
synthetichostpheromone
andhosteggs
Trichogrammapretiosum Ephestiakuehniella Weed:extracts Increasedparasitism Altierietal.(1982)
Spodopterafrugiperda Cotton:leavesinfestedwith Attraction Laumannetal.(2004)
hostcaterpillars
Heliothiszea Tomato:plantextracts Increasedparasitism Nordlundetal.(1985)
Myrmaridae
Anagrusnilaparvatae Nilaparvatalugens Rice:hostdamagedplants Attraction Louetal.(2005)
Anaphesiole LygusHesperus Variousplants:hostfeeding Attraction Manriqueetal.(2005)
(1/2eggdeposition)
Fatourosetal.•Foragingbehaviorofeggparasitoids 679
and Lewis 1991). Wind speeds in the open field make di- feeding-inducedvolatilescanbeadaptive,forexample,when
rected upwind flight for Trichogramma impossible, which all developmental stages co-occur on the same plant and an
was also demonstrated in wind tunnel experiments (Keller indirectassociationoffeedinghostadultsornymphswithegg
et al. 1985; Noldus, van Lenteren, and Lewis 1991). Yet, presence provides areliable cue.
withinthevegetationeitherclosetosoilorwithinthecanopy
effects of wind might be different from those in open areas
Hostcues
(reviewedbyMurlisetal.1992).Underlowwindconditions,
Trichogramma spp. were shown to disperse in all directions Withina(micro)habitat,eggparasitoidsareabletodistinguish
almost uniformly (see Fournier and Boivin 2000 and refer- infested from uninfested areas. This phase of their foraging
encestherein).TheeulophideggparasitoidOomyzusgalleru- behaviorcanbemediatedbycuesoriginatingfromadulthost
cae can be attracted by a synthetic plant compound to insects. Spying on the host communication system seems
freestandingstickytraps(MeinersT,unpublisheddata).This a common strategy in predatory and parasitic arthropods
indicates the capability of egg parasitoids to actively orien- (Vinson1984;Stoweetal.1995;Rutledge1996;ZukandKol-
tate in the field toward an odor source. luru 1998). Several signaling modalities, including acoustic,
visual, and olfactory information channels, are known to be
Herbivore-induced plantvolatiles exploited. Cues used for intraspecific communication are of-
Variousstudieshavedemonstratedthatplantsrespondtofeed- ten host specific and thus provide reliable information for
ingherbivoresbyinductionofvolatilesthatattracttheenemies eavesdropping enemies. Furthermore, they are often volatile
oftheherbivores(reviewedbyDickeetal.1990;DickeandVet pheromonal signals and cantherefore be detected overlong
1999; Dicke and van Loon 2000; Turlings et al. 2002). How- distances. Eavesdropping on such pheromones is effective
ever, plants can respond to insect oviposition by changing for parasitoids only when indicating the presence of the pre-
their release of volatiles prior to feeding damage by larvae. ferredhoststage(e.g.,Jonesetal.1973;Vinson1976;Weseloh
MeinersandHilker(1997,2000)werethefirsttodemonstrate 1981; Godfray 1994; Nordlund 1994; Hilker and Meiners
such ‘‘early alert’’: oviposition by the elm leaf beetle Xantho- 1999; Steidleandvan Loon2002) (Table2).
galerucaluteolainducesthefieldelm(Ulmusminor)toproduce
volatilesthatattracttheeggparasitoidO.gallerucae.Atthesite Exploitation ofsex pheromones
ofeggdeposition,theelmleafbeetleremovestheepidermis The use of volatile host pheromones by egg parasitoids was
of the leaf before laying eggs. However, the removal of plant shown forthefirsttimebyLewisetal.(1982)in studieswith
epidermaltissuepersedoesnotinducethevolatilesattracting Trichogramma pretiosum. Volatiles of the abdominal tips of fe-
O. gallerucae nor do the eggs release attractants, nor does male Heliothis zea moths as well as synthetic chemicals identi-
a combination of egg odor and plant volatiles attract the fied as the sex pheromone of H. zea females (hexadecanal,
eggparasitoids.Infact,theeggdepositioninducestherelease (Z)-7-hexadecenal,(Z)-9-hexadecenal,and(Z)-11-hexadecenal)
ofvolatilesfromelmleaves.Nevertheless,theremovalofplant increased parasitization rates by T. pretiosum. Later, follow-up
tissue is required for the volatile induction, as no attractive studies verified that T. pretiosum responds to calling H. zea
volatilesareemittedwheneggsaretransferredtointactleaves. females (Noldus 1988). Since then, more and more studies
Similar results were found in another tritrophic system demonstrate chemical espionage by egg parasitoids of sex
where the eulophid egg parasitoid, Chrysonotomyia ruforum, is pheromones of moths (e.g., Lewis et al. 1982; Nordlund
attractedbyvolatilesofScotspine(Pinussylvestris)inducedby et al. 1983; Noldus 1988; Noldus et al. 1990; Noldus, van
eggsofthesawflyDiprionpini(Hilkeretal.2002;Mummand Lenteren, and Lewis 1991; Frenoy et al. 1992; Arakaki et al.
Hilker2005).Thesawflydoesnotonlyremovetheplantepi- 1996, 1997; Colazza et al. 1997; Boo and Yang 2000; Reddy
dermiswhenovipositingbutalsoslitthepineneedlelongitu- et al. 2002; Scho¨ller and Prozell 2002; Fiaboe et al. 2003) or
dinallyto insert eggsin arow. sawflies (Hilker et al. 2000) (Table 2). Powell (1999) gives
In both the elm and the pine system, a specific response a detailed overview on the responses of egg parasitoids to
by specialized egg parasitoids toward egg-infested plants was sex pheromones from lepidopteran hosts.
demonstrated: neither the eggs alone nor the artificially However, a response of egg parasitoids to calling virgin fe-
damagedplantsmimickingtheoviposition-associatedwound- malemothsdoesnotnecessarilymeanaresponsetothehost
ing were arresting the egg parasitoids. The plant responses sex pheromone. Insome cases,the sex pheromone blendor
were both local and systemic: egg-laden plant parts as well main compounds of the virgin moths elicited no response
asuninfestedplantpartsnearpartswitheggsemittedattractive in the tested Trichogramma spp. (Noldus and van Lenteren
volatiles(MeinersandHilker2000;Hilkeret al.2002,2005). 1985a; Noldus et al. 1990; Frenoy et al. 1992; Renou et al.
Furtherstudiesshowedthatinsomeplantspeciesnotonly 1992).Here, thekairomoneseems tobeacompound associ-
egg deposition but also feeding of the adults is necessary to atedwithpheromoneproductionratherthanthepheromone
inducevolatilesattractingeggparasitoids(Colazza,Fucarino, itself.
et al. 2004; Colazza, McElfresh, and Millar 2004) (Table 1). Some authors suggest that a synergism between host plant
Colazza,Fucarino,etal.(2004)revealedthatageneralistegg and host sex pheromone may act as a ‘‘bridge in time’’ for
parasitoid, Trissolcus basalis, responds to plant synomones the chemical spies. Noldus, Potting, and Barendregt (1991)
emitted by 2 different bean species (Vicia faba and Phaeseolus showedthatthesexpheromoneofthefemalemothMamestra
vulgaris) that are induced by the pentatomid bug Nezara vir- brassicae adsorbs onto the leaf surface of cabbage plants to
idula. Attraction took place only when egg deposition oc- suchanextentthatfoliageexposedtothepheromoneattracts
curred together with plant damage, in this case feeding conspecific male moths and simultaneously arrested Trichog-
activity ofN. viridula.However,the eggswere laid ontheun- ramma evanescens females. Thiscouldbe a common phenom-
damaged plant part. Thus, also annual plants can produce enon because many hosts of which sex pheromones are
egg parasitoid–attracting synomones induced by insect egg exploited by a diurnal egg parasitoid are nocturnal moths
depositions. and the pheromone compounds are all long-chain fatty acid
Alsofeedingdamageofaplantalone(withouteggdeposi- derivatives with similar chemical properties that easily allow
tion)caninducevolatilesattractingeggparasitoids(Louetal. adsorbance to plant surfaces.
2005;Manriqueetal.2005;Moraesetal.2005)(Table1).Lou Arakaki et al. (1996) showed that Telenomus euproctidis is
et al. (2005) suggested that the egg parasitoid’s response to attractedtothesexpheromone[(Z)-16-methyl-9-heptadecenyl
680 BehavioralEcology
Table2
Responsetovolatilekairomonesofadulthosts
Eggparasitoid Host Source Response Reference
Scelionidae
Trissolcusbrochymenae Murgantiahistrionica Malesandfemales Attraction Contietal.(2003,2004)
Trissolcussimoni Eurydemaventrale
Nezaraviridula
Trissolcusbasalis N.viridula Matedfemalesin Attraction Mattiaccietal.(1993),
a‘‘preovipositionalstate’’ Colazzaetal.(1999),and
Virginmales Salernoetal.(2006)
Defensivemetathoracic
glandscent
Trissolcusutahensis Euschistusconspersus Syntheticaggregation Attractioninthefield KrupkeandBrunner
pheromone (2003)
Telenomusremus Spodopterafrugiperda Virginfemaleabdominal Attraction Nordlundetal.(1983)
tips
Syntheticsexpheromone Increasedparasitismrates
Telenomuseuproctidis Euproctidistaiwana Virginfemales Attractioninthefield Arakakietal.(1996)
Phoresy
Telenomuscalvus Podisusmaculiventris Males Attractioninthefield Brunietal.(2000)
Syntheticaggregation Phoresy Aldrichetal.(1984)and
pheromone Aldrich(1995)
Matedfemales
Telenomusisis Sesamiacalamistis Callingvirginfemales Arrestment Fiaboeetal.(2003)
Telenomusbusseolae Sesamianonagrioides Callingvirginfemales Attraction Colazzaetal.(1997)
Sesamiacalamistis Callingvirginfemales Arrestment Fiaboeetal.(2003)
Gyronpennsylvanicum Leptoglosssusaustralis Males Attractioninthefield YasudaandTsurumachi
Increasedparasitism (1995)andYasuda(1998)
Eulophidae
Chrysonotomyiaruforum Diprionpini Syntheticsexpheromone Arrestment Hilkeretal.(2000)
Neodiprionsertifer
Dipriocampediprioni D.pini
Entodonleucogramma Scolytusmultistriatus Syntheticaggregation Attractioninthefield Kennedy(1984)
pheromone
Encyrtidae
Ooencyrtusnezarae Riptortusclavatus Syntheticaggregation Attractioninthefield Lealetal.(1995)and
pheromoneofmalebugs Mizutani(2006)
Ooencyrtuspityocampae Thaumetopoeapityocampa Virginfemales Attractioninthefield Battisti(1989)
Trichogrammatidae
Lathromerisovicida Sesamiacalamistis Callingvirginfemales Arrestment Fiaboeetal.(2003)
Uscanalariophaga Callosobruchusmaculates Virginfemales Attraction vanHuisetal.(1994)
Trichogrammaevanescens Ephestiaspp. Syntheticsexpheromone Arrestment Scho¨llerandProzell(2002)
Plodiainterpunctella
Pectinophoragossypiella Syntheticcomponentsof Attraction Zaki(1985)
Spodopteralittoralis sexpheromone
Eariasinsulana
Trichogrammabrassicae(or Pierisbrassicae Matedfemalebutterflies Arrestment Fatouros,Huigensetal.
Trichogrammamaidis) Syntheticantisex Phoresy (2005)
pheromone
Ostrinianubilalis Callingvirginfemales Attraction Frenoyetal.(1992)
Noresponsetomainsex Kaiseretal.(1989)
pheromonecomponent
Eggs1pheromonal
blend1maizeextract
Lobesiabotrana Callingvirginfemales Increaseinmovement Garnier-Geoffroyetal.
Increasedparasitism (1999)
Trichogrammapretiosum Heliothis/Helicoverpazea Abdominaltips Increasedparasitism Lewisetal.(1982),Gross
Excretionandsyntheticsex Arrestment etal.(1984),andNoldus
pheromoneofvirgin etal.(1990)
females
Callingvirginfemales Arrestment Noldus(1988)
Plutellaxylostella Syntheticcompoundofsex Increasedparasitism KlemmandSchmutterer
pheromone (1993)
Trichogrammasibericum Rhodobotanaevana Maincomponentofsex Increasedsearchingtime, McGregorandHenderson
pheromone arrestment (1998)
Trichogrammaostriniae Ostriniafurnacalis Matedfemalemoths Attraction Baietal.(2004)
(beforeoviposition)
Accessoryglandsofmated
females
Trichogrammaoleae Palpitaunionalis Syntheticsexpheromone Higherparasitization, Abdelgaderand
attraction Mazomenos(2002)
Prayspleae Sexpheromone Attraction Milonasetal.(2003)
components
Fatourosetal.•Foragingbehaviorofeggparasitoids 681
Table2, continued
Eggparasitoid Host Source Response Reference
Trichogrammaevanescens Mamestrabrassicae Callingvirginfemales Arrestment NoldusandvanLenteren
later Hostsexpheromoneodor Arrestment (1985a),Noldus,Potting,
Trichogrammamaidis Noresponsetomainsex andBarendregt(1991)
(=Trichogrammabrassicae) pheromonecomponent
P.brassicae Virginfemalesin‘‘mate- Arrestment NoldusandvanLenteren
acceptanceposture,’’nosex (1985a)
pheromoneknown
Trichogrammachilonis Helicoverpaassulta Sexpheromoneofvirgin Arrestment BooandYang(2000)
moths
Maincomponentofsex
pheromone
Plutellaxylostella Syntheticsexpheromone Attraction Reddyetal.(2002)
blend
Trichogrammacordubensis Heliothisarmigera Adultfemalemoth Attraction CitedbyNoldus(1989)
Eariasinsulana
Trichogrammasp.nr.buesi Ephestiakuehniella Adultfemalemoth Attraction CitedbyNoldus(1989)
isobutyrate]ofvirgintussockmoths(Euproctistaiwana)beforeit widespreadthansofarassumed.Eavesdroppingonthehost’s
mounts them, hiding in the anal tuft until the female moth sexual communication is supposed tobe a stable strategy be-
startslayinghereggclutch.Thephoreticwaspswerestillable cause the host is probably under strong selection pressure
todetecttraceamountsofthehostsexpheromoneeven48h not to change the chemistry of its intraspecific signals. How-
after release, being retained on moth scale hairs at the anal ever, the detectability of sexual signals can be temporally re-
tufts,thusemployinganotherbridge-in-timestrategy(Arakaki stricted. Additionally, sexual host signals can be emitted far
andWakamura2000). fromovipositionsites,whichlimittheriskofhosteggstobe-
comeexploited.Therefore,sexualhostsignalsmaybeoflim-
Exploitationofantisexpheromones itedreliabilityforeggparasitoids(SteidleandvanLoon2002).
Forthefirsttime,Fatouros,Huigens,etal.(2005)showedthat Unlikeexploitationofantiaphrodisiacsofmatedhostfemales,
an egg parasitoid (Trichogramma brassicae) exploits an antisex exploiting the sex pheromone of virgin females does noten-
pheromone of its host, in this case the large cabbage white sure the egg parasitoid any access to host eggs because the
(Pierisbrassicae).Theantiaphrodisiac,benzylcyanide,istrans- host female still has to find a mate before it can oviposit.
ferred from Pieris males to females during mating to render Except for phoretic egg parasitoids, many studies still show
the females less attractive to conspecific mates (Andersson that the use of sexual signals can be beneficial for egg para-
et al. 2003). Mated host females were most attractive to the sitoids: plants sprayed with synthetic pheromones arrest egg
wasps;unlikeinmostothercasesofchemicalespionagewhere parasitoids, stimulate intensive searching behavior in these
virgin females lured egg parasitoids. To examine the impor- areas, and increase the probability to encounter host eggs
tanceoftheantiaphrodisiacforphoresyinT.brassicae,benzyl resultinginhighparasitismrates(Lewisetal.1982;Nordlund
cyanidewasappliedontovirginfemales.Indeed,theapplica- et al.1983).
tionoftheantiaphrodisiacrenderedthevirginfemalesattrac-
tive to the wasps and stimulated them to mount their hosts. Exploitation ofaggregationpheromones
Flight chamber experiments demonstrated that the wasps Insectpheromonesthatattractbothsexestoaparticulararea
were able to hitchhike on the butterflies until these landed are termed aggregation pheromones (Shorey 1973). They
ontheirhostplant,thendismountedthehost,andparasitized functionaslong-rangesignalsandareknowntobeexploited
thefreshly laid host eggs(Fatouros, Huigens,et al.2005). byseveralparasitoids(Powell1999).InHeteroptera,aggrega-
Other studies indicated an attraction of egg parasitoids to tion pheromones are emitted by male bugs (Aldrich 1995).
mated host females (Colazza et al. 1999; Conti et al. 2003; Mating and oviposition often occur in the same area where
Bai et al. 2004). Bai et al. (2004) found that Trichogramma these aggregation pheromones are emitted, which makes
ostriniae responded positively to odor from gravid females of them a potential host location cue for egg parasitoids. Fe-
their host, the Asian corn borer (Ostrinia furnacalis). Virgin males and males of the leaf-footed plant bug (Leptoglossus
host females and mated host females after their first oviposi- australis),aswellastheireggparasitoidGryonpennsylvanicum,
tion did not elicit any response. This specific response to were captured by traps baited with male bugs but never in
gravid host females could indicate the presence of an antia- traps with females bugs, which indicates the presence of
phrodisiac in the Asian corn borer. In Pieris napi butterflies, a male-derived pheromone acting as a kairomone for the
eggdepositionisfollowedbyareductioninthetiteroftheir wasps (Yasuda 1998). Additionally, parasitization was in-
antiaphrodisiac pheromone (Andersson et al. 2004). Trichog- creased when cages with male bugs were placed next to host
ramma ostriniae might be attracted to just-mated but still ovi- eggs(YasudaandTsurumachi1995).
positionnaivehostfemalesbecauseoftheirhighpheromone Telenomus calvus is a specialized phoretic egg parasitoid of
titer. Host females that have already oviposited might have the spined soldier bug Podisus maculiventris. The wasps are
a lower antiaphrodisiac titer, which renders them less detect- known to utilize the aggregation pheromone of the male
abletothe parasitoids. bugs, a-terpineol, to come in the host male’s vicinity and to
In sexually reproducing species, mated females might pro- wait for female bugs to arrive, whereupon they become pho-
videmorereliablecuesforhost-searchingeggparasitoidsthan retic after the female bug finishes mating (Buschman and
virginones becausematedones areclosertoeggdeposition. Whitcomb 1980; Aldrich et al. 1984; Aldrich 1995). It is as-
Theexploitationofantiaphrodisiacsorsimilarvolatilephero- sumed that the wasps recognize the female bugs through fe-
monesofmatedhostfemalesbyeggparasitoidscouldbemore male-specific volatiles that are produced by small glands
682 BehavioralEcology
underneath the wings. Besides spying on the 2 host phero- host cues is especially important with those host species in
mones, Te. calvus also possesses a number of behavioral and which oviposition occurs away from mating and feeding site
biologicaladaptationstofacilitatephoresy,whichmakesitan likeinthecaseofN.viridula.Chemicaltracesfromadulthosts
efficient phoretic parasitoid (Orr et al. 1986). Some females werealsoshowntobeusedbyotherscelionidwaspsinfinding
of the nonphoretic, more generalistic Telenomus podisi were bug eggs (Chabi-Olaye et al. 2001; Borges et al. 2003; Conti
caught in male-pheromone–baited traps of P. maculiventris etal.2004;Perietal.2006;Salernoetal.2006).Thisempha-
too(Aldrich1985)butdidnotdiscriminatebetweenhosteggs sizes again the importance of the adult host stage for egg
placedintrapsbaitedwiththesyntheticmalepheromoneand parasitoids.
unbaited traps (Bruni et al. 2000). This implies that the syn- Fecalvolatilesofbothlarvaeandadultsoftheelmleafbeetle
thetic pheromone does not affect the searching behavior of (X. luteola) were attractive to its egg parasitoid O. gallerucae
thenonphoreticTe.podisifemaleslikeitdoesinthephoretic (Meiners and Hilker 1997). However, eggs, gravid females,
Te. calvus. It was assumed that Te. calvus relies on other cues orthelarvaethemselveswerenotattractiveintheolfactome-
suchasinfochemicalsoftheeggsorthehostsubstrate(Bruni ter. A substrate contaminated with feces of chrysomelids also
et al.2000). arrested 2 eulophid egg parasitoid species when they had
antennal contact with the contaminated site (Meiners and
Hilker 1997; Meiners et al. 1997). Besides plant odors (see
CLOSERANGEANDCONTACTINFOCHEMICALS above), O. gallerucae uses cues from host feces for location
of the elm leaf beetle’s microhabitat. The beetle’s feces also
Plantcues
actasacontactkairomoneformicrohabitatacceptance.Kair-
Afterlandingonahostplant,eggparasitoidsmainlyusecon- omonesisolatedfromthehosteggsthemselveswereonlyused
tact or short-range volatiles that indicate the presence of the forhostrecognition (MeinersandHilker 1997).
host or more specifically its eggs. Studies by Fatouros, Yet,insomecases,airbornechemicalsofthehosteggsthem-
Bukovinszkine’Kiss, et al. (2005) indicate thatphytochemical selveswereshowntostimulateanintensivesearchbehaviorin
changesin theleaf surface of Brussels sprout plants induced egg parasitoids (Frenoy et al. 1992; Renou et al. 1992;
by eggs of P. brassicae arrest T. brassicae (Table 1). However, Hofstetter and Raffa 1998; DeLury et al. 1999; Bai et al.
no indication was found that egg deposition of P. brassicae 2004; Yong et al. 2007). Analysis of the eggs of Ostrinia nubi-
induces volatiles that are used by the egg parasitoid for host lalis and M. brassicae revealed the presence of various com-
location. Unlike in the other systems where egg deposition pounds on the egg surface such as hydrocarbons being
induces volatile plant cues (see above), the Pieris butterfly is responsibleforthekairomonalactivityonT.brassicae(Renou
not severely damaging the leaf of a Brussels sprout plant be- et al. 1989, 1992). However, other Trichogramma spp. did not
fore or during oviposition. The response of the plant seems react to host eggs from a short distance (Laing 1937; Kaiser
restricted to leaf surface modifications. Molecular evidence et al. 1989). In many cases, kairomones present on the egg
confirmed a locally restricted plant response to P. brassicae surface act at short range and thus play a role in host egg
eggdepositioninArabidopsis(Littleetal.2007).Itisassumed recognition (e.g., Strand and Vinson 1982; Leonard et al.
that chemical changes of the pattern of compounds in the 1987; Nordlund et al. 1987; Pak and De Jong 1987; Bin
wax layer are induced that guide the egg parasitoids to suit- et al. 1993; Meiners and Hilker 1997; Meiners et al. 1997;
able host eggs after landing on the host plant. Also other Contietal.2003).Ingeneral,itisnotexpectedthathosteggs
short-rangeplantcuesthancuticularwaxescouldplayarole: elicitchemical long-range attraction inegg parasitoids.
egg deposition is able to reduce the plant’s photosynthetic
activity (Schro¨der et al. 2005), and thus, closure of stomata
INFOCHEMICALUSEINATRITROPHIC CONTEXT
mayaffect the gaseousleafboundary layer.
Asoutlinedabove,theforagingbehaviorofeggparasitoidsis
stronglyaffected bychemicalcuesfrom thefirst andthesec-
Hostcues
ondtrophiclevel.VetandDicke(1992)offeredaconceptual
Laing(1937)wasthefirsttoreportarrestmentofT.evanescens framework by placing the ecology and evolution of info-
waspsbychemicaltracesleftbythegrainmothSitotrogacereal- chemical use by herbivore-foraging carnivores in a tritrophic
ella.Later,Lewisetal.(1971,1972)foundthatwingscalesleft context. The central problem of foraging carnivores is the
byovipositingH.zeaorPlodiainterpunctellamothswereusedas reliability-detectability problem of infochemicals. Vet and
kairomones by T. evanescens. Several follow-up studies showed Dicke (1992) mentioned 3 solutions for this problem, which
a response of egg (larval) parasitoids to residues of the adult wewilldiscusswithrespecttoeggparasitoids(seealsointhe
host,suchaswingscalesofbutterfliesormoths(e.g.,Noldusand Introduction). Furthermore, they proposed some general
vanLenteren1985b;Zaborskietal.1987;ShuandJones1989; rules that predict how parasitoids solve the reliability-detect-
ThomsonandStinner1990;Fatouros,Bukovinszkine’Kiss,etal. ability problem. Parasitoids specialized at the host and host
2005; Yong et al. 2007), chemical traces of walking bugs plant level are expected to use different foraging strategies
(Colazza et al. 1999; Borges et al. 2003; Conti et al. 2003, and thus different infochemicals than those parasitizing nu-
2004;Salernoetal.2006),oramarkingpheromoneofafruit merous hosts, which are polyphagous herbivores themselves.
fly(RoitbergandLalonde1991)(compareTable3).Jonesetal. Thus, the parasitoids’ behavioral response to a cue depends
(1973) found hydrocarbons like tricosane in wing scales of notonlyontheirdegreeofdietaryspecializationbutalsoon
H. zea as biologically active cues, eliciting significant orienta- the dietary specialization of their host species. The used in-
tion and stimulation of parasitism by T. evanescens. Similar fochemicalscanbeeitherspecificforacertainhostcomplex
findingsonotherTrichogrammaspp.usinghydrocarbonswere or generally present in various complexes, and responses to
publishedbyLewisetal.(1975),Shuetal.(1990),Padmavathi thecuescan beeither innateorlearned.
andPaul(1998),andPauletal.(2002).Colazzaetal.(2007)
revealedthatn-nonadecane,acuticularhydrocarbonreleased
Dietaryspecializationineggparasitoids
bythetarsiandscutellaoffemaleN.viridulabugshadakair-
omonalactivityontheeggparasitoidTr.basalisactingasa‘‘host- Egg parasitoids like Trichogramma species are known to be
gender recognition’’ cue for the egg parasitoids. The fairly polyphagous, parasitizing a broad range of hosts espe-
significance of discriminating female host cues from male ciallyoftheinsectorderLepidoptera(ThomsonandStinner
Fatourosetal.•Foragingbehaviorofeggparasitoids 683
Table3
Responsestoadulthostresidues
Eggparasitoid Host Source Response Reference
Scelionidae
Trissolcusbrochymenae Murgantiahistrionica Chemicaltracesfrom Arrestment Contietal.(2003,2004)
Trissolcussimoni Eurydemaventrale adulthosts
Nezaraviridula
Trissolcusbasalis N.viridula Chemicaltracesof Arrestment Colazzaetal.(1999),
virginmalesandmated Perietal.(2006),and
femalesin Salernoetal.(2006)
a‘‘preovipositional
state’’
n-nonadecane,cuticular Colazzaetal.(2007)
hydrocarbonoffemale
hosts
Telenomuspodisi Euschistusheros Chemicaltracesby Arrestment Borgesetal.(2003)
walkingfemalehosts
Telenomusisis Sesamiacalamistis Chemicaltracesby Arrestment Chabi-Olayeetal.
virginandmated (2001)
females
Eulophidae
Oomyzusgalerucivorus Galerucatanaceti Adultfecesonsubstrate Arrestment Meinersetal.(1997)
Oomyzusgallerucae Xanthogalerucaluteola Adultfecesonsubstrate Arrestment MeinersandHilker
Volatilesoffecesofhost (1997)
adultsandlarvae
Trichogrammatidae
Trichogramma Pierisbrassicae Cabbageleavestreated Arrestment Noldusandvan
evanescens(later Pierisrapae withwingscalesfrom Lenteren(1985b)and
Trichogrammamaidis Mamestrabrassicae adultfemalehosts Gardnerandvan
nowTrichogramma Lenteren(1986)
brassicae)
Trichogrammabrassicae Ostrinianubilali Chemicaltrailofmoth Arrestment Garnier-Geoffroyetal.
females (1996)
Scaleextractsand Increasedparasitism Grenieretal.(1993)
saturatedhydrocarbons
Trichogramma Pierisbrassicae Bodyscalesandtracesof Fatouros,
brassicae adulthosts Bukovinszkine’Kissetal.
(2005)
Trichogramma Heliothiszea Bodyscalesandtheir Arrestmentand Lewisetal.(1971,1972)
evanescens hexaneextracts increasedparasitism andJonesetal.(1973)
Plodiainterpunctella Tricosanefromscale
extracts
Sitotrogacerealella Tracesofadulthosts Arrestment Laing(1937)
Mamestrabrassicae
Choristoneurafumiferana Hexaneextractsfrom Arrestment SchmidtandCarter
scales (1992)
Trichogramma H.zea Hexaneextractsfrom Increasedparasitism Grossetal.(1984)and
pretiosum scales Gueldneretal.(1984)
Acidsinscalefractions
Trichogrammanubilale Ostrinianubilalis Mothscaleextracts Increasedparasitism ShuandJones(1989)
Saturatedhydrocarbon andarrestment andShuetal.(1990)
fraction
Trichogramma Choristoneurafumiferana Hexaneextractsof Arrestment Zaborskietal.(1987)
minutum scales
Trichogrammachilonis Corcyracephalonica Saturated Increasedparasitism PadmavathiandPaul
Trichogramma hydrocarbons,mainly (1998)andPauletal.
brasiliensis tricosane (2002)
Trichogrammaexiguum
Trichogrammaostriniae Ostriniafurnacalis Volatilesofhostscales Attraction Yongetal.(2007)
Braconidae
Ascogaster Cydiapomonella Volatilesofhostscales Attraction DeLuryetal.(1999)
quadridenata
Pteromalidae
Halticopterarosae Rhagoletisbasiola Markingpheromoneof Increasedparasitism RoitbergandLalonde
femaleflies andarrestment (1991)
1990; Pinto and Stouthamer 1994). However, host ranges of Trichogramma spp. being more prevalent in certain habitats
Trichogramma spp. are mainly determined in the laboratory, or onspecific plants (reviewed by Romeiset al. 2005)proba-
where they tend to be broader than in the field (reviewed bly due to their limited moving abilities. Plant structure,
by Romeis et al. 2005). Still, there is growing evidence for host density and distribution, and other (micro)habitat
684 BehavioralEcology
Table4
Responsetokairomonesassociatedwithhosteggs
Eggparasitoid Host Source Response Reference
Scelionidae
Trissolcusbrochymenae Murgantiahistrionica Eggs Arrestment Contietal.(2003)
Eggextracts Increaseinencounters
Eulophidae
Ooencyrtuskuvanae Lymantriadispar Airbornechemicalsoffresh Arrestment HofstetterandRaffa(1998)
eggmasses
Accessoryglandsecretion
Edovumputtleri Leptinotarsadecemlineata Eggwash Arrestment Leonardetal.(1987)
Trichogrammatidae
Trichogrammaevanescens Pierisbrassicae Eggwash Arrestment NoldusandvanLenteren
laterTrichogrammamaidis (1985b)
(=Trichogrammabrassicae)
Trichogrammaostriniae Ostriniafurnacalis Airbornechemicalsofegg Arrestmentandattraction Baietal.(2004)andYong
masses etal.(2007)
Accessoryglandsecretion
ofmatedhostfemales
Trichogrammabrassicae(or Pierisbrassicae Accessoryglandsecretion Arrestment Fatouros(2006)
Trichogrammamaidis) ofmatedhostfemales
Ostriniamubilalis Airbornechemicalsofegg Increasedmobilityand Frenoyetal.(1992),Renou
massesSurfaceextractsof arrestment etal.(1989,1992)
eggmasses
specificitiesmightvaryandinfluencethehost-foragingbehav- foreoftenlimitedintheir flightcapabilities.Sofar,about30
iorofeggparasitoids(GingrasandBoivin2002;Romeisetal. eggparasitoidspeciesareknowntobephoreticontheiradult
2005). This habitat/plant loyalty could narrow their host hosts (Fatouros 2006). Thus, we expect that chemical espio-
range. Certainly, egg parasitoids in monocultures or habitats nage on adult host pheromones sometimes in combination
of low biodiversity will encounter only a small range of host withphoresytobeastrategycommonlyusedbyeggparasitoids
species.Theuncertaintyofthehostrangeinthefieldaswell tosolve thereliability-detectability problem.
aswrongspeciesdeterminationsinthepastmakeitdifficultto
putTrichogrammaspp.intocategoriesasgeneralistsorspecial-
Plantvolatilesinducedbyeggdepositionand/orfeeding
ists. This means that the dietary specialization aspects of Vet
andDicke(1992)aredifficulttoapplyonTrichogrammaspp.as Eggparasitoidsofherbivoroushostsdevelopedtouseathirdso
longastheirhost specificity remains poorly known. far underestimated solution, mentioned by Vet and Dicke
Here, we try to find a general concept for egg parasitoids, (1992): plant volatiles induced by herbivore infestation. This
dealingwiththemajorconstraintsofeggparasitoidsconcern- could solve the detectability problem that egg parasitoids
ing the host like: a small size, sessile and inconspicuous life face.Here,theyareknowntofollow2differentstrategies:plant
stage, and usually limited temporal availability. Apart from volatiles induced by herbivore feeding or by egg deposition.
a generally short longevity, egg parasitoids, like Trichogramma Bothtypesofplantcuescanbespecificinindicatingthepres-
spp., are known to be restricted to passive downwind move- ence of host eggs and thus play important roles for the host
mentsorwalkingandjumping.Whicharethemaininfochem- locationprocessineggparasitoids:sofarabout10specieswere
ical strategies used in theirlong-distance searchforhosts? showntorelyonsuchplantsynomones(seeTable1).
Fromtheplant’spointofview,anattractionofparasitoids/
predators to eggs deposited on the plant might have a great
Infochemicaldetour:theimportanceoftheadulthoststage
advantage because herbivore larvae are killed before they
Eggparasitoidsseemtoheavilyrelyontheadulthoststagein canstartfeeding.Especially,annualplants(withasmallerbio-
allphasesoftheirhost-selectionprocess.Pheromonesandres- massandshorterlifetime)areexpectedtobenefitfromsuch
iduesofhostfemalesandsometimesmaleshavealargeimpact anindirect defensemechanism (Hilker andMeiners2002b).
onindirectlylocatingeggsofmoths,butterflies,bugs,beetles, From the egg parasitoid’s perspective, it remains unclear
flies,orsawflies:sofarabout34differenteggparasitoidspecies when it is beneficial to use oviposition-induced plant cues to
were shown to use adult host cues(see Tables 2and 3)com- locatetheirhostsandwhentheuseoffeeding-inducedplant
pared with only about 6 species that were shown to use host volatiles becomes adaptive. Generally, plant volatiles induced
cues from the host eggs themselves (Table 4). In most cases, by feeding damage should be more abundant due to the
egg-derived stimuli mediate host-recognition behavior (see greater plant damage than plant volatiles induced after egg
above).Consequently,thisinfochemicaldetourbyemploying deposition by herbivores. However, a response to feeding-in-
kairomonesoftheadulthostseemsanimportantstrategyfor duced plant volatiles should be only adaptive to egg parasi-
many egg parasitoids. In contrast, only few larval or pupal toids when they provide reliable information, for example,
parasitoidswereshowntospyonadultsex,marking,oraggre- when host generations overlap and different developmental
gationpheromones(Corteseroetal.1993;Wiskerkeetal.1993; stagesco-occurontheplant.Ontheotherhand,aresponseof
Zaki1996;HoffmeisterandGienapp1999;Reddyetal.2002). eggparasitoidstooviposition-inducedplantvolatilesrequires
Besides an arresting effect to areas likely to contain host fine-tuned sensory abilities, especially when the induction by
eggs,adulthostpheromonesmayhaveamuchgreaterimpor- feedinginducesastrongerresponseintheplantthaneggsdo.
tancetophoreticeggparasitoids.Amongparasitoids,phoresy Such perceptive abilities are likely present mainly in systems
is almost exclusively performed by egg parasitoids, which are where the first and third trophic levels specialized on each
smaller,comparedwithlarvalorpupalparasitoidsandthere- otherover evolutionary time.
Fatourosetal.•Foragingbehaviorofeggparasitoids 685
Weexpectsuchanindirectplantresponsetoeggdeposition conspicuouseggsmightrequirenumerousforagingdecisions,
byreleaseofplantvolatilesattractivetotheeggparasitoidsin which could be optimized by the ability to learn. Vet et al.
those systems where 1) wounding is involved during oviposi- (1995)furtherhypothesizedthatiflearningoccurs,thenthis
tion and 2) the egg parasitoid has the capability to actively ismostlikelytooccurinthemorepolyphagouseggparasitoid
orient to an odor source by walking, jumping, or flying. If species that attack hosts that lay spatially separated single
no simultaneous wounding occurs (either by egg deposition eggs. Yet, also specialist egg parasitoid species searching for
orbyadultorlarvalfeeding), weexpectnoinductionof vol- hosts in a variable chemical environment may benefit from
atilesbytheplantbutshort-rangecues,likelytoberestrictedto theabilitytoassociatehost-indicating chemicalswithpositive
theplantsurfaceandperceivedbytheeggparasitoidonlyin experience,asissuggestedbythestudiesonthespecialistegg
closevicinity (see Fatouros,Bukovinszkine’Kiss, etal. 2005). parasitoid C. ruforum that needs to learn oviposition-induced
plant synomones (seeabove).
Theinfluenceofexperienceandassociativelearning Generalpatternsineggparasitoid–foraging strategies
According to Vet et al. (1990), a response to infochemicals To reach (new) habitats, egg parasitoids have to move over
wasconsideredaslearnedwhenitwasobservedinonlyexpe- larger distances. They can achieve this by spreading passively
rienced insects after having encountered host/prey or host by windorby using largerhostsfortransportation (phoresy)
plant/feeding substrates. Associative learning by connecting (see Figure 1). Both ways implicate a momentum of chance
anunconditionedstimulus,alwayshostderived,withacondi- either by coming down at the right spot in the landscape or
tioned stimulus is frequently observed in parasitoids. Gener- by sitting at the right place to catcha suitable host for trans-
ally, responses of carnivores to host-derived kairomones are portation.However,eggparasitoidsmightusegeneralabiotic
fixed, whereas responses to plant volatiles are more variable or biotic habitat cues or cues of host encounter places (like
and are learned mostly during adult foraging (Vet and Dicke flowerheads)toenhancethechancetoreachasuitablehab-
1992).Immatureparasitoidscanalsogainexperiencewithcer- itat.Ontheotherhand,weexpectdirectedorientationofegg
tainstimulithroughdevelopmentinsidethehost(Corbet1985). parasitoids to hosts over a smaller distance. In closer vicinity
Severalstudiesshowthatlearningofplantcuesduringfor- to host eggs, both host cues (if available in sufficient quanti-
aging in egg parasitoids does occur frequently. For example, ties)andplantcuesmightplayequallyimportantrolesforthe
experienceduringemergencemodifiedthesearchingbehav-
ior of 1 of the 2 tested T. nr brassicae strains toward plant
stimuli: females that emerged from their host on a tomato
plant subsequently searched a tomato leaf longer than fe-
malesemerginginavialwithoutplantstimuli.Whencompar-
ing a preadult experience with the effect of adult learning
through an oviposition experience on host preference in 2
strains of T. nr ivelae, it was shown that adult experience
had a stronger effect than learning through development
insidethehost (Bjorksten andHoffmann 1998).
Responding to oviposition-induced plant cues requires ex-
periencewiththeplant–hostcomplexbysomeeggparasitoids
studiedsofar(e.g., Fatouros,Bukovinszkine’Kiss, etal.2005;
Mumm et al. 2005), whereas others respond innately (e.g.,
Meiners and Hilker 2000; Colazza, Fucarino et al. 2004;
Meiners T, unpublished data). The necessity of experience
to respond to oviposition-induced pine odor might be an
adaptation to the high intraindividual and intraspecific vari-
ability ofpinevolatile blends (Mumm andHilker 2006).
Eggparasitoidsoftenexploithostcuesinnately,forexample,
T.brassicaeabutterflyantisexpheromone(Fatouros,Huigens,
et al. 2005) or C. ruforum the sex pheromones of sawflies
(Hilker et al. 2000). But even such specific host cues like
sex and antisex pheromones need to be learned by some
egg parasitoid species, as was shown for Trichogramma species
(e.g., Kaiser et al. 1989; Scho¨ller and Prozell 2002; Fatouros
etal.2007;FatourosandHuigens,unpublisheddata).Besides
Figure1
Trichogramma spp., also a scelionid wasp was shown to use
Thegeneralhostlocationbehaviorofeggparasitoidsandthe
associative learning that enhanced its arrestment response
possibleinfochemicalsinvolvedareshownonthebasisofavirtual
to host female residues after an oviposition experience (Peri
system.Aftereclosion,aneggparasitoidcanchoosetoremaininthe
et al. 2006). In conclusion, the host range of egg parasitoids samehabitatandsearchforahostplantortochangetoanew
seemsnottoaffecttheabilitytolearncertaincues.However, habitat.Toreachhabitats,thewasphas2possibilities:A)bychance
complexandvariablecuesoftenneedtobeexperiencedfirst anddriftpassivelywiththewindorB)bysearchingadulthostsfor
beforebeingused. transportation(phoresy).Byusingcuesoftheadulthost,eitherto
Vetetal.(1995)statedthatlearningofforagingcuesbyegg directlyfindthehostplantanddepositedherbivorouseggsorto
parasitoids is not expected. The more foraging decisions achievephoresy,eggparasitoidsareshowntorelyontheadulthost
stagemorethanotherparasitoidsdo.Besideshostpheromones,
awaspmakesthemorelikelyinfochemicallearningbecomes
herbivore-inducedplantvolatiles(inducedbyeggdepositionor
adaptive. The high availability of eggs (compared with other
feeding)seemtohaveasofarunderestimatedimpactonthe
stagessuchaslarvaeorpupae)andtheshortlongevityofegg
host-foragingbehaviorofeggparasitoids.Theparasitoids’response
parasitoidsincombinationwiththeirlimitedabilitytosearch toalltypesofinfochemicalsshownmaybeinnateorlearned
may restrain the number of foraging decisions that lead to (seetextformoredetails).R=reliablecue,D=detectablecue,
host encounters. However, the low detectability of mostly in- HIPV=herbivore-inducedplantvolatiles.
686 BehavioralEcology
host location process depending on factors such as learning Synomone:Aninfochemicalofanorganismthatonemission
capabilities orthedietary specialization of theegg parasitoid evokes in the receiver, an individual of a different species,
andits host. a behavioral or physiological response adaptively favorable
Tofullyunderstandinfochemical-exploitingstrategiesusedby toboth receiver andemitter.
foraging egg parasitoids, it is necessary to study plant–host– Chemical espionage: Exploiting intraspecific communication
parasitoidinteractionsatdifferentscalesinthefield.Hereafter, throughinfochemicalsbyathirdorganismforitsownben-
the mechanism of infochemically mediated host searching efit,whichisdetrimentalfortheorganismsthatcommuni-
shouldbeinvestigatedexperimentally.Furthermore,behavioral cateintraspecifically.
and electrophysiological investigations should provide infor- Phoresy: The transport of one organism (phoront) on the
mationontheidentityofthechemicalsthateggparasitoidsuse. bodyofanotherforalimitedtimeperiodandforpurposes
other thandirect parasitism.
CONCLUSIONS
FUNDING
Thispapersummarizestheextensiveresearchconductedsofar
ontheroleofinfochemicalusebyeggparasitoidsduringhost NetherlandsOrganizationforScientificResearchTechnology,
foraging.Eggparasitoidsplayanimportantroleinbiological (NWO-ALW VICI grant 865.03.002 to M.D. and R.M.);
controlprogramsofpestinsects.Understandingtheirhostlo- European Commission contract (MC-RTN-CT-2003-504720
cation behavior is a crucial step for a targeted application of ‘‘ISONET’’toR.M.andM.D.);GermanResearchFoundation
parasitoidsincropfieldsandgreenhouses.Ageneralpattern (DFGFA824/1-11 to N.E.F.).
ofstrategieshasbeenhighlightedhere:duetotheinconspic-
uousnessofhosteggs,eggparasitoidshavedevelopedvarious The authors thank Martinus E. Huigens and Tibor Bukovinszky for
so-calledinfochemicaldetourstrategiestolocatetheirhidden discussionandcommentsonthemanuscript.
hosts.Thisinfochemicaldetourviaspecificcuesfromtheadult
hoststage,sometimesincombinationwithphoresy,orviacues
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GLOSSARY extractsontheratesofparasitizationofAnagastakuehniella(Lep.:
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Parasitoid: Insects that lay their eggs on or in other insects
dae)undergreenhouseconditions.Entomophaga.27:431–438.
(or sometimes other invertebrates). The hatching larvae AnderssonJ,Borg-KarlsonA-K,WiklundC.2003.Antiaphrodisiacsin
thenliveparasiticonthehostandeventuallykillit,whereas Pierid butterflies: a theme with variation! J Chem Ecol. 29:
theadults arefreeliving. 1489–1499.
Infochemical: A chemical that conveys information in an in- AnderssonJ,Borg-KarlsonA-K,WiklundC.2004.Sexualconflictand
teraction between 2 individuals, evoking in the receiver anti-aphrodisiactitreinapolyandrousbutterfly:maleejaculatetai-
a behavioral or physiological response that is adaptive to loringandabsenceoffemalecontrol.ProcRSocLondBBiolSci.
271:1765–1770.
oneof theinteractants orboth.
Arakaki N, WakamuraS. 2000. Bridge intime andspacefor an egg
Pheromone: An infochemical emitted by one organism evok-
parasitoid-kairomonal use of trace amount of sex pheromone ad-
ingaresponseinareceivingorganismofthesamespecies.
sorbedoneggmassscalehairofthetussockmoth,Euproctistaiwana
Sexpheromone:Apheromonethatisproducedbyamember (Shiraki)(Lepidotera:Lymantriidae),byaneggparasitoid,Teleno-
of one sex specifically to attract members of the other sex mus euproctidis Wilcox (Hymenoptera: Scelionidae), for host loca-
forthe purposeof sexualreproduction. tion.EntomolSci.3:25–31.
Antiaphrodisiac:Anantisexpheromonetransferredduringmat- ArakakiN,WakamuraS,YasudaT.1996.Phoreticeggparasitoid,Tele-
ingtoreducethefemales’receptivityandreinforcemonogamy. nomuseuproctidis(Hymenoptera:Scelionidae),usessexpheromone
Aggregationpheromone:Apheromonethatcausesaggregative of tussock moth Euproctis taiwana (Lepidoptera: Lymantriidae) as
akairomone.JChemEcol.22:1079–1085.
behaviorinconspecificsofbothsexesorinthesamesexas
Arakaki N, WakamuraS, YasudaT, YamagishiK. 1997. Two regional
theemitter.
strainsofaphoreticeggparasitoid,Telenomuseuproctidis(Hymenop-
Kairomone: An infochemical of an organism that on emis-
tera:Scelionidae),thatusedifferentsexpheromonesoftwoallopat-
sionevokesinthereceiver,anindividualofadifferentspe- rictussockmothspeciesaskairomones.JChemEcol.23:153–161.
cies, a behavioral or physiological response adaptively Bai SX, Wang ZY, He KL, Zhou DR. 2004. Olfactory responses of
favorable to thereceiver but not theemitter. TrichogrammaostriniaePanget.Chentokairomonesfromeggsand