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Basic and Applied Ecology 6 (2005) 215—236

KEYWORDBiologicalConservatgical contrFood ecoloMulti-tropactions;Non-targePlant volaTrichomes

1439-1791/$ - sdoi:10.1016/j.

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Habitat and plant specificity of Trichogramma eggparasitoids—underlying mechanisms andimplications

Jorg Romeisa,�, Dirk Babendreiera, Felix L. Wackersb,Thomas G. Shanowerc

aAgroscope FAL Reckenholz, Swiss Federal Research Station for Agroecology and Agriculture, Reckenholzstr. 191,8046 Zurich, SwitzerlandbNetherlands Institute of Ecology (NIOO-KNAW), Centre of Terrestrial Ecology, Boterhoeksestr. 48, 6666 GA Heteren,The NetherlandscNorthern Plains Agricultural Research Laboratory, USDA-ARS, 1500 N. Central Ave., Sydney, MT 59270, USA

Received 26 April 2004

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ing author. Tel.: +41 1ess: joerg.romeis@fal

SummaryEgg parasitoids of the genus Trichogramma are among the most important and best-studied natural enemies worldwide. Parasitism levels by Trichogramma vary greatlyamong different habitats, plants or plant structures on which the host eggs arelocated. Here we summarise the published evidence on mechanisms that may underliethe observed variation in parasitism rates. These mechanisms include plant spacing,plant structure, plant surface structure and chemistry, plant volatiles and plantcolour. In addition, plants can affect parasitoid behaviour and activity by providingcarbohydrate food sources such as nectar to the adult wasps, and by affecting thenutritional quality of the host eggs for progeny development. Knowledge of plant andhabitat factors that affect Trichogramma spp. efficacy has important implications forbiological control, and for assessing the risks that mass-released Trichogramma spp.may pose to non-target insects.& 2004 Elsevier GmbH. All rights reserved.

ZusammenfassungEiparasitoide der Gattung Trichogramma gehoren weltweit zu den wichtigsten und ambesten bekannten Nutzlingen. Parasitierungsraten von Trichogramma variierendeutlich zwischen verschiedenen Habitaten, Wirtspflanzen bzw. Teilen einer Pflanze,auf denen sich die Wirtseier befinden. In der vorliegenden Arbeit fassen wirzusammen, was hinsichtlich der Mechanismen bekannt ist, die fur die beobachteten

4 Elsevier GmbH. All rights reserved.

3777299; fax: +41 13777201..admin.ch (J. Romeis).

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Unterschiede in der Parasitierungsleistung verantwortlich sein konnen. DieseMechanismen umfassen Faktoren wie den Abstand zwischen den Pflanzen, diePflanzenstruktur, die strukturelle und chemische Beschaffenheit der Pflanzenober-flache, pflanzliche Duftstoffe sowie die Farbe der Pflanze. Hinzu kommt, dass Pflanzendas Verhalten bzw. die Aktivitat der adulten Parasitoide beeinflussen konnen indem siezuckerhaltige Nahrung z.B. in Form von Nektar zur Verfugung stellen. Ausserdemhaben die Pflanzen einen Einfluss auf die chemische Zusammensetzung der Wirtseier,was sich wiederum auf die Eiparasitoide auswirken kann. Ein gutes Verstandnis derHabitat- und Pflanzen-Faktoren, welche die Eiparasitoide beeinflussen, ist wichtig umden Einsatz von Trichogramma spp. in der biologischen Schadlingsbekampfung zufordern und auch um die moglichen Umweltauswirkungen von im Pflanzenschutzeingesetzten Trichogramma spp. zu erfassen.& 2004 Elsevier GmbH. All rights reserved.

Introduction

There is a large and expanding body of evidencethat habitat and plant characters have a strongimpact on the parasitism efficacy of parasitic waspsin natural systems as well as in biological control(Kester & Barbosa, 1991; Bottrell, Barbosa, &Gould, 1998; Rutledge & Wiedenmann, 1999; Hare,2002; Lill, Marquis, & Ricklefs, 2002). Egg para-sitoids belonging to the genus Trichogramma(Hymenoptera: Trichogrammatidae) are importantnatural enemies of a wide range of pests and aresuccessfully used in inundative and inoculativebiological control programmes worldwide (Li,1994; Smith, 1996; van Lenteren, 2000). Mostspecies are regarded as generalists, even thoughthe better-known species show a specialisation atthe level of the insect order of Lepidoptera (Pinto &Stouthamer, 1994). Trichogramma species differdistinctly from most other parasitic wasps due totheir minute size, ranging from 0.2 to 1.5mm (Pinto& Stouthamer, 1994). As a consequence, they arefor instance more affected by plant surfacestructures and have a low capacity for activeflights.

Trichogramma spp. are thought to be morehabitat- than host-specific (Salt, 1935; Flanders,1937; Curl & Burbutis, 1978). Habitat and plantfactors can directly or indirectly affect varioussteps in the host selection process of a femaleTrichogramma spp. A thorough understanding ofthe searching and parasitisation behaviour of theseparasitoids and their habitat and plant preferencescan be key to the optimisation of biological controlprogrammes (van Steenburgh, 1934; Flanders &Quednau, 1960) as well as to the assessment ofpossible non-target effects in mass-release pro-grammes. Here, we summarise the availableinformation on the interactions between Tricho-gramma spp. and the habitat or food plants of itshosts. Literature on Trichogrammatoidea spp.

(Hymenoptera: Trichogrammatidae) is not includedin this review, but many of the findings forTrichogramma spp. are likely to be similarly validfor Trichogrammatoidea spp. and other small-bodied egg parasitoids such as Mymaridae andScelionidae. Since the taxonomy of the Tricho-gramma genus is still much debated (Pinto &Stouthamer, 1994; Pinto, 1999), we use the speciesnames as they have been used in the originalstudies throughout this review.

Habitat specificity

Evidence is accumulating that Trichogramma spp.are more prevalent in certain habitats or on specificplants (Salt, 1935; Flanders, 1937; Pinto & Oatman,1988; Hirose, 1994; Pinto, 1999). Due to the habitatand plant specificity of different Trichogrammaspecies, the spectrum of species reared from acertain host can vary with the food plant fromwhich the eggs were collected (Lopez, Jones, &House, 1982; Pinto & Oatman, 1988; Monje,Romeis, Zebitz, & Shanower, 1998). Also, parasit-ism levels on a specific host species can vary widely,depending on the plant on which the eggs are found(Martin, Lingren, Greene, & Ridgway, 1976; Martin,Lingren, Greene, & Grissell, 1981; Nordlund,Chalfant, & Lewis, 1984; Keller, Lewis, & Stinner,1985; Romeis & Shanower, 1996; Stuart &Polavarapu, 2000; Gingras, Dutilleul, & Boivin,2003; Kuhar, Barlow, Hoffmann, Fleischer, Grodenet al., 2004).

In addition to habitat effects, parasitisation byTrichogramma spp. may also vary with the plantstructure or region of the plant on which the hosteggs are located. Studies on cotton (Gossypiumhirsutum) (Orphanides & Gonzalez, 1970) andmaize (Zea mays) (Phillips & Barber, 1933) haveshown that egg parasitism levels can differbetween upper and lower leaf surface. Other

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studies reported significant differences in parasiti-sation rates among host eggs on different plantstructures of cotton (Saavedra, Torres, & Ruiz,1997), rice (Oryza spp.) (Feijen & Schulten, 1981)and loblolly pine (Pinus taeda) (McCravy & Ber-isford, 1998). A good example is pigeonpea (Caja-nus cajan), where eggs laid on flower calyxes andpods were shown to be poorly parasitised (levelsbelow 4%), whereas eggs oviposited on leavessuffered high parasitisation (Romeis, Shanower, &Zebitz, 1998a, 1999b). Parasitism levels can alsodiffer among plant sections in the horizontal plane.This has been demonstrated in several field cropsincluding maize (Burbutis, Curl, & Davis, 1977;Neuffer, 1987; Wang, Ferro, & Hosmer, 1997, butsee Hawlitzky, Dorville, & Vaillant, 1994), cotton(Orphanides & Gonzalez, 1970; Gonzalez, Orpha-nides, van den Bosch, & Leigh, 1970) and sugarcane(Saccharum officinarum) (Monje, 1990). Differ-ences in the spatial distribution of Trichogrammaspp. are even more pronounced in vineyards andtree crops. Many studies have reported an unevendistribution (usually measured as egg parasitisationrates) for different Trichogramma species thatwere either released or occurred naturally ongrapes (Vitis vinifera) (Castaneda–Samayoa, Holst,& Ohnesorge, 1993), pine (Pinus spp.) (Hirose,Shiga, & Nakasuji, 1968), apple (Malus domestica)(Stein, 1961; Goujet & Martouret, 1982; Yu, Laing,& Hagley, 1984b; Wetzel, Dickler, Hassan, &Wrzeciono, 1995), balsam fir (Abies balsamea)(Kemp & Simmons, 1978; Jennings & Houseweart,1983), white spruce (Picea glauca) (Smith, 1988) orbirch (Betula spp.) (Kot, 1964). In some systems,the host preferentially oviposits on plant structures(Feijen & Schulten, 1981; Romeis et al., 1999b;Kuske, Babendreier, Edwards, Turlings, & Bigler,2004) or plant varieties (Hirai, 1988) that aredifficult for Trichogramma spp. to reach or handle.These findings could provide indirect evidence forthe ‘enemy-free space’ hypothesis that proposesthat the presence of antagonists affects ovipositiondecisions by the herbivore (Rossi, Reeve, & Cronin,1994; Lawton, 1996).

The mechanisms responsible for the observedpatterns are often not known, but both abiotic andbiotic parameters can play a role. In addition,observed differences in activity might partly be dueto preferential landing by adult wasps on certainregions of the plant (Suverkropp, 1994). Species ofTrichogramma are known to differ in their prefer-ences for specific light intensities (Kot, 1979;Smith, Hubbes, & Carrow, 1986) and humidity/temperature regimes (Quednau, 1957; Biever,1972; Boldt, 1974; Kot, 1979, 1995). Both tempera-ture and relative humidity can affect several

important life-table parameters of Trichogrammaspp. (see appendix in Noldus, 1989b), as well astheir walking speed and activity (Ording & Schie-ferdecker, 1968; Biever, 1972; Boldt, 1974; Kot,1979; Forsse, Smith, & Bourchier, 1992; Bourchier &Smith, 1996; Suverkropp, 1997). All of these factorscan be directly related to parasitisation levels. Forexample, Bourchier and Smith (1996), showed thattemperature alone could explain 75% of thevariation in field parasitism rates by T. minutumRiley in white spruce plantations in Canada. Severalauthors reported that the adaptability to tempera-ture varies among different species and strains ofTrichogramma spp. (Kot, 1964; Biever, 1972; Boldt,1974; Pak & Oatman, 1982; Pak & van Heiningen,1985; McDougall & Mills, 1997). In terms of bioticparameters, plant structure (see below) and hostdistribution or density (Goujet & Martouret, 1982;Keller et al., 1985; Monje, 1990; Wetzel et al.,1995) can also affect parasitoid activity. In addi-tion, there are indications that certain species ofTrichogramma have developed adaptations tospecific habitats. Thorpe (1984/85) reported thatT. pretiosum Riley and T. minutum showed adistinct vertical stratification of their activity, withthe arboreal T. minutum caught at higher eleva-tions than the field species T. pretiosum. Flanders(1937) and Quednau (1959) pointed out thatdifferences in the walking and flying habits ofdifferent Trichogramma species may be accountedfor as habitat adaptations. Results by Limburgand Pak (1991) indicated that characteristics ofT. dendrolimi Matsumura and T. evanescens West-wood movement, including walking speed, turningangle, time not walking and number of flyingattempts are genetically determined and cantherefore be the basis for selection.

Plant influence

Plant spacing

Walking and short jumps are probably the majormeans of short-distance dispersal in Trichogrammaspp., especially at low temperatures (Kadlubowski,1962 in Kot, 1979, Kot, 1964; Pak, van Halder,Lindeboom, & Stroet, 1985; Bigler, Bieri, Fritschy, &Seidel, 1988). Direct plant contact, as can beachieved through closer plant spacing, shouldtherefore favour parasitoid dispersal and affectthe success of inundative biological control pro-grammes. In agreement with this hypothesis, glass-house studies with cabbage (Brassica oleracea)showed that the rate of parasitisation by T. maidis

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Pintureau and Voegele decreased exponentiallywith increasing distance between plants (Paket al., 1985). Further evidence for the walking/jumping mode of dispersal is also provided by mass-release studies in grape where dispersal along theplant row was found to be much higher thandispersal among rows (Kast & Hassan, 1986;Castaneda-Samayoa et al., 1993). In contrast,parasitoid dispersal after point releases was foundto be independent of plant spacing in cabbage (vanAlebeek, Pak, Hassan, & van Lenteren, 1986) andmaize (Neuffer, 1987). This difference amongstudies might be due to the fact that at optimumtemperatures, short flights become an importantmechanism in between-plant movements (Suverk-ropp, 1997). In a system where between-plantmovement was minimal, dispersion by flight hasbeen shown to depend on wind, temperature and insome cases light intensity (Fournier & Boivin,2000). In addition to the effect on parasitoiddispersal, plant spacing will also influence theclimatic conditions within a field (Jones, 1992)and therefore affects the parasitoids indirectly.

Plant structure

Plant structure is defined by three components:(i) plant size or surface area, (ii) heterogeneity(abundance and diversity of plant parts), and (iii)connectivity (abundance of connections betweenplant parts) (Andow & Prokrym, 1990). A number ofstudies have evaluated the effect of plant structureon Trichogramma spp. parasitism efficacy.

As trichogrammatids search the plant surface forhosts by walking (Schmidt, 1994), the ability tolocate a host decreases with increasing foliage area(Knipling & McGuire, 1968). This has been con-firmed for different species of Trichogramma inperennial crops including cotton (Fye & Larsen,1969; Ables, McCommas, Jones, & Morrison, 1980),maize (Need & Burbutis, 1979; Kanour & Burbutis,1984; Bigler & Brunetti, 1986; Maini, Burgio, &Carrieri, 1991; Wang et al., 1997), cabbage (Kot,1979), tomato (Lycopersicon esculentum) (Pizzol,Ciociola, Marro, & Tronchetti, 1997) and sweetpepper (Capsicum annuum) (Burbutis & Koepke,1981).

Andow and Prokrym (1990) studied the impact ofstructural complexity on parasitism by T. nubilaleErtle and Davis when provided with host eggclusters on paper panels of different architecture.Structural complexity was found to decreaseT. nubilale parasitism significantly. Part of thedecrease in parasitism was due to the fact thatthe parasitoids searched simple surfaces more

intensively than complex ones providing the firstevidence that structural complexity per se canaffect the searching behaviour of Trichogrammaspp. These findings were confirmed by Lukianchukand Smith (1997) for T. minutum and Gingras andBoivin (2002) for T. evanescens using paper orplastic models of different structural complexity. Ina recent study, Gingras, Dutilleul, and Boivin (2002)compared the parasitism efficacy of T. evanescenson model plants that differed in their size (height),heterogeneity and connectivity. Variability in para-sitism could be best explained by connectivity(Gingras & Boivin, 2002). Similar findings were alsoreported in a later study deploying differentspecies of Brassica (Gingras et al., 2003). Recently,Andow and Olson (2003) found that there was asignificant variation among individuals of T. nubi-lale in their ability to parasitise hosts on simple orcomplex surfaces. The results suggest that thevariation was related to a maternal effect, dom-inance variation, or both.

Surface structure and chemistry

After landing on a plant, the female wasp begins arandom search for hosts, with host kairomones suchas moth scales and sex pheromones stimulating anarrestment behaviour in the vicinity of eggs(Gardner & van Lenteren, 1986; Noldus, 1989a;Noldus, Potting, & Barendregt, 1991; Reddy, Holo-painen, & Guerrero, 2002). Host eggs are onlyrecognised from a distance of about 4mm (Wajn-berg, 1994). Since host finding on the plant ismostly done by walking (Schmidt, 1994), fasterwalking females have a higher chance of findinghosts as they can search a larger surface area perunit time (Bigler et al., 1988; Bieri, Bigler, &Fritschy, 1990; but see van Hezewijk, Bourchier, &Smith, 2000). Physical and chemical plant surfacecharacters can therefore impede parasitoid search-ing and host encounter rates simply by decreasingwalking speed. In addition, plant surface charac-ters can also alter the parasitoid’s walking patternby changing the distribution of turning angles,again affecting their host finding ability (Keller,1987; Babendreier, Schoch, Kuske, Dorn, & Bigler,2003d).

Due to the small size of Trichogramma spp.,trichomes and trichome exudates can easily inhibitthe parasitoid’s movements. A lower efficacy ofTrichogramma spp. on pubescent versus glabrousvarieties has been reported for cotton (Treacy,Zummo, & Benedict, 1985; Treacy, Benedict,Segers, Morrison, & Lopez, 1986; Ramnath &Uthamasamy, 1992) and soybean (Glycine max)

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(Hirai, 1988). Trichomes and their sticky exudateshave been found to be responsible for the low eggparasitism levels in tobacco (Nicotiana tabacum)(Rabb & Bradley, 1968; Katanyukul & Thurston,1973; Gentry, Young, & Burton, 1973; Martin et al.,1976, 1981; Elsey & Chaplin, 1978), the wild tomatoLycopersicon hirsutum f. glabratum (accession PI134417) (Kauffman & Kennedy, 1989; Kashyap,Kennedy, & Farrar, 1991a, b; Farrar, Barbour, &Kennedy, 1994) and pigeonpea (Romeis et al.,1998a, 1999b; Ballal & Singh, 2003). Even thoughlaboratory studies revealed that trichogrammatidscan get caught in sticky glandular exudates, thiseffect is likely to be less important under fieldconditions because the adhesiveness of the exu-dates are decreased due to the effects of environ-mental factors (Obrycki & Tauber, 1984; Romeiset al., 1999b). Another example of the impact oftrichomes and their exudates on Trichogrammaspp. is chickpea (Cicer arietinum). The glandulartrichomes cover the entire plant surface andexcrete a non-sticky acidic exudate that rendersthe parasitoids totally ineffective under fieldconditions (Romeis & Shanower, 1996). Laboratorystudies with T. chilonis Ishii have shown that bothtrichomes and the exudates deter the parasitoidsafter landing (Romeis, Shanower, & Zebitz, 1999c).

In addition to physical interactions, plant surfacechemicals can also affect parasitoid searchingbehaviour (Keller, 1987; Lukianchuk & Smith,1997). Compounds contained in trichome exudates,i.e. 2-tridecanone and 2-undecanone, were foundto deter Trichogramma spp. on the wild tomatoL. hirsutum f. glabratum (accession PI 134417)(Kashyap et al., 1991a) and on chickpea (Romeiset al., 1999c). As suggested by studies on pigeon-pea, plant surface chemicals other than thosecontained in glandular exudates can also effectTrichogramma spp. searching behaviour (Romeiset al., 1998a). Unfortunately, the compoundsinvolved have not be identified.

Plant volatiles

Volatile plant semiochemicals are exploited by alarge number of dipteran and hymenopteran para-sitoids during habitat and/or plant selection (Priceet al., 1980; Lewis & Martin, 1990; Vet & Dicke,1992). The first indication that Trichogramma spp.are affected by plant volatiles was given by Mayer(1960). This author reported that females of aspecies referred to as T. embryophagum-cacoeciaewere less active parasitising host eggs whenexposed to an airstream passed over leaves ofBrussels sprouts (B. oleracea) or pine needles when

compared to pure air. Since then, a number ofstudies have investigated the response of Tricho-gramma spp. to volatiles derived from fresh plantmaterial and plant extracts using airflow olfact-ometers. In most studies, parasitoids were found tobe responsive (Bar, Gerling, & Rossler, 1979;Cabello Garcıa & Vargas, 1985; Nordlund, Chalfant,& Lewis, 1985; Kaiser, Pham–Delegue, Bakchine, &Masson, 1989; Boo & Yang, 1998; Romeis, Shanower,& Zebitz, 1997; Romeis et al., 1998a; but see Pak &van Lenteren, 1984; Romeis et al., 1999c; Reddy etal., 2002). In some instances, the response wasfound to vary among different plant parts tested(Romeis et al., 1997, 1998a; Boo & Yang, 1998). Itseems that plant volatiles generally do not attractthe parasitoids over a distance but rather arrest orrepel them after entering a habitat (Romeis et al.,1997). This is likely adaptive given that the smallsize of the parasitoids would generally preventthem from flying upwind towards an odour source(van Steenburgh, 1934; Fournier & Boivin, 2000).Some studies provide evidence for the fact thatplant volatiles may lead to increased egg parasitismlevels. Parasitism on different crops increasedsignificantly when plants were sprayed with awater extract of Amaranthus spp. (Altieri, 1981;Altieri, Lewis, Nordlund, Gueldner, & Todd, 1981;Altieri, Annamalai, Katiyar, & Flath, 1982). Simi-larly, glasshouse and field trials have shown thatparasitism on maize plants was increased whenplants were sprayed with tomato-hexane extract(Nordlund, Chalfant, & Lewis, 1984/85, 1985).Plant-derived volatiles can also have a negativeeffect on Trichogramma. Kashyap et al. (1991b)reported an increased mortality in T. pretiosumwhen wasps were exposed to volatiles emitted byfoliage of the wild tomato L. hirsutum f. glabratum(accession PI 134417).

Plant volatiles are regarded as stimuli that areeasy to detect by a foraging parasitoid, butprovide little reliable information with respect tothe presence of potential hosts. The more reliablehost-derived stimuli, on the other hand, aregenerally difficult to detect, thus presenting theparasitoids with a ‘reliability–detectability pro-blem’ (Vet, Wackers, & Dicke, 1991; Vet & Dicke,1992). Parasitoids that attack plant-feeding hoststages often make use of volatiles induced by theherbivore-inflicted damage. However, for egg para-sitoids such as Trichogramma spp., plant volatilesreleased in response to the feeding stages of theherbivore are not necessarily informative (Vet etal., 1991; Vet & Dicke, 1992). An exception wouldbe those cases in which the plant releases specificvolatiles in response to damage inflicted duringoviposition by adult herbivores (Hilker & Meiners,

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2002). Since Trichogramma spp. are generalists atthe plant level, we would expect that they respondto general plant volatiles rather than to odours thatare specific for a certain plant species. In agree-ment with this, Reddy et al. (2002) reported apositive response of T. chilonis to two green leafvolatiles, i.e. (Z)-3-hexenyl acetate and hexylacetate. Similar responses to general plant volatilestimuli have been found for other generalistparasitoids (e.g. Steidle, Steppuhn, & Reinhard,2001).

While it has been reported for various generalistparasitoid species that they can modify theirresponse to plant volatiles through experience(Vet et al., 1991; Takasu & Lewis, 1993; Wackers,Bonifay, & Lewis, 2002; Vet, Lewis, Papaj, & vanLenteren, 2003), odour learning has been rarelyreported for Trichogramma spp. (Kaiser et al.,1989; Bjorksten & Hoffmann, 1998).

Plant colour

Only few studies have addressed colour perceptionor preference by parasitoids (Wackers & Lewis,1999 and references therein) and even less isknown about Trichogramma spp. colour response.Kadlubowski (1970) reported a preference byT. embryophagum (Hartig) for yellow over blue,red and white. Unfortunately, no details on themethodology and colours used are given. Exposingdifferent coloured sticky traps in the field, Romeis,Shanower, and Zebitz (1998b) caught the highestnumber of female wasps (predominantly T. chilonis)on white traps followed by green, blue, red, yellowand black traps. The colour response of maleT. chilonis was significantly different from that ofthe females, with more males caught on yellow andgreen than on white traps. The reasons for thedifferent colour preferences of the two sexes areunknown and need further investigation. Compar-ing the parasitism efficacy of T. minutum onsimilarly structured white and green paper sur-faces, Lukianchuk and Smith (1997) detected noeffect of surface colour on the number of eggsparasitised. However recently, Keasar, Ney-Nifle,and Mangel (2000) reported that T. thalense Pintoand Oatman, after having attacked hosts on a greenor black background, subsequently showed a pre-ference for the respective colour, suggesting anassociative learning effect. In general, the studiesconducted indicate that Trichogramma spp. candifferentiate among colours, even though it re-mains unclear whether this differentiation is basedon hue or saturation. The relevance of this abilityfor the host location process remains to be shown.

A recent study on T. carverae Oartman and Pintosuggests that colour cues are used during the foodlocation process (Begum, Gurr, Wratten, & Nicol,2004). Female wasps were reported to preferalyssum (Lobularia maritima) plants bearing whiteflowers over those with light pink, dirty pink orpurple ones.

Use of food sources by adult wasps

Adult Trichogramma spp., like most parasitoidspecies, require sugars as an energy source tosustain a range of physiological processes. Theymay obtain sugars from floral nectar, extrafloralnectar, honeydew, plant sap or leached phloemsugars (Wackers, 2005). In addition, females ofmost species also retain an element of carnivoryduring their adult life by engaging in host-feeding(Jervis & Kidd, 1986). Host feeding and sugarfeeding are believed to cover separate nutritionalrequirements of the parasitoid. Sugar-rich foodsuch as nectar or honeydew primarily provide forthe parasitoid’s energetic needs. Insect eggs, onthe other hand, are primarily a source of proteinsrequired for physiological processes such as eggmaturation. They are usually unsuitable as anenergy source and add little to Trichogrammaspp. longevity (Leatemia, Laing, & Corrigan,1995). In part, this may be explained by the factthat eggs usually only contain traces of nutrition-ally suitable sugars such as glucose (Chino, 1957).The bulk of carbohydrates in Lepidopteran eggs isusually present as glycogen. The relative poorsurvival in host-feeding studies suggests that adultparasitoids lack the enzymes in their digestive tractto utilise this carbohydrate.

Nectar and honeydew are more suited as a sourceof carbohydrates. These sugar sources can have astrong impact on Trichogramma spp. longevity,fecundity, and sex ratio (Schulze, 1924; Ashley &Gonzales, 1974; Stinner, Ridgway, & Morrison, 1974;Stavraki, 1976; Walter, 1983a; Yu, Hagley, & Laing,1984a; Smith et al., 1986; Hohmann, Luck, &Oatman, 1988; Hoffmann, Walker, & Shelton,1995; Leatemia et al., 1995; McDougall & Mills,1997; Olson & Andow, 1998; Gurr & Nicol, 2000).Feeding benefits may be positively correlated withfemale size, as honey feeding was found to increasefecundity primarily in large females of T. pretiosum(Bai, Luck, Forster, Stephens, & Janssen, 1992). Inthe case of the larval parasitoid Cotesia rubecula(Marshall) (Hymenoptera: Braconidae) it could beshown that food-deprived parasitoids primarilyengage in food foraging, rather than seeking out

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hosts. Food satiated individuals, on the other hand,lose their interest in food-associated stimuli andfully concentrate on host search (Wackers, 1994).Trichogramma spp. appear to respond in a similarmanner to food deprivation, even though differ-ences between species may exist (Hegazi, Khafagi,& Hassan, 2000). Sugar feeding can also increasehost encounter rates as a parasitoid’s energyreserves determine the individual’s overall flightpropensity and searching activity (Ording & Schie-ferdecker, 1968; Forsse et al., 1992; Pompanon,Fouillet, & Bolutreau, 1999).

Natural food sources, such as nectar and honey-dew, may contain various carbohydrates, aminoacids, proteins, lipids, antioxidants, organic acidsand other non-nutritive substances (Baker & Baker,1975, 1982; Kunkel & Kloft, 1977; Wackers, 2005).Few studies have investigated the role of theseindividual compounds on the fitness of Trichogram-ma spp. Narayanan and Mookherjee (1955) foundthat 10% solutions of glucose, maltose, fructose andsucrose increased longevity of a species referredto as T. evanescens minutum equally well. Ashleyand Gonzales (1974) found no effect on femaleT. pretiosum when fed with glucose, but reportedan increase in longevity and fecundity in sucrose-fed parasitoids. McDougall and Mills (1997) showedthat 43% fructose and sucrose solutions prolongedlongevity of T. platneri to approximately 20 days;an increase by a factor 13 relative to control insectskept with water only. Leatemia et al. (1995)compared the effect of different carbohydratessources (honey, sucrose, fructose) on longevity,fecundity and progeny sex ratio of T. minutum. Interms of longevity, the positive effect of the twocarbohydrate solutions was almost as strong as theeffect of the honey solution. In terms of fecundity,honey-fed individuals outperformed parasitoidskept with sucrose or glucose. These results indicatethat parasitoids use honey compounds other thancarbohydrates (e.g. amino acids or proteins) for eggproduction. It is interesting to note that thesecompounds provide an added benefit to nutrientsobtained through host feeding. Surprisingly, pro-geny sex ratio (% females) was significantly lowerfor females fed on sugars or honey as compared tounfed wasps or wasps kept on water. Despite thefact that some of the non-nutritive compoundscontained in nectar and honeydew have knowninsecticidal properties their potential effect onTrichogramma spp. has only been investigated inone case (Romeis, Babendreier, & Wackers, 2003).

While laboratory studies have convincingly de-monstrated the positive impact of food supple-ments on Trichogramma life-table parameters, weknow relatively little about food sources used by

Trichogramma spp. in the field or their effect onparasitisation rates. A study by Wellinga and Wysoki(1989) indicated that T. platneri Nagarkatti can usefloral nectar as food. The authors compared thedaily survival rate of wasps when offered flowers ofavocado (Persea americana) (with and withoutanthers), anthers of avocado, or flowers fromdifferent herbs (Oxalis cernua, Mercuralis annuaand Euphorbia spp.). Irrespective of the presenceof anthers, parasitoids provided with avocadoflowers lived longer than unfed wasps or waspsoffered avocado anthers only. However, the flower-ing herbs did not increase parasitoid longevity. Thismay be due to the fact that flower morphologyprevented parasitoid access or successful flowerhandling as has been reported for other hymenop-teran parasitoids (Wackers, Bjornsen, & Dorn, 1996;Patt, Hamilton, & Lashomb, 1997; Baggen, Gurr, &Meats, 1999). Alternatively, the floral scent mighthave acted as a repellent to the parasitoids(Wackers, 2004). Wellinga and Wysoki (1989) foundno evidence of pollen feeding by T. platneri anddirect observations showed that wasps ignoredavocado pollen even after antennal contact. Thisrejection is likely due to the small size ofTrichogramma spp. which physically precludesingestion of pollen grains (Jervis, Kidd, & Heimpel,1996). However, Zhang, Zimmermann, and Hassan(2004) reported that T. brassicae Bezdenko in-creased its longevity when provided with maizepollen on wet filter paper. This may have been dueto (pseudo)germination of the pollen, a processduring which pollen nutrients are released (Stanley& Linskens, 1974). Somchoudhury and Dutt (1988)found no significant increase in longevity orfecundity of T. perkinsi Girault and T. australicumGirault when provided with flowering maize orsorghum (Sorghum bicolor), indicating that theparasitoids are not able to use these pollen sources.Besides this laboratory study, we found only onereport in the literature in which Trichogramma spp.were recorded on flowers (Medicago sativa, Viciaspp., Phacelia spp.) in the field (Dobrosmyslov,1968, in Walter, 1983a). Several herbs includingbuckwheat (Fagopyrum esculentum), mustard(Brassica nigra) and dill (Anethum graveolens),have been listed as good food plants for Tricho-gramma spp. (Zandstra & Motooka, 1978), withoutreference to observations underlying these state-ments. Telenga (1958, in Jervis, Kidd, Fitton,Huddleston, & Dawah, 1993) reported that theactivity of Trichogramma spp. was increased inapple orchards where Phacelia tanacetifolia andEryngium spp. was sown. Evidence for the useof floral nectar has recently been reported forT. carverae by Begum et al. (2004). The authors

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reported an increase in both longevity and realisedfecundity in female wasps provided with flowers ofalyssum (L. maritima).

In contrast to floral nectar, extrafloral nectariesare usually exposed and thus easily accessible.While there is no reason to assume that Tricho-gramma spp. should refrain from using this foodsource, evidence for extrafloral nectar feeding byTrichogramma spp. is even more scarce than forfloral feeding. Treacy, Benedict, Walmsley, Lopez,and Morrison (1987) provided indirect evidence forthe use of extrafloral nectar, as their study showedlower parasitisation rates in nectariless cotton, ascompared to cotton bearing extrafloral nectaries.Keller et al. (1985) and Wellinga and Wysoki (1989)observed Trichogramma spp. feeding on fluids fromdamaged plant tissue. Maybe the most prevalentfood source for Trichogramma spp. is the honeydewproduced by sap sucking phytophagous insects(Eidmann, 1934; Wellenstein, 1934; Gyorfi, 1945;Franz and Voegele, 1976 in Wetzel et al., 1995;McDougall & Mills, 1997).

Plant effects on host quality

Plant compounds that are ingested by a herbivoremight be passed on to insect eggs, potentiallyaffecting egg parasitoids. Herbivores may evensequester plant-derived compounds in their eggsas protectants (Blum & Hilker, 2002). However,active sequestration is often difficult to distinguishfrom passive mechanisms.

The effect of the egg content on acceptance andsuitability for Trichogramma spp. has almostexclusively been studied within the context ofdeveloping artificial host eggs for mass rearing ofthese parasitoids (Grenier, 1994). Little is knownabout how the host’s diet affects the quality of thehost eggs for Trichogramma spp. Navarajan Paul,Mohanasundaram, and Subramaniam (1975) com-pared the suitability of Corcyra cephalonica Stain-ton (Lepidoptera: Pyralidae) eggs collected frommoths reared on greengram (Vigna radiata),sorghum or groundnut (Arachis hypogaea) forT. chilonis and T. japonicum Ashmead. The host’sfood plant had a significant effect on parasitoidlife-history parameters including developmentrate, size, longevity and fecundity. In addition tocompounds derived from the food plants, insecteggs may also contain protective compounds thatare produced by the adult females de novo (Blum &Hilker, 2002). Protective compounds can either beapplied to the egg surface and thus affect theparasitoid’s host acceptance behaviour or seques-

tered within the eggs, with possible consequencesfor parasitoid development as well as host accep-tance (Blum & Hilker, 2002). The use of defensivecompounds on the egg surface or within the eggs isparticularly common in the Coleoptera and Lepi-doptera. Only few studies provide indications thatthese compounds may affect host acceptance byand/or suitability for Trichogramma spp. Song,Bourchier, and Smith (1997) reported that sprucebudworm eggs from moths which had been rearedon artificial diet were better accepted byT. minutum when compared to eggs from mothsreared on balsam fir, which were already rejectedduring the external examination phase. Interest-ingly, the eggs did not differ in their suitability forparasitoid development. Similarly, Babendreier,Kuske, and Bigler (2003a) observed that most eggsof checkerspot butterflies (Melitaea parthenoidesKeferstein, Melitaea diamina Lang and Mellictaathalia Rottemburg; Lepidoptera: Nymphalidae)feeding on Plantago spp. are rejected byT. brassicae early in the external examinationphase. However, those eggs that were acceptedfor oviposition, yielded viable parasitoid offspring.Studies with T. brassicae under confined conditionsin the laboratory showed that eggs of two cocci-nellid species are both poorly accepted and alsounsuitable hosts for parasitoid development (Ba-bendreier, Rostas, Hofte, Kuske, & Bigler, 2003c).Host dissections revealed that 45% of Adaliabipunctata L. (Coleoptera: Coccinellidae) eggswere parasitised by T. brassicae females in a 24 hperiod. Although parasitoid larvae could be foundin the host eggs, no parasitoid successfullyemerged. Direct observations revealed that fewfemales showed any drumming behaviour on andoviposited into the host egg masses during a 10-minobservation period. The eggs of Coccinella septem-punctata L. (Coleoptera: Coccinellidae) were allrejected and no drumming on these eggs was everobserved. These results might be explained by thepresence of compounds in or on the surface of eggsfrom both coccinellid species that are known toact as protectants against conspecific and intra-guild predation (Lognay, Hemptinne, Chan, Gaspar,Marlier et al., 1996; Hemptinne, Lognay, Gauthier,& Dixon, 2000).

Implications for enhancingTrichogramma efficacy

The reported prevalence of certain speciesof Trichogramma in specific habitats and environ-mental conditions highlights the importance of

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selecting the appropriate species for inoculativeand inundative release programmes. Plant surfacearea, plant density and the structural complexity ofthe plant and the habitat must also be taken intoaccount in augmentative parasitoid release pro-grammes (Schutte & Franz, 1961; Kot, 1979; Kanour& Burbutis, 1984; Smith, 1988; Andow & Prokrym,1991; Prokrym, Andow, Ciborowski, & Sreenivasam,1992; Lukianchuk & Smith, 1997). In addition, thisknowledge can be used in conservation biologicalcontrol, i.e. by enhancing the efficacy of naturallyoccurring parasitoids through specific habitat man-agement measures or the choice of specific hostplants or plant varieties.

Habitat management

Habitat manipulation allows us to provide naturalenemies with vital resources such as food, alter-native hosts or shelter from adverse environmentalconditions (Coll, 1998; Gurr, van Emden, & Wrat-ten, 1998; Landis, Wratten, & Gurr, 2000; Gurr,Wratten, & Luna, 2003). As such, it can be apowerful tool to enhance the performance ofnatural enemies in regulating pest insects. Thereis increasing evidence that habitat diversification isespecially beneficial for polyphagous species suchas Trichogramma spp. (Sheehan, 1986). A numberof studies have investigated the impact of habitatdiversification on Trichogramma spp. activity(Table 1). Most of these studies report increasedparasitisation. While some authors suggested me-chanisms which might have led to the observedincrease in parasitoid activity, none of the con-ducted studies is designed to demonstrate thesemechanisms.

It is believed that the active flight of smallinsects such as Trichogramma spp. is confined incomparison to larger species that are often lessaffected by turbulence. This would limit theeffectiveness of spatially restricted types of habi-tat manipulation, such as the use of field edges(Corbett & Plant, 1993). Mark-recapture studies byLong, Corbett, Lamb, Reberg-Horton, Chandleret al. (1998) appear to confirm this. Trichogrammaspp. were labelled by spraying a rubidium chloridesolution on insectary hedgerows adjacent to vege-table fields or to orchards. Using this method,about 20% of the parasitoids within the hedgerowwere marked. Recaptures at 7 and 80m within thevegetable fields revealed no marked parasitoids,while 2.5% of the wasps caught at a distance of 7minside the orchards were labelled. In addition, fieldstudies reported a significant decrease in eggparasitism levels with increasing distance from

the surrounding hedgerows (Table 1). In accordanceto these studies, field studies in Australia revealeda significant beneficial effect of flowering borderson another egg parasitoid, Copidosoma koehleriBlanchard (Hymenoptera: Encyrtidae) with a de-crease in parasitism with increasing distance to theborder region (Baggen & Gurr, 1998).

Manipulation of plant attributes

Several reviews (Bottrell et al., 1998; Verkerk,Leather, & Wright, 1998; Cortesero, Stapel, &Lewis, 2000) have discussed the possibility ofmanipulating plant characters to improve theefficacy of biological control agents. The idea isnot new, though traditionally plant varieties andcultivars have been developed primarily based onother criteria (e.g. yield, resistance to pests orabiotic constraints). Much effort has been ex-pended in developing resistant cultivars, but theseare often not compatible with biological control(van Emden, 1991; Hare, 2002).

There are a number of plant characteristics thatcould be modified to enhance the efficacy ofTrichogramma spp. The most obvious are morpho-logical (e.g. trichomes, spines, waxy leaf surface)or chemical (e.g. trichome exudates, leaf volatiles)attributes, which constrain parasitoid foraging orprevent access to the host. Among the best-documented examples are studies on tomato(Kauffman & Kennedy, 1989; Kashyap et al.,1991a, b), cotton (Treacy et al., 1986), chickpea(Romeis et al., 1999c) and pigeonpea (Romeiset al., 1998a; Romeis, Shanower, & Peter,1999a). Developing genotypes that lack theseinhibiting attributes may enhance the impact ofTrichogramma spp.

Another approach would be to increase theattractiveness of the specific olfactory (volatile)or visual (e.g. colour) cues that help Trichogrammaspp. to locate suitable habitats. However, thisapproach may have limited potential given thatTrichogramma spp. do not exhibit much long-rangeorientation. Moreover, the constitutive expressionof such cues could be counterproductive if it resultsin parasitoids wasting time and energy in theabsence of hosts (Powell, 1986; Cortesero et al.,2000).

A third approach to improve natural enemyperformance would be through the use of supple-mentary food resources. Evidence with regard tothe effect of sugar sources on field parasitisationlevels is scarce and conflicting. The study by Treacyet al. (1987) indicated that the presence of cottonextrafloral nectar increased egg parasitism rates

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Table 1. Effects of habitat diversification on parasitisation efficacy of Trichogramma spp.

Trichogrammaspecies

Lepidopteran host Host plant Type of habitatdiversification

Effect on eggparasitism

Proposed mechanism Remarks Reference

T. pretiosum+T. sp. Helicoverpa zea Soybean Intercrop with maize;weedy soybean plot

+ Chemical attraction/retention

Altieri and Todd(1981), Altieri et al.(1981)

T. pretiosum Sentinel eggs (Ephestiakuehniella)

Faba beans Intercrop withAmaranthus retroflexus

+ Chemical attraction/retention

Glasshouse study; astimulating effect of water-extract of Amaranthus spp.on Trichogramma spp. hadbeen reported earlier(Altieri, 1981; Altieri et al.,1981, 1982).

Altieri et al. (1982)

T. spp. Laspeyresia dorsana,Autographa gamma

Pea, cabbage Intersowing of Phaceliatanacetifolia

n.r. Provision of nectarsource

Voronin (1982)

T. spp. Mamestra brassicae Cabbage Field border of smallwoods

+* Parasitism decreased withincreasing distance fromthe hedgerows

Rost and Hassan(1985)

T. spp. Helicoverpa zea Maize Intercrop with tomatoand/or beans

+ Nordlund et al.(1984)

T. sp. Chilo sp. Maize Agroforestry systemwith Leucaenaleucocephala

+* A significant inverse linearrelationship betweenhedgerow spacing and ratesof egg parasitism was found

Ogol et al. (1998)

T. sp. near mwanzai Chilo spp., Sesamiacalamistis

Maize Intercrop with cowpea + Intercropping did not affectnumber of host egg batchesper plant or hostdistribution

Skovg(ard and Pats(1996), Pats et al.(1997)

T. minutum Ostrinia nubilalis Maize Intercrop with bean andsqash or with clover

- Andow and Risch(1987)

T. chilonis Ostrinia furnacalis Maize Intercrop with sweetpotatoes

O Nafus and Schreiner(1986)

T. spp. (mainlyT. chilonis)

Helicoverpa armigera Pigeonpea Intercrop with sorghum + Parasitoid movementfrom sorghum intopigeonpea

A follow-up study by Romeiset al. (1999a) showed thatthe increase in eggparasitism levels was mostlikely due to an abnormaloviposition behaviour byH. armigera rather than toan increase in parasitoidactivity/efficacy

Duffield (1994)

T. pretiosum Diaphania hyalinata Squash Intercrop with maizeand cowpea

+ Alternative hosts inmaize

Letourneau (1987)

J.Rom

eiset

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T. spp. Helicoverpa armigera Lucerne(Medicago sativa)

Strip-cutting + Parasitoids migratedfrom harvested stripsinto adjacentunharvested ones

Hossain et al. (2001)

T. semblidis Eupoecilia ambiguella,Lobesia botrana

Vine Interculture withbrambles (Rubusfruticosus) or nettles(Urtica dioica and U.urens)

+* Provision of alternativehosts

Parasitism at 8–10mdistance from thehedgerows was significantlydecreased

Schade (1991),Schade and Sengonca(1998a, b)

T. minutum Endopiza viteana Vine Buckwheat (Fagopyrumesculentum) as a covercrop

n.r. Provision ofcarbohydrate sources,i.e. buckwheat nectar orhoneydew produced byaphids feeding onbuckwheat

Damage caused by thetarget pest was recorded;egg parasitisation was notdirectly measured andalternative hypothesesexplaining the reduced pestdamage were notconsidered

Nagarkatti et al.(2003)

T. spp. Apple Sowing of Phaceliatanacetifolia andEryngium spp.

n.r. Provision of nectarsources

Telenga (1958 inJervis et al., 1993)

T. spp. Carpocapsa pomonella Apple Sowing of buckwheat(Fagopyrumesculentum), mustard(Brassica nigra), dill(Anethum graveolens)

n.r. Provision of nectarsources

Zandstra andMotooka (1978)

T. minutum Choristoneurafumiferana

Balsam fir Increasing proportion ofnon-host food plants inthe stand

+ Provision of alternativehosts

An alternative explanationis the fact that deciduousor mixed stands in theboreal forest harbour anunderstory that is morediverse in flowering plantsthat could possibly providefood for adult parasitoids(Cappuccino et al., 1998)

Kemp and Simmons(1978), Quayle et al.(2003)

T. embryophagum Sentinel eggs(Mamestra brassicae)

Pine Border of deciduoustrees

+* Parasitoids were found tomigrate 50–60m into thepine stands; significantincrease in parasitism ofegg cards in the borderregion

Walter (1983b)

T. evanescens Bupalus pinaria Pine Mixed stand with spruceand/or beech

+ Steiner (1931)

+: Enhanced level of egg parasitism in the diversified habitat compared to the monoculture; +*: no effect on overall parasitism rate or overall parasitism rate was not recorded. Parasitism ratewas increased in close proximity to the field border; �: decreased level of egg parasitism in the diversified habitat compared to the monoculture; o: no effect of habitat diversification on eggparasitism levels; n.r.: egg parasitism levels were not recorded.

Hab

itatand

plant

specifi

cityof

Trichogramma

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by Trichogramma spp. Lundgren, Heimpel, andBomgren (2002), on the other hand, found noeffect of weekly applications of a sucrose solutionon parasitism by T. brassicae in cabbage. Inaddition, plant-derived food supplements can alsobe used by herbivores (Romeis & Wackers, 2002;Romeis, Stadler, & Wackers, 2005) and the costsand benefits of such an approach have to becarefully assessed. One solution would be to selectfor plant-derived food supplements (e.g. extra-floral nectar) that are palatable to the parasitoidswithout being accepted by the herbivores (Rogers,1985; Wackers, 1999; Romeis & Wackers, 2000).

Two important negative consequences must beconsidered before manipulating plant attributes toimprove natural enemy efficacy. The manipulationsmust be neutral or negative for the targetherbivore (pest). If the manipulation inadvertentlyenhances herbivore performance or intra-guildpredation (hyperparasitoids), the net result maybe an increase in plant damage. Also, manipula-tions should not adversely affect other pest and/ornatural enemy species utilising the same host plant(Bottrell et al., 1998). While this will undoubtedlyoccur, it may be difficult to predict the conse-quences in advance. For example, eliminating theproduction of glandular trichome exudates maygreatly enhance Trichogramma spp. efficacy onpigeonpea (Shanower, Romeis, & Peter, 1996). Butit is unclear what the impact would be on the host,Helicoverpa armigera (Hubner) (Lepidoptera: Noc-tuidae), other insect herbivores, their naturalenemies, or even on specific plant pathogens,which may be affected by the trichome exudates.

Implications for non-target effects ofinundative parasitoid releases

As discussed above, plant and habitat parametersaffect the searching efficacy and parasitism byTrichogramma spp. with implications for biologicalcontrol. As we have outlined here, however, theseplant and habitat parameters also have importantconsequences for possible detrimental effects ofmass-released trichogrammatids on non-targetspecies. A growing body of literature has shownthat non-target effects of biological control agentsmay not be as rare as formerly thought (Howarth,1991; Louda, Pemberton, Johnson, & Follett,2003), and the evaluation of potential non-targeteffects has become a central issue for biologicalcontrol workers and conservation biologists in thepast decade. It is generally agreed that parasitoidswith a wide host range such as Trichogramma spp.

are potentially the most hazardous natural enemies(van Lenteren, Babendreier, Bigler, Burgio,Hokkanen et al., 2003). Since these parasitoidsare released in large numbers worldwide, risksassociated with these releases must be acknowl-edged.

In general, most concerns have been expressedabout non-target effects occurring outside therelease fields, although effects on beneficial insectswithin the target habitat have also been reported(Babendreier et al., 2003c). There is little informa-tion on the proportion of mass-released Tricho-gramma spp. that are leaving the target habitatand enter adjacent non-target habitats. Resultsfrom studies related to this question, however,suggest that emigration from release fields can besignificant (Bigler, Bosshart, Waldburger, & Ingold,1990; Andow & Prokrym, 1991; Andow, Lane, &Olson, 1995). Field studies by Kuske, Widmer,Edwards, Turlings, Babendreier et al. (2003) usingsticky traps revealed that T. brassicae that werereleased in maize entered adjacent wild flowerstrips and common reed (Phragmites australis)stands only during a short period of time, whichwas restricted to the mass-release events andshortly thereafter.

So, what is the impact of plants or habitats onthe magnitude of non-target effects caused byTrichogramma mass releases? Andow et al. (1995)evaluated the potential non-target effects ofinundative releases of T. nubilale with specialemphasis on the Karner blue (Lycaeides melissasamuelis Nabakov; Lepidoptera: Lycaenidae), anendangered butterfly living in proximity to maize insome parts of the USA. Since this butterfly lives inoak (Quercus spp.) savannas, Andow et al. (1995)released large numbers of parasitoids in this non-target habitat but failed to find any parasitisedsentinel eggs [Ostrinia nubilalis (Hubner); Lepidop-tera: Crambidae]. Orr, Garcia-Salazar, and Landis(2000) also released T. brassicae in non-targethabitats including wetlands, old fields and forests.They found that parasitism of sentinel egg cardscarrying eggs of three different lepidopteranspecies was significantly lower in non-target habi-tats when compared to maize fields. In contrast tothe previous studies, Kuske et al. (2004) usednaturally oviposited eggs of Archanara geminipunc-ta (Haworth) (Lepidoptera: Noctuidae) and Chilophragmitellus Hubner (Lepidoptera: Pyralidae) andfound that T. brassicae females released in nearbymaize fields are not able to parasitise these non-target hosts in common reed stands. While eggsof C. phragmitellus are not readily accepted byT. brassicae when offered under laboratory condi-tions, eggs of A. geminipuncta are well accepted

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and suitable hosts. However, the latter were foundto completely escape parasitism in the fieldbecause they are laid hidden between leaf sheathand reed stalk.

Until now there is only one study available thatrelates non-target effects of Trichogramma spp. tothe searching efficacy of individual parasitoids.Babendreier et al. (2003d) investigated the efficacyof inundatively released T. brassicae in non-targethabitats with additional experiments carried out inthe laboratory. Under field conditions, sentinel eggs(Ephestia kuehniella Zeller; Lepidoptera: Pyrali-dae) were applied directly onto selected commonplants in different non-target habitats. The mainresult was that parasitism in meadows, flower stripsand hedgerows were about an order of magnitudelower than that recorded from maize plants in thefield. These low parasitism levels recorded fromnon-target habitats correspond well with resultsfrom a second study in that eggs of non-targetbutterflies and from E. kuehniella were applied ongrassy and herbaceous plants and exposed toT. brassicae in field cages and in the field(Babendreier, Kuske, & Bigler, 2003b). Subse-quently, laboratory studies demonstrated thatseveral parameters known to influence parasitismrate (time spent on the plants, walking speed andnumber of turns) were reduced on commonmeadow plants such as Trifolium pratense (Baben-dreier et al., 2003d). For example, this plant isdensely covered with trichomes and the parasitismrates of T. brassicae could be related to leafcharacteristics of the plant. However, the studysuggested that these laboratory results can onlypartly explain the lower parasitism rates in non-target habitats compared to maize and thatstructural complexity on the whole plant/habitatlevel also may have limited parasitism levels ofT. brassicae in the investigated non-target habitats(Babendreier et al., 2003d).

Altogether, these studies clearly show that plantand/or habitat parameters are very importantfactors determining (and limiting) non-target ef-fects of Trichogramma spp. mass releases. Theyfurthermore may explain why host ranges deter-mined for Trichogramma spp. in the laboratorytend to be broader than the host range found in thefield (Curl & Burbutis, 1978). At first, this mayappear to be in contradiction to recent reports byMansfield and Mills (2002) and Babendreier et al.(2003a, b) showing that physiological host range issimilar to ecological host range, but these resultswere obtained after massive releases of tricho-grammatids. It may be suggested that the efficacyof finding and parasitising host eggs on complexplants or in complex ‘wild’ habitats may be too low

for inundatively released Trichogramma spp. tomaintain viable populations thereby reducing thenumber of hosts attacked in the field.

Conclusions

Trichogramma egg parasitoids play an importantrole both as a pest management tool and as a keyecological component of natural and manipulatedsystems. This paper summarises the extensiveresearch on the role of the plant and habitat inthe complex and diverse ecology of Trichogrammaspp. The multi-trophic interactions between Tri-chogramma spp., their hosts, host plants andhabitats can be a valuable source of informationfor other (less well studied) tri-trophic systems.Still, one has to consider the specific character-istics of each system to understand the constraintsand driving forces. For instance, plant and habitatfactors that affect Trichogramma spp., such astrichomes or plant connectivity, may be of lessimportance to larger-bodied arthropods. Moreover,plant or host cues that are often important in long-range habitat and host location of larger (flying)arthropods, probably play a relatively subordinaterole in the case of Trichogramma simply becausetheir ability to fly actively up-wind is low and long-distance dispersal is probably mainly effected bypassive transport. The information available sug-gests that understanding the requirements ofnatural enemies with regard to habitat and asso-ciated environmental conditions, can provide valu-able tools with which we can enhance or modify thehabitat to accomodate the natural enemies. Thiscan reveal new strategies which may improvenatural enemy performance and ultimately enhancethe success of biological control programs.

Acknowledgements

We are grateful to Guy Boivin (Agriculture etAgroalimentaire Canada, Saint-Jean-sur-Richelieu,Canada) for his comments on an earlier draft of themanuscript.

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