Biological Control xxx (2009) xxx–xxx

ARTICLE IN PRESS

Contents lists available at ScienceDirect

Biological Control

journal homepage: www.elsevier .com/locate /ybcon

Perspective

Sub-lethal effects of two pyrethroids on biological parameters and behavioralresponses to host cues in the egg parasitoid Telenomus busseolae

Ahmet Bayram a,*, Gianandrea Salerno b, Andrea Onofri b, Eric Conti b

a Dicle University, Faculty of Agriculture, Department of Plant Protection, 21280 Diyarbakir, Turkeyb Dipartimento di Scienze Agrarie e Ambientali, Università di Perugia, Borgo XX Giugno 74, 06121 Perugia, Italy

a r t i c l e i n f o

Article history:Received 13 April 2009Accepted 29 September 2009Available online xxxx

Keywords:Sesamia nonagrioidesNoctuidaeTelenomus busseolaeScelionidaeCyfluthrinDeltamethrinSub-lethal effects

1049-9644/$ - see front matter � 2009 Elsevier Inc. Adoi:10.1016/j.biocontrol.2009.09.012

* Corresponding author. Fax: +90 412 248 81 53.E-mail addresses: abayram@dicle.edu.tr, tbusseola

Please cite this article in press as: Bayram, A., etthe egg parasitoid Telenomus busseolae. Biologic

a b s t r a c t

The present study was undertaken to investigate possible integration of synthetic pyrethroids with bio-logical control of Sesamia nonagrioides Lefebvre (Lepidoptera: Noctuidae) by the egg parasitoid Telenomusbusseolae Gahan (Hymenoptera: Scelionidae). The effects of two commonly used synthetic pyrethroids,deltamethrin (Decis Jet 15 EC) and cyfluthrin (Bayteroid 5 EC), on the parasitoid were studied. Lethal con-centrations (LC25) were estimated for both insecticides, and their sub-lethal effects on some biologicalparameters and behavioral responses to different kairomonal cues mediating host location were investi-gated. Parasitoid females exposed to cyfluthrin (LC25) parasitized significantly fewer eggs than untreatedfemales, whereas neither the level of emergence from parasitized eggs nor the sex ratio of the offspringwas affected by the insecticides. None of the above biological parameters were significantly affected bydeltamethrin (LC25). Both insecticide treatments reduced the longevity of the parasitoids. The effects ofboth insecticides (LC25) on the behavioral responses of parasitoid females to the sex pheromone of S. non-agrioides, which acts as a long-distance kairomone, were investigated in a Y-tube olfactometer. Cyfluth-rin-treated parasitoids failed to respond to the host pheromone, whereas deltamethrin-treated femalesresponded similarly to untreated females. In addition, sub-lethal effects of pyrethroids on parasitoidarrestment behaviors were evaluated in an open arena containing abdominal scales from virgin femalemoths, which are a source of short-distance kairomone for the parasitoid. No significant differences inarrestment behaviors (residence time, linear speed) were found. Based on our results, possible conse-quences of treating maize with cyfluthrin or deltamethrin on the effectiveness of surviving T. busseolaein the field are discussed.

� 2009 Elsevier Inc. All rights reserved.

1. Introduction

The effectiveness of an egg parasitoid in biological control ishighly dependent upon the parasitoid’s ability to locate and recog-nize the host. This ability entails perception of and response tophysical and especially semiochemical cues elicited by the host,by the plant, and/or by the plant–host interaction (Vinson, 1998;Vet and Dicke, 1992; Hilker and Meiners, 2002). The process ofodor detection and consequent parasitoid responses is dependenton neural transmissions, which are expected to be affected by neu-rotoxic insecticides, including pyrethroids, commonly used in var-ious agro-ecosystems (Haynes, 1988; Soderlund and Bloomquist,1989; Croft, 1990; Salerno et al., 2002; Stark and Banks, 2003; Des-neux et al., 2004a,b; Desneux et al., 2007). This aspect has beeninvestigated here on Telenomus busseolae Gahan (Hymenoptera:Scelionidae), an egg parasitoid of the corn stalk borer, S. nonagrio-ides Lefebvre (Lepidoptera: Noctuidae).

ll rights reserved.

e@gmail.com (A. Bayram).

al. Sub-lethal effects of two pyral Control (2009), doi:10.1016/

S. nonagrioides is a major multivoltine pest of maize in Mediter-ranean countries (Tsitsipis, 1988; Alexandri and Tsitsipis, 1990;Kornasor et al., 1995; Sertkaya et al., 1999) with a high reproduc-tive capability and low economic injury levels (Bayram, 2003). Thelarvae of this pest, by tunneling into the stem and cobs, cause sig-nificant crop losses in maize, reduce the nitrogen/protein ratio ofgrain (Bayram, 2003), and may be associated with mycotoxigenicfungi (Avantaggiato et al., 2003). Chemicals, including the syn-thetic pyrethroids (notably cypermethrin, lambda-cyhalothrin, cyf-luthrin and deltamethrin), are the principal agents used to controlS. nonagrioides in Mediterranean countries. Foliar insecticide appli-cations should be made before larvae enter the stalk or cobs andare only moderately effective due to the endophytic nature of thelarvae (Tsitsipis, 1988). Therefore, because egg parasitoids like T.busseolae are of great potential for limiting this pest, integratedpest management (IPM) should combine both chemical and biolog-ical control strategies (Sertkaya et al., 1999; Conti and Bin, 2000;Conti et al., 2003).

T. busseolae is one of the most important natural enemies of themaize stem borers Sesamia spp. and Busseola fusca (Fuller) (Lepi-

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012

2 A. Bayram et al. / Biological Control xxx (2009) xxx–xxx

ARTICLE IN PRESS

doptera: Noctuidae) (Alexandri and Tsitsipis, 1990; Sétamou andSchulthess, 1995; Sertkaya et al., 1999). Because of the T. busseolaespecialization in parasitizing concealed egg masses (Conti and Bin,2000; Conti et al., 2003; Bayram et al., 2004) the parasitism of S.nonagrioides eggs by this parasitoid may reach 65% and may evenincrease up to 100% by the end of the plant growing season (Alex-andri and Tsitsipis, 1990; Kornosor et al., 1995; Sertkaya et al.,1999). Recent attempts to achieve biological control of S. nonagrio-ides by using T. busseolae demonstrated long-term storage possibil-ities for this parasitoid without altering its fitness parameters(Bayram et al., 2005).

During the host location process, T. busseolae females use thesex pheromone of its host as a long-range cue (Colazza et al.,1997), and both the synomones that are induced systemically inthe plant by S. nonagrioides oviposition (Conti and Salerno, per-sonal observations) and the scales of the hosts are used as short-range cues (Colazza and Rosi, 2001; Conti et al., 2003). The secre-tions from the host’s colleterial glands act as a host recognitionkairomone (De Santis et al., 2008).

Insecticides used in maize agro-ecosystems for control of S. non-agrioides may adversely affect T. busseolae efficacy, not only be-cause of lethal effects on parasitoid populations, but also becauseof sub-lethal effects on parasitoid biology and host-searching andparasitization abilities. Indeed, the lowest efficacy of natural con-trol exerted by T. busseolae was recorded in fields where S. nonag-rioides was controlled using insecticides (Sertkaya, 1999). To date,no detailed studies have been conducted on insecticide usage andits compatibility with T. busseolae as an important part of IPM incorn. Previous studies on the side-effects of insecticides on scelio-nid egg parasitoids mainly dealt with Trissolcus spp., and focusedon the adult parasitoids which emerged from treated host eggs(Smilanick et al., 1996; Saber et al., 2005), on their emergence rate(Orr et al., 1989; Zeren et al., 1994; Kivan, 1996), and on insecticidetoxicity toward adults under field or laboratory conditions (Orret al., 1989; Zeren et al., 1994). Additionally, Salerno and co-authors (2002) found significant sub-lethal effects of the LD25 ofdeltamethrin on the arrestment response and walking behaviorof Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) to acontact kairomone (chemical traces) from its host, Nezara viridulaL. (Heteroptera: Pentatomidae). Relatively few studies have beencarried out on insecticide side-effects toward parasitoids belongingto the genus Telenomus (Waddill, 1978; Mani and Krisnamoorthy,1986) and none were focused on the sub-lethal effects of insecti-cides on the parasitoid’s physiological and behavioral traits suchas fecundity and responses to the host. Therefore, this study aimedto reveal the sub-lethal effects of deltamethrin and cyfluthrin on T.busseolae females, focusing on the effects on parasitoid life-historytraits and behavioral responses to the volatile and contact cuesmediating host location.

2. Materials and methods

2.1. Insect origin and rearing

T. busseolae used for the experiments originated from parasit-ized eggs of S. nonagrioides collected in 2007, in Adana, Turkeyand were reared in the Entomology Laboratories of the Departmentof Agricultural and Environmental Sciences (D.S.A.A.), at the Uni-versity of Perugia. The parasitoid culture was maintained for 10generations on the eggs of S. nonagrioides under laboratory condi-tions (26 ± 1 �C, 70 ± 5% RH and 16:8 L:D) and fed a diet devised bySafavi (1968).

The host, S. nonagrioides, was reared on the meridic diets de-vised by Giacometti (1995) for larvae and adults, under constantenvironmental conditions (26 ± 1 �C, 70 ± 5% RH and 16:8 L:D).

Please cite this article in press as: Bayram, A., et al. Sub-lethal effects of two pyrthe egg parasitoid Telenomus busseolae. Biological Control (2009), doi:10.1016/

Cardboard cylinders, with parafilm strips rolled onto them, wereused as an oviposition substrate. Females oviposited under theparafilm strips, which allowed the eggs to be collected by unrollingthe strips. Unless otherwise stated, all parasitoid incubations be-fore and after treatments were performed under standard labora-tory conditions (26 ± 1 �C, 70 ± 5% RH and 16:8 L:D).

2.2. Determination of the LC25 of insecticides

The two insecticides used in the experiments were cyfluthrin(Bayteroid 5 EC, Makhteshim Chemical Works, Beer Sheva, Israel)and deltamethrin (Decis Jet 15 EC, Bayer Crop Science, Milan, Italy).

The doses bioassayed with T. busseolae, prepared according tothe formulations of the insecticides, were equivalent to 100%,50%, 25% and 12.5% of the recommended dosages for field applica-tion, and were 3, 1.5, 0.75 and 0.375 ml l�1 for cyfluthrin; and 0.5,0.25, 0.125 and 0.0625 ml l�1 for deltamethrin.

Filter papers (MN 640m Macherey-Nagel, Duren, Germany,55 mm diameter) were dipped into emulsions of different dosesof deltamethrin and cyfluthrin following the method describedby Salerno and co-authors (2002). Then these filter papers were leftunder laboratory conditions under constant ventilation to dry for1 h. The control groups were treated with distilled water only.

Parasitoid exposure to insecticide-impregnated or control pa-pers was conducted by using cylindrical arenas constructed fromtransparent plexiglass (40 mm internal diameter, 5 mm internalheight) sandwiched between two glass plates (75 � 75 mm) andkept firmly in place by clips. Three holes (3 mm diameter) weredrilled through the wall of the arena for ventilation to prevent afumigation effect inside the arena. One hole was used for introduc-tion of the parasitoids and was later closed with a bamboo stopper.The other two holes were drilled on opposite sides of the lateralwall and covered with metallic mesh to prevent the parasitoidsfrom escaping from the arena. Clean air was allowed to pass atan average rate of 0.23 ml s�1 through the two holes by using tub-ing connected to a pump.

As mentioned above, T. busseolae is morphologically (it has adorso-ventrally flattened body shape) and behaviorally specializedfor parasitizing concealed host eggs through its ability to crawl un-der corn leaf sheaths (Conti and Bin, 2000). Because of this adapta-tion, this parasitoid always tends to escape from closedenvironments by crawling through small crevices. All internal sur-faces of the arena (i.e., the wall and both bases) were thereforecarefully covered with portions of treated or control filter paper.Specifically, the wall was covered with a filter paper strip(5 � 126 mm) by using double-sided adhesive tape, which wasthen drilled by a tiny pin to ensure ventilation through the lateralholes. The arenas were immediately prepared after desiccation ofthe filter papers and the strips were left under laboratory condi-tions (10 �C and complete dark) 12 h prior to the laboratory bioas-says, which were performed between 0700 and 1900 h. Arenaswere kept under constant room conditions (23 ± 1 �C, 50 ± 10%RH and 16:8 L:D).

Preparative to the experiments, T. busseolae females were keptwith males at emergence for 24–36 h to allow mating. Then theywere placed individually into glass vials (10 mm diameter,35 mm high) with a diet devised by Safavi (1968), and kept for12 h before the experiment. About 20 mated, fed, 1- to 2-day-oldfemale parasitoids were introduced carefully into the arenasthrough the third hole by a mouth aspirator, which was thenclosed by a bamboo stopper. Three replicates were carried outfor each treatment, and a total of 278 and 294 females for cyfluth-rin and deltamethrin, respectively, was tested. During the experi-ments, the arenas were checked every hour, and were rotated toensure parasitoid movement on the filter paper. After a treatmentperiod of 12 h, the arenas were opened gently, all parasitoids

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012

A. Bayram et al. / Biological Control xxx (2009) xxx–xxx 3

ARTICLE IN PRESS

(apparently dead or alive) were removed and singly transferredwith mouth aspirator to glass tubes (10 mm diameter, 35 mmhigh) containing the diet, and kept under constant laboratory con-ditions. The numbers of dead and alive parasitoids were assessed24 h after exposure to allow for recovery of knocked-outindividuals.

Response curves based on the logarithm of dose were estimatedby using a generalized linear model with binomial error and logitlink function (Stark and Banks, 2003; Robertson et al., 2007). Thelethal concentrations of both insecticides were derived from thefitted model by using the dose–response package (drc) in the R sta-tistical environment (Ritz and Streibig, 2005; R Development CoreTeam, 2008). For the experiments on physiological and behavioralsub-lethal effects we chose the LC25 because this is below the 30%mortality threshold recommended for the use of insecticides inIPM (Croft, 1990; Barrett et al., 1994; Desneux et al., 2004a).

2.3. Fecundity of LC25-treated female adults, percentage of emergenceand sex ratio of offspring

Preparative to the experiments, T. busseolae females were keptwith males at emergence for 24–36 h to allow mating. Then theywere placed individually in glass vials (10 mm diameter, 35 mmhigh) containing a diet devised by Safavi (1968), and kept for12 h before the experiment. Twenty mated, fed and naïve (i.e.,which had no foraging experience with the host) female parasit-oids were introduced into the cylindrical arenas containing filterpaper impregnated with the LC25 of cyfluthrin, deltamethrin, orwith distilled water (control). The treatments were conductedusing the same procedure described above and lasted for 12 h. Fivereplicates were carried out for each treatment with 20 femaleseach; therefore, a total of 100 female parasitoids were exposed toeach treatment. At the end of the experiment the arenas wereopened carefully and the surviving parasitoids were gently re-moved by using a mouth aspirator and singly transferred into glasstubes (30 mm diameter, 160 mm high), where they were providedwith the diet and kept under constant laboratory conditions.

For fecundity experiments, 20 randomly chosen female parasit-oids from each treatment were introduced singly into glass tubes(10 mm diameter, 35 mm high) for 24 h, each containing one fresh(<12 h old) S. nonagrioides egg mass (100 ± 5 eggs) glued on card-board. The egg mass was replaced with an unparasitized freshegg mass after 24 h to evaluate the 24-to-48-h fecundity of theparasitoids. All egg masses were then labeled and incubated for20 days, though most of the emergences occurred within 17 daysof the initial parasitism. After the incubation period, the numberof parasitized eggs, percentage of emergence and sex ratio of theoffspring were recorded for each treatment. Data over 48 h werecalculated by pooling those obtained from each 24-h period.

One-way ANOVA was used to analyze the effects of exposure onfecundity of T. busseolae over 48 h, percentage emergence, and sexratio of the offspring. Means were separated by the Fisher’s LSDtest (a = 0.05). The data in percentages were arcsine-square roottransformed and the data on fecundity were log-transformed priorto the analyses in order to satisfy assumptions of normality.

2.4. Longevity of treated adults

Exposure of parasitoid adults to the LC25 of deltamethrin andcyfluthrin, along with an untreated control experiment, was car-ried out using the same procedure described above. After 12 h ofexposure, female parasitoids were removed from the arena andtransferred singly into glass vials (30 mm diameter, 160 mm high)provided with the diet, labeled, and kept under constant laboratoryconditions. Parasitoid survival was checked and recorded daily un-til all individuals died. The diet was renewed when necessary.

Please cite this article in press as: Bayram, A., et al. Sub-lethal effects of two pyrthe egg parasitoid Telenomus busseolae. Biological Control (2009), doi:10.1016/

Twenty-three replications were carried out for the control and cyf-luthrin and 21 replications for deltamethrin.

The data on the longevity of T. busseolae females were analyzedwith one-way ANOVA, followed by Fisher’s LSD test (multiple com-parison based on a confidence interval at 95%) to identify signifi-cant differences between groups. The data were log-transformedprior to the analyses in order to satisfy assumptions of normality.

2.5. Behavioral responses to the host sex pheromone

The parasitoid females, insecticide-treated or untreated as de-scribed previously (maintained at 23 ± 1 �C and 50 ± 10% RH), weretransferred singly into glass vials (10 mm diameter, 35 mm high)and kept under constant laboratory conditions for 12 h beforethe bioassays.

The behavioral responses of T. busseolae females (that survivedthe LC25 treatments) to the sex pheromone of S. nonagrioides wereinvestigated in a Y-tube olfactometer in plexiglass (stem 90 mm;arms 80 mm at a 130� angle; internal section 15 � 15 mm) sand-wiched between two glass plates (Colazza et al., 1999b). Medical-grade compressed air flowed through both arms at 144 ml min�1

per arm. The flow was regulated by flowmeters and bubbledthrough a water jar to humidify the air before it passed into theolfactometer. The olfactometer was surrounded by a black fabriccurtain to minimize possible cues from the room and was illumi-nated by two 22-W cool white fluorescent tubes located abovethe device. Both arms were connected to glass jars. Because sexpheromone emission by virgin S. nonagrioides fluctuates in timeand lasts for 4–6 h after the onset of scotophase (Babilis andMazomenos, 1992), we used commercially available synthetic sexpheromone, loaded in rubber septa (Novapher, Milan, Italy), to pro-vide a stable odor source in all bioassays. The rubber septum wassuspended by means of a wire in one of the two glass jars, whichwere sealed with parafilm tape to prevent loss of the odorant.

In each experiment, a single odor source was used in one arm ofthe Y olfactometer, while the other unbaited arm served as a con-trol, i.e., with only humidified air. To reduce variability, all bioas-says were conducted in a completely randomized design andwere performed during daytime (between 0800 and 1700 h) at23 ± 1 �C and 50 ± 10% RH. The same olfactometer and jars wereused for two to three bioassays, including parasitoids from LC25-treated and untreated controls. After each set of trials, the glassplates and the glass jars were cleaned with hexane, acetone, etha-nol and distilled water, and the plexiglass part of the olfactometerwas cleaned with a laboratory detergent, rinsed with hot tap water(90 �C, for 5 min) and finally with distilled water. In order to avoidthe possible presence of bias between the two olfactometer arms,the olfactometer arm loaded with the odor source was changedafter each set of bioassays.

One female parasitoid was introduced into the Y-tube at the en-trance of the stem. The parasitoid’s walking pattern was then re-corded for 10 min with a monochrome CCD video camera (SonySSC M370 CE) fitted with a 12.5–75 mm/F1.8 zoom lens. To ex-clude reflected light, the olfactometer was illuminated by infraredlight (homogenous emission of wavelengths at 950 nm providedby 108 LEDs) from below, and the camera lens was covered withan infrared pass filter (Kodak Wratten filter 87A�). Analog videosignals from the camera were digitalized by a video frame grabber,and digital data were processed by XBug (Colazza et al., 1999a).Each parasitoid was allowed 10 min to choose one of the arms ofthe olfactometer; then it was discarded whether or not it had madea choice. A choice was considered to have been made when a wasppassed a threshold line located 3 cm from the beginning of the armand remained there for 20 s. The following parameters were calcu-lated to describe parasitoid walking patterns: residence time per-centage, i.e., the percentage of total time spent in each of the

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012

4 A. Bayram et al. / Biological Control xxx (2009) xxx–xxx

ARTICLE IN PRESS

olfactometer arms; and average linear speed in each arm (millime-ters per second). Data were analyzed with t-tests for paired com-parisons and, prior to analysis, were subjected to angular orsquare root transformation to satisfy the assumption of normality(Sokal and Rohlf, 1995). Twenty-one replicates were carried out forthe control, 19 for cyfluthrin, and 16 for deltamethrin.

2.6. Behavioral responses to host abdominal scales

Parasitoids were treated with the LC25 of both insecticides orwith distilled water as a control for 12 h at 23 ± 1 �C and50 ± 10% RH. After the treatment, surviving females were gentlytransferred singly into glass vials (10 mm diameter, 35 mm high),provided with the diet, and kept under constant laboratory condi-tions for 12 h before the bioassays.

The parasitoid arrestment response to the scales of its host wasinvestigated on a filter paper open arena (185 mm diameter),where the parasitoids could move in an unconstrained field. A cen-tral circular area (10 mm diameter) in the open arena was contam-inated by gently brushing abdominal scales of three virgin S.nonagrioides females (<24 h old). Two 22-W cool white fluorescenttubes that simulate daylight were located above the device to illu-minate the arena. The locomotory behavior of each female was re-corded with the same system used in the previous experiments.

One female parasitoid was gently dropped into the scale-con-taminated circle. The bioassays started immediately and continuedfor 15 min, or were stopped when the parasitoid flew from orwalked out of the arena. To reduce variability, all bioassays wereconducted in a completely randomized design and were performedduring daytime at 23 ± 1 �C and 50 ± 10% RH. The same arena wasused for a set of two to three bioassays, using parasitoids from thedifferent treatments and/or untreated controls. After each set oftrials, the arena was changed with a new host scale-contaminatedarena. The equipment used for preparation of the arena wascleaned with hexane, ethanol, and distilled water. The parasitoidsused in the bioassays were naïve (had no contact with the host)and were used only once.

The following two parameters were calculated to describe theparasitoid arrestment response to its host: total time spent in thehost scale-contaminated area, and average linear speed (millime-ters per second). Data were then subjected to one-way ANOVA.Eighteen replicates were carried out for both the control and cyf-luthrin and 20 for deltamethrin.

Table 2Longevity and fecundity of T. busseolae females after exposure for 12 h to the LC25 ofcyfluthrin or deltamethrin or to distilled water, and the sex ratio and emergence of

3. Results

3.1. Determination of the LC25 for deltamethrin and cyfluthrin

LC25 values for cyfluthrin and deltamethrin after 12 h of treat-ment, calculated from the fitted model by using the dose–responsecurve package of R environment, were equal to 0.081398 and0.017456 ml l�1 respectively (Table 1). These LC25 values wereused to treat adult T. busseolae to determine the effects of the

Table 1Dose–response statistics for cyfluthrin and deltamethrin on Telenomus busseolaefemales.

Insecticide n Slope ± SE Lethal concentrationsLC25 (95% FL)

Cyfluthrin (Bayteroid) 278 1.36 ± 0.35 0.081 (0.007–0.170)Deltamethrin (Decis Jet) 294 1.41 ± 0.31 0.017 (0.002–0.032)

Lethal concentrations and 95% fiducial limits (FL) were estimated by using a non-linear fitted dose–response model (drc, R environment).

Please cite this article in press as: Bayram, A., et al. Sub-lethal effects of two pyrthe egg parasitoid Telenomus busseolae. Biological Control (2009), doi:10.1016/

two insecticides on adult fecundity and longevity, behavioral re-sponses to host cues, and the emergence rate and sex ratio of theirprogeny.

3.2. Sub-lethal effects on the biology of treated female parasitoids andtheir progeny

T. busseolae females exposed to the LC25 of either insecticidelived shorter than the untreated parasitoids (F = 4.761, df = 2, 64,P = 0.012) (Table 2). The fecundity, i.e., the total number of eggsparasitized per surviving female after 12 h exposure to the LC25

of deltamethrin and cyfluthrin, also varied significantly(F = 3.995, df = 2, 57, P = 0.024). The parasitoids exposed to cyfluth-rin were less fecund than the control parasitoids, whereas the dif-ference between the deltamethrin-treated and control parasitoidswas not significant (Table 2).

On the other hand, treatment of adult females with the LC25 ofthe insecticides had no harmful effects on the development of theiroffspring. The sex ratios of the offspring from treated and controlfemales, which were strongly female-biased as expected for thisspecies, were not affected by the treatments (F = 0.086, df = 2, 57,P = 0.918) (Table 2). Similarly, the percentage of emergence of off-spring was always higher than 98% and not significantly differentamong the treatments (F = 0.242, df = 2, 57, P = 0.786) (Table 2).

3.3. Sub-lethal effects on host-searching behavior of treated femaleadults

Only the treatment with cyfluthrin affected the behavioral re-sponses of T. busseolae to the synthetic sex pheromone of its host,S. nonagrioides. Parasitoid females exposed to the LC25 of cyfluthrinspent a similar percentage of time in the two arms of the Y olfac-tometer (t = �0.609, df = 18, P = 0.550), showing no orientation to-ward odors and thus indicating an effect of the insecticide onparasitoid behavior. In contrast, the parasitoids exposed to theLC25 of deltamethrin (t = 2.188, df = 15, P = 0.045) or, as expected,to distilled water (control) (t = 2.269, df = 20, P = 0.034), spentmore time in the arm containing the sex pheromone, comparedto the arm without the pheromone (control) (Fig. 1). Similarly,the cyfluthrin-treated females showed similar linear speeds inthe two Y olfactometer arms (t = 1.712, df = 11, P = 0.113), whereasthe deltamethrin-treated females (t = �2.35, df = 12, P = 0.037) andthe control females significantly responded to the sex pheromoneby reducing their linear speeds in the pheromone-containing arm(t = �2.294, df = 19, P = 0.033) (Fig. 2).

The time spent by the insecticide-treated and untreated parasit-oids in the open arena area that had been contaminated with hostscales was not significantly different among the different treat-ments and control (F = 0.041, df = 2, 53, P = 0.959). Similarly, therewere no significant differences in parasitoid linear speeds(F = 0.601, df = 2, 53, P = 0.552) (Fig. 3).

their F1 offspring (Mean ± SEM).

Treatment Longevity(d)

Fecundity(No. ofparasitizedeggs over48 h)

Sex ratio(% female)

Emergence(%)

Cyfluthrin 11.65 ± 2.69b 65.95 ± 3.79b 82.59 ± 0.87a 98.37 ± 0.63aDeltamethrin 11.04 ± 0.64b 68.55 ± 2.35ab 82.20 ± 1.11a 98.26 ± 0.47aControl

(distilledwater)

19.13 ± 3.43a 75.90 ± 2.14a 83.01 ± 0.80a 98.28 ± 0.80a

Columns with the same letter are not significantly different (LSD test, P < 0.05).

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012

Fig. 1. Percentage of total time (Mean ± SEM) spent by treated (LC25 of cyfluthrin or deltamethrin) and control (distilled water) females of T. busseolae in the arm of a Yolfactometer with an airflow carrying the synthetic host pheromone compared to the control arm. Asterisks denote significant differences (Student’s t-tests, P < 0.05).

Fig. 2. Linear speed (Mean ± SEM) of treated (LC25 of cyfluthrin or deltamethrin) and control (distilled water) females of T. busseolae in the arm of a Y olfactometer with anairflow carrying the synthetic host pheromone compared to control arm. Asterisks denote significant differences (Student’s t-tests, P < 0.05).

Resi

denc

e �

me

(s)

0

200

400

600

800

1000

1200

1400

cyfluthrin deltamethrin control

0.0

0.5

1.0

1.5

2.0

2.5

a a a

A A

A

Line

ar s

peed

(mm

/s)

Fig. 3. Residence time (columns) (Mean ± SEM) and linear speed (dots) (Mean ± SEM) of treated (LC25 of cyfluthrin or deltamethrin) and control (distilled water) females of T.busseolae in an open arena area that was contaminated with host abdominal scales. Different letters above bars indicate significantly different means (ANOVA; P < 0.05).

A. Bayram et al. / Biological Control xxx (2009) xxx–xxx 5

ARTICLE IN PRESS

4. Discussion

For successful integration of biological and chemical control inan IPM program, knowledge of the effects that pesticides have onbeneficial arthropods is necessary (Croft, 1990). There are severalapproaches utilized to study the effects of pesticides on naturalenemies, such as topical application or ingestion of toxins, expo-

Please cite this article in press as: Bayram, A., et al. Sub-lethal effects of two pyrthe egg parasitoid Telenomus busseolae. Biological Control (2009), doi:10.1016/

sure of natural enemies to sub-lethal doses (residues), or fieldstudies assessing changes in natural enemy populations in re-sponse to pesticide application (Longley and Jepson, 1996a; Long-ley, 1999; Alix et al., 2001; Desneux et al., 2005). Each approachprovides different information related to pesticide impact on natu-ral enemies. Topical application and ingestion of toxins provideknowledge about direct effects and acute toxicity to insects. Expo-

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012

6 A. Bayram et al. / Biological Control xxx (2009) xxx–xxx

ARTICLE IN PRESS

sure of natural enemies to lethal or sub-lethal doses of insecticidesprovides important information about the compatibility of thechemical and biological control as well as the effect of the insecti-cide on natural enemies (Desneux et al., 2007). Natural enemiessurviving a previous exposure to a pesticide may still have sus-tained subtle or overt significant damage that may be manifestedas alterations to biological (e.g., fecundity, longevity, sex ratio)(Croft, 1990; Stark and Banks, 2003; Desneux et al., 2007) andbehavioral traits (Haynes, 1988; Salerno et al., 2002; Desneuxet al., 2007).

Our study showed that application of the LC25 of cyfluthrin nega-tively affects the fecundity of T. busseolae, whereas deltamethrin hasno such effect. On the other hand, neither insecticide adversely af-fected the emergence and sex ratios of the offspring of treated fe-males. Our results concerning reduction in fecundity are partlyconcordant with results of other authors, although their researchinvestigated different parasitoid species and different insecticides:Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammati-dae) treated with LD20 of chlorpyrifos (Delpuech and Meyet, 2003);Trichogramma cacoeciae Marchal treated with six insecticides andtwo mineral oils (Youssef et al., 2004); and Trybliographa rapae(Hymenoptera: Fitigidae) treated with LD10 of chlorfenvinphos.Egg resorption has been considered as a possible cause of reducedfecundity (Alix et al., 2001). However, we can likely exclude this pos-sibility in T. busseolae because this proovigenic species shows no eggresorption after up to 14 days of host deprivation (Chabi-Olaye et al.,1997). Therefore, if we consider that cyfluthrin also negatively af-fects the parasitoid behavioral response to host sex pheromone,the observed reduction in fecundity over 48 h may be due to pertur-bations in behavioral responses rather than reduction of egg load.However, this aspect requires further investigation.

The longevity of T. busseolae females treated with the LC25 ofeither deltamethrin or cyfluthrin was significantly reduced in com-parison to the control. The effect of insecticides on longevity of par-asitoids seems to be highly dependent on the type of insecticide,the parasitoid species, and the method of application. Reductionsin longevity have been generally observed in parasitoids that hadbeen exposed to insecticides when developing inside of hosts(Rosenheim and Hoy, 1988; Smilanick et al., 1996; Suh et al.,2000; Desneux et al., 2006a,b), although in some cases no reduc-tions in longevity were indicated (Saber et al., 2005). Instead, veryfew studies have reported alterations of biological features of par-asitoids as a consequence of treating adults. Alix et al. (2001) founda significant reduction in longevity of males and females of Trybli-ographa rapae topically treated with LD10 of chlorfenvinphos. In thepresent study, the reduced longevity of T. busseolae females in-duced by exposure to the LC25 of the insecticides may not affectthe reproductive efficacy of the parasitoids under field conditionsbecause the parasitoid lays most of its eggs (>70%) within 72 h ofemergence (Chabi-Olaye et al., 1997; Sertkaya and Kornosor,2003). However, premature death in female parasitoids may affectthe reproduction of T. busseolae when host eggs are not readilyavailable for the parasitoid during the initial part of its lifespan.

The ability to locate a host and then the time allocated to host-searching are critical in parasitoids that are considered to be effec-tive agents for biological control of pests. Therefore, the two mainkairomones used by T. busseolae females for location of the eggs ofS. nonagrioides, i.e., the sex pheromone and chemicals from theabdominal scales of virgin females, are two important cues foroptimizing host-searching (Colazza et al., 1997; Conti et al.,2003). In our experiments, only cyfluthrin appeared to reduce par-asitoid responsiveness to the host sex pheromone, whereas no sig-nificant insecticide effects were observed on the parasitoid’scapacity to respond to host scales.

Pyrethroid effects on parasitoid responses to host cues could beexpected based on results of previous studies (Haynes, 1988; Croft,

Please cite this article in press as: Bayram, A., et al. Sub-lethal effects of two pyrthe egg parasitoid Telenomus busseolae. Biological Control (2009), doi:10.1016/

1990; Salerno et al., 2002; Desneux et al., 2007) and because of theknown mechanism of action of these insecticides, together withthe knowledge that detection of chemical stimuli and its associationwith orientation behavior is entirely dependent on nervous trans-missions. Targets of pyrethroids are directly linked with neuraltransmissions by modification of sodium channels, GABA receptors,calcium and chloride channels, and peripheral-type benzodiazepinereceptors (Soderlund and Bloomquist, 1989; Narahashi et al., 1992;Soderlund et al., 2002). However, in our study, cyfluthrin interferedwith kairomone perception whereas no effects of deltamethrin weredetected. A possible explanation may be that all behavioral observa-tions undertaken on T. busseolae were performed 12 h after the expo-sure. This period may enable parasitoids to compensate for sub-lethal effects of deltamethrin, as was reported in the case of aphidparasitoids, i.e., foraging behaviors of Aphidius rhopalosiphi De Ste-fani-Perez (Hymenoptera: Braconidae) were normalized over a 12-h period after exposure to deltamethrin residues (Longley and Jep-son, 1996b). Orientation behavior of the aphid parasitoid, Aphidiuservi Haliday (Hymenoptera: Braconidae) toward aphid-infestedplants was not modified after exposure to deltamethrin (Desneuxet al., 2006a) or lambda-cyhalothrin (another synthetic pyrethroid)residues (Desneux et al., 2004a). All altered behaviors induced bysub-lethal doses of lambda-cyhalothrin disappeared within 24 h(Desneux et al., 2004a).

In the present study, the behavioral responses of T. busseolae tocontact cues, i.e., abdominal scales of virgin S. nonagrioides werenot affected by the LC25 of either insecticide. These short-rangekairomonal cues are used during the final steps of the host selec-tion process by T. busseolae, before host recognition and hostacceptance (Colazza and Rosi, 2001; Conti et al., 2003). Our resultsreported here suggest that the two pyrethroid treatments do notaffect the arrestment response of T. busseolae upon its contactingthe host kairomone. However, we cannot exclude the possibilitythat an effect could have occurred earlier on after treatment, butthat the parasitoids had recovered in the 12 h that had elapsedsince the end of the treatment. Trichogramma brassicae Bezdenko(Hymenoptera: Trichogrammatidae) males exposed to a sub-lethaldose of deltamethrin showed no differences in their behavioral re-sponses (locomotory activity and residence time) to an area con-taminated with the sex pheromone from females (Delpuechet al., 2001). Salerno et al. (2002) reported that Trissolcus basalis fe-males treated with LD25 of deltamethrin showed a significantlylower residence time on host-contaminated patches compared tountreated females, and that the treatment also temporarily re-duced parasitoid walking speed. The LC25 of deltamethrin for T.busseolae in our study was much lower than that for T. basalis (Sal-erno et al., 2002), determined by the same method, possibly be-cause of the larger size of the latter parasitoid. Such a differencein the LC25 for the two parasitoid species may explain the differenteffects of deltamethrin.

To our knowledge, the present study is the first attempt to testthe sub-lethal effects of pyrethroids on parasitoid responses to vol-atile and contact kairomonal cues mediating host location, to-gether with parasitoid fecundity and longevity. The combinationof biological and behavioral studies provides valuable informationfor IPM decision-making on the possibility of using T. busseolaewith selected pyrethroids. If T. busseolae females are exposed toresidues of cyfluthrin in a treated field, their capacity to migrateto non-treated fields infested by S. nonagrioides and to locate hostpopulations would be impaired because of their lower ability to re-spond to the host sex pheromone, in addition to being less fecundand shorter lived; reduced efficacy, therefore, should be expected.However, because of the repellency effects of pyrethroids, undernatural field conditions T. busseolae females may avoid treatedfields or plants or may not remain confined to such environmentsfor long. Therefore field or semi-field studies should be performed

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012

A. Bayram et al. / Biological Control xxx (2009) xxx–xxx 7

ARTICLE IN PRESS

to evaluate the role of the sub-lethal effects of these pyrethroids onthe T. busseolae host location capacity.

Acknowledgments

We would like to thank Andrea Luchetti, Donatella Marchionni,Daniela Fortini, and Cesare Dentini for maintaining the insect cul-tures and Fulvio Ielo for help during data collection. We also wouldlike to thank the European Science Foundation – Behavioral Ecol-ogy of Insect Parasitoids (ESF-BEPAR) program for financially sup-porting the first author (A. Bayram) with an exchange grant (GrantNo: 1953).

References

Alexandri, M.P., Tsitsipis, J.A., 1990. Influence of the egg parasitoid Platytelenomusbusseolae (Hym.: Scelionidae) on the population of Sesamia nonagrioides (Lep.:Noctuidae) in Central Greece. Entomophaga 35, 61–70.

Alix, A., Cortesero, A.M., Nenon, J.P., Anger, J.P., 2001. Selectivity assessment ofchlorfenvinphos reevaluated by including physiological and behavioral effectson an important beneficial insect. Environmental Toxicology and Chemistry 20,2530–2536.

Avantaggiato, G., Quaranta, F., Desiderio, E., Visconti, A., 2003. Fumonisincontamination of maize hybrids visibly damaged by Sesamia. Journal of theScience of Food and Agriculture 83, 13–18.

Babilis, N.A., Mazomenos, B.E., 1992. Pheromone production in Sesamianonagrioides: diel periodicity and effect of age and mating. Journal of InsectPhysiology 38, 561–564.

Barrett, K., Grandy, N., Harrison, E.G., Hassan, S., Oomen, P., 1994. Guidancedocument on regulatory testing procedures for pesticides with non-targetarthropods, SETAC-Europe, p. 51.

Bayram, A., 2003. Development of economic injury levels for Sesamia nonagrioidesLefebvre (Lepidoptera: Noctuidae) and some biological features of its eggparasitoid Telenomus busseolae (Gahan) (Hymenoptera: Scelionidae). Ph.D.Thesis, Natural and Applied Sciences Institute of Cukurova University, Adana-Turkey. No: 767, p. 102 (in Turkish with English abstract).

Bayram, A., Salerno, G., Conti, E., Wajnberg, E., Bin, F., Kornosor, S., 2004. Sexallocation in Telenomus busseolae, a solitary parasitoid of concealed eggs: theinfluence of host patch size. Entomologia Experimentalis et Applicata 111, 141–149.

Bayram, A., Ozcan, H., Kornosor, S., 2005. Effect of cold storage on the performanceof Telenomus busseolae Gahan (Hymenoptera: Scelionidae), an egg parasitoid ofSesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae). Biological Control 35,68–77.

Chabi-Olaye, A., Schulthess, F., Shanower, T.G., Bosque-Perez, N.A., 1997. Factorsinfluencing the developmental rates and reproductive potentials of Telenomusbusseolae (Gahan) (Hym.: Scelionidae), an egg parasitoid of Sesamia calamistisHampson (Lep.: Noctuidae). Biological Control 8, 15–21.

Colazza, S., Rosi, M.C., Clemente, A., 1997. Response of the egg parasitoid Telenomusbusseolae to sex pheromone of Sesamia nonagrioides. Journal of ChemicalEcology 23, 2437–2444.

Colazza, S., Peri, D., Salerno, G., Peri, E., Lo Pinto, M., Liotta, G., 1999a. Xbug, a videotracking and motion analysis system for Linux. XII InternationalEntomophagous Insects Workshop. Pacific Grove, California, September 26–30.

Colazza, S., Salerno, G., Wajnberg, E., 1999b. Volatile and contact chemicals releasedby Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on theegg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biological Control16, 310–317.

Colazza, S., Rosi, M.C., 2001. Differences in the searching behaviour of two strains ofthe egg parasitoid Telenomus busseolae (Hymenoptera: Scelionidae). EuropeanJournal of Entomology 98, 47–52.

Conti, E., Bin, F., 2000. Parasitoids of concealed noctuid eggs and their potential inbiological control of gramineae stemborers. Redia LXXXIII 87, 104.

Conti, E., Salerno, G., Bayram, A., Bin, F., 2003. Strategies involved in host location ofTelenomus busseolae and Trichogramma turkestanica, egg parasitoids of Sesamianonagrioides. Abstracts from the XIII International Entomophagous InsectsWorkshop, p. 30. Journal of Insect Science 3, 33.

Croft, B.A., 1990. Sublethal influences. In: Arthropod Biological Control Agents andPesticides. Wiley Interscience, New York, pp. 157–183.

De Santis, F., Conti, E., Romani, R., Salerno, G., Parillo, F., Bin, F., 2008. Colleterialglands of Sesamia nonagrioides as a source of the host-recognition kairomone forthe egg parasitoid Telenomus busseolae. Physiological Entomology 33, 7–16.

Delpuech, J.M., Legallet, B., Fouillet, P., 2001. Partial compensation of the sublethaleffect of deltamethrin on the sex pheromonal communication of Trichogrammabrassicae. Chemosphere 42, 985–991.

Delpuech, J.M., Meyet, J., 2003. Reduction in the sex ratio of the progeny of aparasitoid wasp (Trichogramma brassicae) surviving the insecticide chlorpyrifos.Archives of Environmental Contamination and Toxicology 45, 203–208.

Desneux, N., Pham-Delegue, M.H., Kaiser, L., 2004a. Effect of sub-lethal and lethaldose of lambda-cyhalothrin on oviposition experience and host searching

Please cite this article in press as: Bayram, A., et al. Sub-lethal effects of two pyrthe egg parasitoid Telenomus busseolae. Biological Control (2009), doi:10.1016/

behaviour of a parasitic wasp, Aphidius ervi. Pest Management Science 60, 381–389.

Desneux, N., Rafalimanana, H., Kaiser, L., 2004b. Dose–response relationship inlethal and behavioural effects of different insecticides on the parasitic waspAphidius ervi. Chemosphere 54, 619–627.

Desneux, N., Fauvergue, X., Dechaume-Moncharmont, F.X., Kerhoas, L., Ballanger, Y.,Kaiser, L., 2005. Diaeretiella rapae limits Myzus persicae populations followingapplications of deltamethrin in oilseed rape. Journal of Economic Entomology98, 9–17.

Desneux, N., Denoyelle, R., Kaiser, L., 2006a. A multi-step bioassay to assess theeffect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere 65,1697–1706.

Desneux, N., Ramirez-Romero, R., Kaiser, L., 2006b. Multistep bioassay to predictrecolonization potential of emerging parasitoid after a pesticide treatment.Environmental Toxicology and Chemistry 25, 2675–2682.

Desneux, N., Decourtye, A., Delpuech, J.M., 2007. The sublethal effects of pesticideson beneficial arthropods. Annual Review of Entomology 52, 81–106.

Giacometti, R., 1995. Rearing of Sesamia nonagrioides Lefebvre on meridic diet(Lepidoptera, Noctuidae). Redia 78, 19–27.

Haynes, H.F., 1988. Sublethal effects of neurotoxic insecticides on insect behavior.Annual Review of Entomology 33, 149–168.

Hilker, M., Meiners, T., 2002. Chemoecology of insect eggs and egg deposition.Blackwell Pub., Oxford.

Kivan, M., 1996. Effects of some insecticides that are used controlling Eurygasterintegriceps Put. (Hem., Scutelleridae) on emergence of its egg parasitoidTrissolcus semistriatus Nees. (Hym., Scelionidae). Turkish Journal ofEntomology 20, 27–34 (in Turkish with English abstract).

Kornosor, S., Sertkaya, E., Ozpinar, A., 1995. Distribution of the egg parasitoidPlatytelenomus busseolae (Gahan) (Hym.: Scelionidae) and its effect on thepopulation of Sesamia nonagrioides Lef. (Lep.: Noctuidae) in the Mediterraneanregion of Turkey. In: Wajnberg, E. (Ed.), Fourth International Symposium ofTrichogramma and Other Egg Parasitoids, Les Colloques de INRA, Paris. No. 73,pp. 193–199.

Longley, M., Jepson, P.C., 1996a. Effects of honeydew and insecticide residues on thedistribution of foraging aphid parasitoids under glasshouse and field conditions.Entomologia Experimentalis et Applicata 81, 189–198.

Longley, M., Jepson, P.C., 1996b. The influence of insecticide residues on primaryparasitoid and hyperparasitoid foraging behaviour in the laboratory.Entomologia Experimentalis et Applicata 81, 259–269.

Longley, M.A., 1999. A review of pesticide effects upon immature aphid parasitoidswithin mummified hosts. International Journal of Pest Management 45, 139–145.

Mani, M., Krisnamoorthy, A., 1986. Susceptibility of Telenomus remus Nixon, anexotic parasitoid of Spodoptera litura (F.) to some pesticides. Tropical PestManagement 32, 49–51.

Narahashi, T., Frey, J.M., Ginsburg, K.S., Roy, M.L., 1992. Sodium and GABA-activatedchannels as the targets of pyretroids and cyclodienes. Toxicology Letters 64/65,429–436.

Orr, D.B., Boethel, D.J., Layton, M.B., 1989. Effect of insecticide applications insoybeans on Trissolcus basalis (Hymenoptera: Scelionidae). Journal of EconomicEntomology 82, 1078–1084.

R Development Core Team, 2008. R: A language and environment for statisticalcomputing. R Foundation for Statistical Computing. URL: http://www.R-project.org (ISBN 3–900051–00–3), Vienna, Austria.

Ritz, C., Streibig, J., 2005. Bioassay analysis using R. Journal of Statistical Software12, 1–22.

Robertson, J.L., Russel, R.M., Preisler, H.K., Savin, N.E., 2007. Bioassays withArthropods. CRC Press, Boca Raton, Florida.

Rosenheim, J.A., Hoy, M.A., 1988. Sublethal effects of pesticides on the parasitoidAphytis melinus (Hymenoptera: Aphelinidae). Journal of Economic Entomology81, 476–483.

Saber, M., Hejazi, M.J., Kamali, K., Moharramipour, S., 2005. Lethal and sublethaleffects of fenitrothion and deltamethrin residues on the egg parasitoid Trissolcusgrandis (Hymenoptera: Scelionidae). Journal of Economic Entomology 98, 35–40.

Safavi, M., 1968. Etude biologique et ecologique de hyméptéres parasites des oeufspunaises des céréales. Entomophaga 13, 281–495.

Salerno, G., Colazza, S., Conti, E., 2002. Sub-lethal effects of deltamethrin on walkingbehaviour and response to host kairomone of egg parasitoid Trissolcus basalis.Pest Management Science 58, 663–668.

Sertkaya, E., 1999. Determination of natural enemies of corn stalkborer, Sesamianonagrioides Lefebvre (Lepidoptera, Noctuidae) in Cukurova and investigationson relations with its egg parasitoids Platytelenomus busseolae (Gahan)(Hymenoptera, Scelionidae) and Trichogramma evanescens Westwood(Hymenoptera, Trichogrammatidae). Ph.D. Thesis, Natural and AppliedSciences Institute of Cukurova University, Adana-Turkey, No: 474, p. 90 (inTurkish with English abstract).

Sertkaya, E., Kornosor, S., 2003. Some biological aspects of the egg parasitoid,Telenomus busseolae (Gahan) (Hym., Scelionidae) on the Sesamia nonagrioidesLef. (Lep., Noctuidae) eggs. Turkish Journal of Entomology 27, 231–239 (inTurkish with English abstract).

Sertkaya, E., Bayram, A., Kornosor, S., 1999. Natural parasitization rate ofPlatytelenomus busseolae (Gahan) (Hym.: Scelionidae) and Trichogrammaevanescens Westwood (Hym.: Trichogrammatidae) on Sesamia nonagrioidesLef. (Lep.: Noctuidae) and Ostrinia nubilalis Hbn. (Lep.: Pyralidae) eggs and theirpopulation developments. In: Proceedings of the Fourth Turkish National

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012

8 A. Bayram et al. / Biological Control xxx (2009) xxx–xxx

ARTICLE IN PRESS

Congress of Biological Control (Adana, Turkey), pp. 45–56 (in Turkish withEnglish abstract).

Sétamou, M., Schulthess, F., 1995. The influence of the egg parasitoids belonging tothe Telenomus busseolae (Hymenoptera: Scelionidae) species complex onSesamia calamistis (Lepidoptera: Noctuidae) populations in maize fields insouthern Benin. Biocontrol Science and Technology 5, 69–81.

Smilanick, J.M., Zalom, F.G., Ehler, L.E., 1996. Effect of methamidophos residue onthe pentatomid egg parasitoids Trissolcus basalis and T. Utahensis(Hymenoptera: Scelionidae). Biological Control 6, 193–201.

Soderlund, D.M., Bloomquist, J.R., 1989. Neurotoxic actions of pyrethroidinsecticides. Annual Review of Entomology 34, 77–96.

Soderlund, D.M., Clark, J.M., Sheets, L.P., Mullin, L.S., Piccirillo, V.J., Sargent, D.J.,Stevens, T., Weiner, M.L., 2002. Mechanisms of pyrethroid neurotoxicity:implications for cumulative risk assessment. Toxicology 171, 3–59.

Sokal, R.R., Rohlf, F.J., 1995. Biometry: The Principles and Practice of Statistics inBiological Research. Freeman & C, New York.

Stark, J.D., Banks, J.E., 2003. Population-level effects of pesticides and othertoxicants on arthropods. Annual Review of Entomology 48, 505–519.

Suh, C.P.C., Orr, D.B., Van Duyn, J.W., 2000. Effect of insecticides on Trichogrammaexiguum (Trichogrammatidae: Hymenoptera) preimaginal development andadult survival. Journal of Economic Entomology 93, 577–583.

Please cite this article in press as: Bayram, A., et al. Sub-lethal effects of two pyrthe egg parasitoid Telenomus busseolae. Biological Control (2009), doi:10.1016/

Tsitsipis, J.A., 1988. The corn stalk borer, Sesamia nonagrioides: forecasting, crop-lossassessment and pest management. In: Cavalloro, R., Sunderland, K.D. (Eds.),Integrated Crop Protection in Cereals. Balkema/Rotterdam/Brookfield, pp. 171–177.

Vet, L.E.M., Dicke, M., 1992. Ecology of infochemical use by natural enemies in atritrophic context. Annual Review of Entomology 37, 141–172.

Vinson, S.B., 1998. The general host selection behavior of parasitoid Hymenopteraand a comparison of initial strategies utilized by larvaphagous and oophagousspecies. Biological Control 11, 79–96.

Waddill, V.H., 1978. Contact toxicity of four synthetic pyrethroids and methomyl tosome adult insect parasites. The Florida Entomologist 61, 27–30.

Youssef, A.I., Nars, F.N., Sefanos, S.S., Elkhair, S.S.A., Shehata, W.A., Agamy, E., Herz,A., Hassan, S.A., 2004. The side-effects of plant protection products used in olivecultivation on the hymenopterous egg parasitoid Trichogramma cacoeciaeMarchal. Journal of Applied Entomology 128, 593–599.

Zeren, O., Yigit, A., Gullu, M., 1994. The side effect of some insecticides used insunn pest, Eurygaster integriceps Put. (Hym., Scutelleridae) control on eggparasitoid, Trissolcus spp. Turkiye III. Biyolojik Mucadele Kongresi Bildirileri.Izmir, Ege Universitesi Basimevi, Bornova, Turkey (in Turkish with Englishabstract).

ethroids on biological parameters and behavioral responses to host cues inj.biocontrol.2009.09.012