Response of the Fruit Fly Parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to Mango Fruit Volatiles
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CHEMICAL ECOLOGY Response of the Fruit Fly Parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to Mango Fruit Volatiles MORFA CARRASCO,1 PABLO MONTOYA,2 LEOPOLDO CRUZ-LOPEZ,3 AND JULIO C. ROJAS3 Environ. Entomol. 34(3): 576Ð583 (2005) ABSTRACT The response of Diachasmimorpha longicaudata (Ashmead) females to mango fruit that were intact (healthy), mechanically damaged, or infested with Anastrepha ludens (Loew) larvae, and their respective hexanic and methanolic extracts, was studied using behavioral, electrophysiological, and chemical techniques. Female parasitoids signiÞcantly preferred to visit infested mangoes and their extracts over healthy and mechanically damaged mangoes in wind tunnel and Þeld cage bioassays. This suggests that the presence of the larvae inside the fruit is of clear importance in the host location behavior performed by this species. Methanolic extracts of infested mangoes evoked a signiÞcant electroantennography (EAG) response in female antennae compared with the responses elicited by solvent, healthy, and mechanically damaged mango extracts, but EAG response to hexanic extracts of infested mangoes was only signiÞcant compared with solvent control. Most of the compounds found in infested mango hexanic extracts were commonly found in healthy and mechanically damaged mango hexanic extracts, except 2-phenylethyl acetate, which seems to be exclusively present in infested mangoes. Also, infested mango extracts contain several compounds in higher amounts compared with the other two types of mangoes, as do the methanolic extracts from infested mangos. These differences could explain why female parasitoids preferred to visit infested mangos, with their correspondent methanolic and hexanic extracts. Our results suggest that this species uses a complex mixture of compounds for host location. KEY WORDS mango, Anastrepha ludens, Diachasmimorpha longicaudata, host location behavior Diachasmimorpha longicaudata (Ashmead) is a soli- during location of their herbivore hosts, little infor- tary fruit ßy endoparasitoid native to the Indo-Aus- mation exists on volatiles responsible for attraction, tralian region, which has shown a high capacity of except from Greany et al. (1977), who reported that adaptation to different environments where it has females prefer acetaldehyde over two other attractive been introduced and currently is used for biological fermentation products: ethanol and acetic acid. How- control of fruit ßies in several countries (Camacho ever, the evidence that D. longicaudata ßew upwind 1994, Sivinski et al. 1996, Montoya et al. 2000). In a and landed on healthy fruit (Cheng et al. 1992, Eben multi-trophic context, success of parasitoids as biolog- et al. 2000, this study) also suggests that other com- ical control agents depends mostly on their host lo- pounds, in addition to fermentation products previ- cation behavior, where chemical cues from herbivores ously reported (Greany et al. 1977), may be involved and/or their hosts seems to be an essential component in host location behavior of this species. (Vet and Dicke 1992). In this study, we evaluated the response of D. lon- Host location behavior of this parasitoid has been gicaudata females to healthy, mechanically damaged widely studied. Several studies have shown that ripe, mango fruit and mango fruit infested with larvae of the infested, and/or decomposing fruit are attractive to Mexican fruit ßy, Anastrepha ludens (Loew), and their females of D. longicaudata, and thus chemical com- methanolic and hexanic extracts in Þeld cage and wind pounds seem to be the most important cues used by tunnel bioassays; we also chemically identiÞed the females during the host location process (Greany et al. compounds present in active extracts and performed 1977, Cheng et al. 1992, Messing and Jang 1992, Eben a behavioral evaluation of some of the identiÞed com- et al. 2000, Jang et al. 2000). Despite ample behavioral pounds. evidence that this parasitoid exploits chemical cues Materials and Methods 1 Instituto Tecnológico de Tapachula, Carretera a Puerto Madero km 1, Tapachula, 30700 Chiapas, Mexico. Biological Material. Female parasitoids were ob- 2 Corresponding author: Programa Mosca del Mediterráneo, tained from the Moscafrut mass-rearing facilities DGSV-SAGARPA, Central Poniente 14, Col. Centro, Tapachula, 30700 Chiapas, Mexico (e-mail: firstname.lastname@example.org). (Metapa de Dominguez, Chiapas), following rearing 3 Departamento de Entomologṍa Tropical, El Colegio de la Frontera methods described by Cancino (1997). The parasi- Sur, Apartado Postal 36, Tapachula, 30700 Chiapas, Mexico. toids used were naive when tested, having no previous 0046-225X/05/0576Ð0583$04.00/0 䉷 2005 Entomological Society of America
June 2005 CARRASCO ET AL.: D. longicaudata RESPONSE TO MANGO FRUIT VOLATILES 577 exposure to host larvae or fruit. Fruit were selected placed 25 cm apart in the corner of the upwind end of from mango trees (Mangifera indica L., ÔcriolloÕ) lo- the ßight tunnel. To minimize the inßuence of visual cated in Frontera Hidalgo, Chiapas, Mexico, in lots of cues on wasp responses, fruit was placed into plastic 60 mangoes. After selection, the fruit were kept in containers (9 cm high by 9 cm diameter) that were paper bags to avoid infestation. When the fruit became covered with aluminum wrap with a 1.5-cm opening. ripe, they were cut and separated into three groups. Air previously cleaned with activated charcoal was One group was exposed to females of Anastrepha lu- blown through the containers into the tunnel with a dens (Loew) for infestation at a rate of 10 ßies per fruit pump at a rate of 1 liter/min to provide a continuous for 1 h and then held for 12 d inside an incubator (26 ⫾ ßow of mango odor through the tunnel. Positions 1⬚C and 65 ⫾ 5% RH) to allow the fruit ßy larvae to within the tunnel were alternated for each Þve insects develop to the third instar, which was conÞrmed by to avoid positional bias. Each observation was begun dissection. A second group of ripe mangoes was me- by placing the release cylinder on a 15-cm-high plat- chanically damaged by dropping them on the ßoor form at the downwind end of the tunnel, and one from 2 m high, and they were placed in maturation insect was released and observed for 5 min. The insects boxes for 12 d. A third group of mangoes was held were recorded for taking off, random ßight, hovering without damage or infestation. near the fruit, extract, or compound, and landing on a Fruit Extracts. Healthy, infested, and mechanically source as previously deÞned by Jang et al. (2000). damaged mangoes were weighed and placed by Electroantennography. Antennal receptivity of fe- groups of three in individual 4-liter glass containers. male D. longicaudata to extracts was determined by Fruit were covered with 450 ml of methanol and hex- electroantennography (EAG). An antenna was ex- ane and left at 25⬚C for 24 h. Extracts were concen- cised at its base, and the distal part of the terminal trated to the equivalent of 1 g of fruit per milliliter of segment was cut off. The antenna was mounted be- solvent. The extracts were stored at 5⬚C for later use. tween two glass capillary electrodes. The capillaries Field Cage Bioassays. The response of female para- were Þlled with saline solution into which Ag-AgCl sitoids to mango fruit was evaluated using a wooden wires were inserted (Malo et al. 2002). The signals frame cage (70 by 70 by 70 cm) wrapped with a plastic generated by the antenna were passed through a high- net. Bioassays were carried out from 0830 to 1030 impedance ampliÞer Syntech UN-06 (Syntech NL hours at 29 ⫾ 2⬚C and 70 ⫾ 5% RH and with a light 1200; Hilversum, the Netherlands) and displayed on a intensity of 1,062 lux. Healthy, mechanically damaged, monitor using Syntech software for processing EAG. and infested mangoes were hung 20 cm from the top The stimulus (1-s duration) was delivered into a pu- and bottom of the cage, and they were placed 15 cm riÞed airstream (1 liter/min) ßowing continuously apart. Individual parasitoids were released from small over the preparation. Samples of the standard solu- plastic containers in the bottom of the cage. All ßights, tions test extracts or compounds were applied to Þlter hovering, and landings were recorded for 5 min. One paper strips, and the solvent was allowed to evaporate hundred parasitoids were release individually, and the (20 s). The paper strip was placed in the cartridge or positions of fruit were rotated after each trial. Extracts clean pipette and left for 40 s before applying. The were evaluated in the same way as fruit. Extracts were vapor from the cartridge was injected into the air- loaded on Þlter paper positioned 20 cm from the top stream passing over the antennal preparation by and bottom of the cage and 15 cm apart from each means of a second airstream. A cartridge with a clean other. Individual parasitoids were released in the bot- Þlter paper ⫹ hexane was used as a control. Stimula- tom of the cage. tion with the control preceded and followed every two Wind Tunnel Bioassays. The responses of parasitoid test stimulations. females to healthy, mechanically damaged, and in- Chemical Analysis. Gas chromatographyÐmass fested fruit, their hexanic and methanolic extracts, and spectrometry was made with a Varian Star 3400 CX gas some selected volatile compounds were evaluated in chromatograph linked to a Varian Saturn 4D mass nonchoice (extracts and synthetic compounds) and spectrometer (Varian, Walnut Creek, CA). The hex- two-choice (fruit) tests. Observations were carried anic samples were analyzed using a nonpolar DB-5MS out in a ßight wind tunnel that was 120 cm long and capillary column (30 m by 0.25 mm inner diameter; 30 cm high and wide. A fan was used to pull air through J&W ScientiÞc, Folsom, CA), whereas the methanolic the tunnel at a velocity of 0.2 m/s. Activated charcoal extracts were analyzed using a polar DB-WAX capil- was used to Þlter intake air. Illumination was provided lary column (60 m by 0.32 mm inner diameter; J&W by two ßuorescent bulbs mounted 60 cm above the ScientiÞc), both programmed from 50 to 250⬚C at wind tunnel, giving a light intensity of 230 lux. Wasps 15⬚C/min. The carrier gas was helium. The injector were individually placed in a 5-cm-high plastic pot (4 port temperature was held at 200⬚C. Mass spectral cm inner diameter; release cylinder), and they were identiÞcations were conÞrmed wherever possible by allowed to acclimate to the wind tunnel room condi- comparison of retention times and mass spectrum of tions (25 ⫾ 1⬚C, 60 ⫾ 5% RH) for at least 1 h before synthetic standards. Where pure standards were not being observed. In the nonchoice tests, a cotton wick available (Sigma-Aldrich, Toluca, Mexico), identiÞca- loaded with a gram equivalent of the tested extract or tion was based on comparison with spectral data from 1 l of the selected compound was placed in the center the computer library (NIST 2002). The relative per- of the wind tunnel, 10 cm from the upwind end. For centage of the components was calculated from the two-choice experiments, fruit to be compared were sum of areas of all recorded peaks.
578 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 3 Fig. 1. Mean ⫾ SE response of hovering (a) and landing (b) of D. longicaudata females on hexanic and methanolic extracts of healthy (HM), mechanically damaged (MDM), and infested mango (IM) fruit evaluated in a wind tunnel. Bars in each graph followed by the same letter indicate no signiÞcant differences in response at the 5% level according to Tukey test. Statistical Analysis. Behavioral (cage bioassays and Response of D. longicaudata to Fruit Odor and nonchoice tests in the wind tunnel) and EAG data Extracts in the Wind Tunnel. Diachasmimorpha lon- were analyzed with a one-way analysis of variance gicaudata females landed signiÞcantly more often on (ANOVA). In some cases, before ANOVA, data were the odor of infested mangoes over odor of healthy 公x transformed to stabilize the variance, and means mangoes (2 ⫽ 7.84; df ⫽ 1; P ⬍ 0.001) and on the odor were separated by the Tukey test. A 2 test was used of mechanically damaged mango over odor of healthy to analyze behavioral data in two-choice tests. A sig- fruit (2 ⫽ 18.08; df ⫽ 1; P ⬍ 0.001) in two-choice tests. niÞcance level of 0.05 was used for all statistical tests. In contrast, females landed equally on odors of in- Data were analyzed using Jandel Sigma Stat (version fested and mechanically damaged mangoes (2 ⫽ 1.68; 2.0, Chicago, IL) and Statistico (Kernel release 5.5 A; df ⫽ 1; P ⬎ 0.05). Stat Soft, Tulsa, OK). The responses of females to methanolic and hexanic extracts of uninfested, infested, and mechanically damaged mangoes are shown in Fig. 1. Females did not Results show any apparent response when hexane and meth- Response of D. longicaudata to Fruit and Extracts in anol was offered in the wind tunnel. Females ßew Cages. D. longicaudata females signiÞcantly preferred upwind more frequently to hexanic extracts of in- to visit infested mangoes over healthy and mechani- fested mango compared with healthy mango extracts cally damaged mangoes (F ⫽ 36.50; df ⫽ 2,18; P ⬍ (F ⫽ 5.08; df ⫽ 2,12; P ⫽ 0.025). There were no 0.001). Females did not show any preference for signiÞcant differences among females that ßew up- healthy and mechanically damaged fruit. Female para- wind to hexanic extracts of infested mango and me- sitoids signiÞcantly preferred to visit methanolic ex- chanically damaged fruit. However, signiÞcantly more tracts of infested mangoes over methanolic extracts of females landed on infested mango extracts than on healthy and mechanically damaged mangoes (F ⫽ extracts of healthy and mechanically damaged fruit 26.76; df ⫽ 2,18; P ⬍ 0.001). No female preference for (F ⫽ 5.18; df ⫽ 2,12; P ⫽ 0.024). With respect to the methanolic extracts of healthy over mechanically methanolic extracts, signiÞcantly more females ßew damaged mangoes was observed. Hexanic extracts of upwind (F ⫽ 6.24; df ⫽ 2,12: P ⫽ 0.014) and landed the three types of fruit did not elicit any apparent (F ⫽ 5.56; df ⫽ 2,12; P ⫽ 0.020) on infested mangoes response in the females. than on healthy and mechanically damaged fruit.
June 2005 CARRASCO ET AL.: D. longicaudata RESPONSE TO MANGO FRUIT VOLATILES 579 Fig. 2. Mean ⫾ SE EAG response (mV) of female D. longicaudata to hexanic (a) and methanolic (b) extracts of healthy (HM), mechanically damaged (MDM), and infested mango (IM) fruit. Hex, hexane; met, methanol. Bars in each graph followed by the same letter indicate no signiÞcant differences in response at the 5% level according to Tukey test. EAG Female Response to Fruit Extracts. Hexanic be exclusively present in infested mangoes. Also, there extract of infested mangoes elicited a signiÞcant EAG were quantitative differences of the components response in female antennae compared with solvent among treatments. Infested mango extracts contain controls (F ⫽ 3.93; df ⫽ 3,72; P ⫽ 0.012). However, several compounds in higher amounts compared with there were no signiÞcant differences between the the other two types of mangoes. The methanolic ex- EAG response elicited by this extract and the re- tract chromatogram (Fig. 3b) shows a different chem- sponses elicited by healthy and mechanically damaged ical composition compared with that of the hexanic mango extracts (Fig. 2a). Methanolic extract of in- extract. The compounds present in the methanolic fested mangoes elicited a signiÞcant EAG response in extracts have not been identiÞed yet, but most of them female antennae in comparison with the responses seem to be carboxylic acid derivatives. Similar to the elicited by solvent, healthy, and mechanically dam- infested mango hexanic extracts, some compounds aged mango extracts (F ⫽ 8.52; df ⫽ 3,48; P ⫽ 0.001). seem to be in higher amounts in the methanolic ex- The EAG response elicited by mechanically damaged tracts of infested mangoes than in healthy and me- mango extracts was signiÞcantly different to that of the chanically damaged fruit extracts. solvent, but it was similar to that elicited by healthy Response of D. longicaudata Females to Selected mango extract (Fig. 2b). Mango Volatiles. The responses of female parasitoids Chemical Analysis. Representative chromatograms to selected synthetic compounds are shown in Fig. 4. of the infested mango hexanic and methanolic extracts Females ßew upwind to cotton wick loaded with are shown in Fig. 3. The compounds identiÞed in 3-carene, caryophyllene, cis-ocimene, ␣-humulene, hexanic extracts are listed in Table 1 with respective ␣-pinene, limonene oxide, ethyl octanoate, and a 10- relative amounts. They correspond to a mixture component blend. There were no differences among mainly of terpene and ester compounds; the major these compounds, including the 10-component blend component was 3-carene (Fig. 3a). Most of the com- (F ⫽ 1.58; df ⫽ 7,23; P ⫽ 0.21). Landing was elicited pounds found in infested mangoes were commonly by 3-carene, cis-ocimene, caryophyllene, ␣-pinene, found in healthy and mechanically damaged mango and ethyl octanoate, but no signiÞcant differences extracts, except 2-phenylethyl acetate, which seems to were found among them (F ⫽ 0.30; df ⫽ 4,14; P ⫽ 0.87).
580 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 3 Fig. 3. Representative chromatograms of hexanic (a) and methanolic (b) extracts from infested mangoes. Number on each peak refers to compounds listed in Table 1. However, the responses, particularly landing, were seems to be of clear importance in orienting the low and did not elicit the level of olfactory response searching behavior of this parasitoid, at least at short that fruit and extracts evoke. distances. In this sense, several authors (Knipling 1992, Vet and Dicke 1992, Godfray 1994, van Alphen and Jervis 1996) stated that any product from the herbi- Discussion vore (e.g., feces, cuticle, pheromones, accessory Results obtained from Þeld cages and wind tunnel glands) could be a signal for their enemies, and that bioassays showed that D. longicaudata females are parasitoids should respond to the stimulus most attracted to mango fruit, independently of whether closely associated with the host (Lewis et al. 1990). fruit are healthy, mechanically damaged, or infested. Godfray (1994) pointed out that parasitoids fre- However, wasps signiÞcantly preferred infested fruit quently orient toward cues that are derived from the and their methanolic and hexanic extracts. This sug- activity of the host, although not actually from the host gests that the presence of the larva inside the fruit itself. Table 1. Percentage composition of the compounds found in healthy (HM), mechanically damaged (MDM), and infested mango (IM) hexanic extracts Mean proportion (range) Peak Compound HM (n ⫽ 7) MDM (n ⫽ 5) IM (n ⫽ 9) 1a ␣-Pinene 6.2 (0.0Ð19.5) 9.9 (0.6Ð18.2) 2.8 (0.7Ð5.4) 2a Myrcene T T 0.1 (0.0Ð0.3) 3a ␤ Pinene 0.13 (0.0Ð0.9) 0.2 (0.0Ð0.7) 1.4 (0.0Ð4.9) 4a Ethyl hexanoate T T 0.2 (0.0Ð1.3) 5a 3-Carene 36.7 (3.6Ð64.3) 37.9 (15.4Ð59.2) 51.0 (28.4Ð82.2) 6a Limonene 0.2 (0.0Ð0.81) 0.2 (0.0Ð0.81) 1.4 (0.0Ð3.6) 7a cis-Ocimene 0.1 (0.0Ð0.62) 0.3 (0.0Ð0.78) 0.7 (0.0Ð1.8) 8 Isopentyl isobutyrate T ND 0.6 (0.0Ð2.8) 9a Terpinolene ⬍0.1 0.7 (0.0Ð3.8) 2.0 (0.0Ð5.9) 10a Limonene oxide 11.4 (0.0Ð48.3) 24.2 (0.0Ð54.9) 2.1 (0.0Ð9.0) 11a Ethyl octanoate 5.8 (0.0Ð20.6) 1.9 (0Ð4.4) 6.6 (0.0Ð34.2) 12 2-Phenylethyl acetate ND ND 0.5 (0.0Ð3.4) 13 Phenylethyl acetate ⬍0.1 ND 5.5 (0.0Ð23.6) 14 ␤-Gurjunene ND T 0.3 (0.0Ð1.5) 15a ␤-Caryophyllene 1.0 (0.0Ð2.1) 0.3 (0.0Ð1.3) 0.8 (0.0Ð1.7) 16a ␣-Humelene 5.5 (0.0Ð18.6) 1.5 (0.0Ð2.6) 2.9 (0.0Ð4.9) 17 ␣-Gurjunene ND 0.14 (0.0Ð0.45) 2.2 (0.0Ð11.8) 18 ␤ ÐCubebene 1.5 (0.0Ð3.2) 0.3 (0.0Ð1.3) 1.4 (0.0Ð2.4) 19 ␥-Gurjunene 7.1 (0.0Ð21.0) 3.9 (0.0Ð7.1) 1.4 (0.0Ð2.5) a Compounds conÞrmed with standard retention times. ND, not detected; T, traces.
June 2005 CARRASCO ET AL.: D. longicaudata RESPONSE TO MANGO FRUIT VOLATILES 581 Fig. 4. Mean ⫾ SE response of D. longicaudata females to synthetic compounds found in mango extracts tested in a wind tunnel. Bars within each activity followed by the same letter indicate no signiÞcant differences in response at the 5% level according to Tukey test. Similar results to those found in this study were fested fruit. The presence of acetaldehyde, ethanol, reported by Cheng et al. (1992) and Eben et al. (2000). and acetic acid in the extracts cannot be ruled out For example, Eben et al. (2000) found that D. longi- because they may have been hidden by the solvent caudata females visited more guava, grapefruit, and peak in the chemical analysis. The above quantitative mango fruit infested with A. ludens larvae than healthy differences may explain why infested mangoes and ones. In contrast, Greany et al. (1977) reported that D. their respective extracts elicited more landing re- longicaudata females were equally attracted to me- sponses than fruit and extracts from healthy and me- chanically damaged peaches and peaches infested chanically damage mangoes. with A. suspensa (Loew) larvae, and healthy peaches The fact that females were also attracted to healthy were not attractive at all. fruit (e.g., Eben et al. 2000) suggests that some vola- Our chemical analysis showed that there are some tiles are common in both types of fruit. Some of the qualitative and quantitative differences among fruit compounds identiÞed from mango volatiles are also extracts. 2-Phenylethyl acetate seems to be exclusively commonly found in many fruit, such as citrus present in hexanic extracts of infested mangoes, and (Takeoka et al. 1988, Kekelidze et al. 1989), guava some other compounds (i.e., 3-carene, limonene, ter- (Ekundayo and Ajani 1991), coffee (Mathieu et al. pinolene, ␣-gurjenene) show a higher concentration 1998), and apricots (Takeoka et al. 1990, Chassagne in infested mangoes. Although 2-phenylethyl acetate and Crouzet 1995). Thus, a generalist parasitoid like D. has been reported to be several fresh fruit and ßowers longicaudata could use these compounds, in combi- (Honda et al. 1998, Jordan et al. 2003, Pino et al. 2003), nation with fermentation compounds, as cues for host it also can be produced by microorganisms such as habitat location. For host location, females can use yeast, which may have the ability to ferment carbo- short-range volatile compounds derived from the me- hydrates to produce the volatiles (Nout and Bartelt dium and/or excretion of the feeding larvae (Law- 1998). The chemical analysis also revealed that com- rence 1981, Duan and Messing 2000) and sound or pounds occurring in the methanolic extracts are dif- vibration produced by host larvae feeding or crawling ferent to those present in the hexanic extracts and that inside the fruit. there are quantitative differences among methanolic We found that D. longicaudata females exhibit a extracts of healthy, mechanically damaged, and in- lower response to mango extracts than to mango fruit
582 ENVIRONMENTAL ENTOMOLOGY Vol. 34, no. 3 odor. A possible explanation for this low female re- Ekundayo, O., and F. Ajani. 1991. Volatile constituents of sponse to extracts is that all compounds needed for Psidium guajava L. (guava) fruits. Flav. Fragr. J. 6: 233Ð female attraction have not been extracted with the 236. method used or that some compounds were missing Godfray, H.C.J. 1994. Parasitoids. Behavioral and evolution- during the extraction process. Also, the fact that the ary ecology. Princeton University Press, Princeton, NJ. Greany, P. D., J. H. Tumlinson, D. L. Chambers, and G. M. behavioral activity of compounds evaluated (e.g., Boush. 1977. Chemical mediated host Þnding by Bios- some terpenes such as ␣-pinene, ethyl octanoate, or its teres (Opius) longicaudatus, a parasitoid of tephritid fruit blend) was not comparable with that elicited by ex- ßy larvae. J. Chem. Ecol. 3: 189 Ð195. tracts or fruit that may be caused by some other com- Honda, K., H. Omura, and N. Hayashi. 1998. IdentiÞcation pounds identiÞed in the extracts but not evaluated of ßoral volatiles from Ligustrum japonicum that stimulate may be important in eliciting attraction by themselves ßower-visiting by cabbage butterßy, Pieris rapae. J. Chem. or functioning as synergist of a blend. The behavioral Ecol. 24: 2167Ð2180. evaluation of all compounds and their possible mix- Jang, E. B., R. H. Messing, and L. A. Carvalho. 2000. Flight tures is a time-demanding task, but the fact that ex- tunnel responses of Diachasmimorpha longicaudata (Ash- tracts elicited antennal responses opens the possibility mead) (Hymenoptera: Braconidae) to olfactory and vi- sual stimuli. J. Insect Behav. 13: 525Ð538. of analyzing fruit volatiles with coupled electrophysi- Jordan, M., C. Margaria, P. Phillip, and K. Goodner. 2003. ologyÐ gas chromatography and facilitating the iden- Volatile components and aroma active compounds in tiÞcation of behavioral active compounds. aqueous essence and fresh pink guava fruit puree In conclusion, results of this study extend our un- (Paidium guajava L.) by Gc/ms and multidimensional derstanding of the host location behavior of D. longi- Gc-Gc/o. J. Agric. Food Chem. 51: 1421Ð1426. caudata. First, these results showed that females prefer Kekelidze, N. A., E. P. Lomidze, and M. I. Janikashvili. 1989. infested fruit and their extracts over healthy and me- Analysis of terpene variation in leaves and fruits of Citrus chanically damaged mango fruit, which conÞrms pre- unshiu Marc. during ontogenesis. Flav. Fragr. J. 4: 37Ð 42. vious studies with this species. Second, this study in- Knipling, E. F. 1992. Principles of insect. Parasitism anal- dicates that other compounds (e.g., terpenes), in ysed from new perspectives. Agriculture handbook 693, ARS-USDA, Washington, D.C. addition to the previously reported compounds by Lawrence, P. O. 1981. Host vibration a cue to host location Greany et al. (1977), may also mediate female orien- by parasite, Biosteres longicaudatus. Oecologia (Berl.). 48: tation toward infested fruit. The latter suggests that 249 Ð251. this species uses a complex mixture of compounds for Lewis, W. J., L.E.M. Vet, J. H. Tumlinson, J. C. Van Lenteren, host location. and R. P. Papaj. 1990. Variations in parasitoid foraging behavior: essential elements of a sound biological control theory. Environ. Entomol. 19: 41Ð 48. Acknowledgments Malo, E. A., N. Medina-Hernandez, A. Virgen, L. Cruz- López, and J. C. Rojas. 2002. Electroantennogram and We thank E. Malo for advice in EAG analysis, J. Valle-Mora Þeld responses of Spodoptera frugiperda males (Lepidop- for advice in statistical analysis, and A. del Mazo and A. tera: Noctuidae) to plant volatiles and sex pheromone. 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