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Species-Specific Close-Range Sexual Communication Systems Prevent Biological Control 39 (2006) 225–231 www.elsevier.com/locate/ybcon Species-speciWc close-range sexual communication systems prevent cross-attraction in three species of Glyptapanteles parasitic wasps (Hymenoptera: Braconidae) Adela Danci a, Paul W. Schaefer b, Axel Schopf c, Gerhard Gries a,¤ a Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6 b United States Department of Agriculture, Agricultural Research Service, BeneWcial Insects Introduction Research Laboratory, Newark, DE 19713, USA c Institute of Forest Entomology, Forest Pathology and Forest Protection, BOKU—University of Natural Resources and Applied Life Sciences, A-1190 Vienna, Austria Received 21 February 2006; accepted 21 July 2006 Available online 2 August 2006 Abstract The braconid parasitoids Glyptapanteles indiensis (Marsh) and G. liparidis (Bouché) occur in sympatry and allopatry, respectively, with their congener G. Xavicoxis (Marsh). We tested the hypothesis that all three parasitoids, but particularly sympatric G. indiensis and G. Xavicoxis, use species-speciWc sex pheromone blends for close-range sexual communication. In coupled gas chromatographic–electro- antennographic detection (GC–EAD) analyses of body extracts of conspeciWc females, male G. indiensis antennae responded to Wve com- ponents, one of which is speciWc to G. indiensis, and four are in common with G. Xavicoxis. Male G. liparidis antennae responded to six components, two of which are speciWc to G. liparidis, and four are in common with G. Xavicoxis. In Y-tube olfactometer experiments, body extracts of females elicited close-range attraction and wing-fanning responses only by conspeciWc but not by heterospeciWc males, supporting the hypothesis of close-range species-speciWc sex pheromone blends. © 2006 Elsevier Inc. All rights reserved. Keywords: Glyptapanteles Xavicoxis; Glyptapanteles indiensis; Glyptapanteles liparidis; Lymantria dispar; Hymenoptera; Braconidae; Parasitoid; Species- speciWcity; Pheromone; Close-range pheromonal communication 1. Introduction hymeria intermedia (Nees) and B. lasus (Walker) (Hyme- noptera: Chalcididae) exhibit courtship behavior when Sexual communication in parasitoids is mediated mainly exposed to pheromone extract of conspeciWc but not heter- by pheromones that are emitted by females and induce ospeciWc females, suggesting that they use species-speciWc searching, courtship, and mating behavior by males sex pheromones (Mohamed and Coppel, 1987). Intrigu- (Quicke, 1997). ingly, male Melittobia digitata (Dahms) (Hymenoptera: SpeciWcity of the pheromone blend might serve as a Eulophidae) emit sex pheromone that attracts conspeciWc reproductive isolating mechanism. Male sawXy parasitoids females, but also cross-attracts female M. femorata Syndipnus gaspesianus (Provancher) (Hymenoptera: Ich- (Dahms) and M. australica (Girault), suggesting that all neumonidae) are not attracted to sympatric heterospeciWc three species use similar if not identical long-range phero- female S. rubiginosus (Walley) or their pheromone (Z)-9- mones. However, following antennal contact of prospective hexadecenoate (Eller et al., 1984). Similarly, males of Brac- mates, heterospeciWcs are rejected, likely due to species-spe- ciWc contact pheromones (Cônsoli et al., 2002). Bioacoustic signals constitute alternative reproductive * Corresponding author. Fax: +1 604 291 3496. isolating mechanisms. Both Diachasmimorpha longicaudata E-mail address: [email protected] (G. Gries). (Ashmead) and D. kraussii (Fullaway) (Hymenoptera: Bra- 1049-9644/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2006.07.009 226 A. Danci et al. / Biological Control 39 (2006) 225–231 conidae) use pheromonal, visual and bioacoustic signals. (18 £ 18 £ 12 cm) contained 10–15 mated female parasit- Males are attracted to the females’ cuticular pheromone, oids, Wve L. dispar larvae (3–4 instar) (Fuester et al., 1987), and respond with wing vibrational bioacoustic signals and larval diet (Bell et al., 1981). After 1–2 days, parasitized which, in turn, increase the females’ activity. The females’ host larvae were removed and placed on a diet in plastic cuticular chemicals are similar across species, but acoustic cups (192 ml) with tight-Wtting paper lids (Sweetheart Plas- signals of males appear to be species-speciWc (Rungrojwa- tics, Wilmington, Massachusetts). Every second day, larval nich and Walter, 2000). frass was removed, and the diet replenished if needed. The Sympatric Glyptapanteles Xavicoxis and G. indiensis parasitoid cocoons to be used for mass rearing were placed (Hymenoptera: Braconidae) are gregarious and solitary in plastic Petri dishes (14 cm diam.) and food-provisioned parasitoids, respectively, of larval Indian gypsy moth, as described above. Lymantria obfuscata (L.) (Lepidoptera: Lymantriidae), Cocoons of G. indiensis and G. liparidis were provided by which occurs in the northern parts of India, Pakistan and the BeneWcial Insects Introduction Research Laboratory Afghanistan. Allopatric G. liparidis is a gregarious endo- (see above), and the Institute of Forest Entomology, Forest parasitoid attacking mainly 2nd and 3rd instars of the Pathology and Forest Protection, BOKU—University of gypsy moth, Lymantria dispar (L.), and alternate host spe- Natural Resources and Applied Life Sciences, Vienna, Aus- cies of the lepidopteran families Lymantriidae and Lasio- tria. Parasitoid cocoons with insects to be used in bioassays campidae for further generations during the season and as were transferred individually to capped plastic cups (30 ml) hibernating hosts. It occurs in Japan, Korea, the Kurile provisioned with sugar water-soaked cotton wicks. Rearing Islands, Russia, North Africa, and Europe (Marsh, 1979). took place under a 16L:8D photoregime at 22–25 °C and Sexual communication in G. Xavicoxis is mediated, in 50–70% RH. part, by a four-component close-range pheromone (Danci et al., 2006). Females press their abdominal tip to the 2.2. Acquisition of pheromone extracts substrate depositing pheromone in the process. These “deposits,” or body extract of females, provoke substrate- Groups of 1- to 3-day-old female G. Xavicoxis, G. indien- antennation, wing-fanning and close-range anemotactic sis, and G. liparidis were macerated in three separate hex- attraction responses by conspeciWc males. Pheromonal ane-containing vials (ca. 10 l per female) placed on dry ice. communications in G. liparidis and G. indiensis may be After extracts were kept at room temperature for »15 min, similarly complex but have not yet been investigated. the supernatant was withdrawn, Wltered through glass wool Congeners in the Lepidoptera often share pheromone in a pipette, and quantiWed to determine the volume repre- components. Allopatric congeners may use the very same senting one female body extract equivalent (FBE). pheromone (Gries et al., 2002b), whereas sympatric con- geners typically employ one or more additional phero- 2.3. Acquisition of volatiles mone components to maintain reproductive isolation (Gries et al., 1996). Similarly, the tortricid moths Archips Body extract of female G. Xavicoxis elicited strong close- argyrospilus (Walker) and A. mortuanus (Kearfoot) share range behavioural responses by conspeciWc males, with pheromone components in species-speciWc ratios (Cardé headspace volatiles not signiWcantly contributing to the et al., 1977a). attractiveness of the stimulus (Danci et al., 2006). Nonethe- Our objective was to test the hypothesis that G. Xavic- less, to generate experimental evidence for close-range oxis, G. indiensis, and G. liparidis use species-speciWc com- pheromonal communication in congeneric G. indiensis and ponents to confer speciWcity to their close-range sexual G. liparidis, we decided to bioassay Wrst the strongest possi- communication systems. ble stimulus, a combination of body extracts and headspace volatiles. 2. Materials and methods To acquire headspace volatiles, unmated 1- to 2-day-old female G. indiensis and G. liparidis were placed into vertical 2.1. Experimental insects cylindrical Pyrex glass chambers (10 ID £ 6 cm), and were provisioned with a sugar water-soaked cotton wick. Con- Glyptapanteles Xavicoxis and its host L. dispar were trol chambers contained the same food source, but no para- reared in the Global Forest Quarantine Facility at Simon sitoids. A water aspirator drew humidiWed, charcoal-Wltered Fraser University (SFU), and populations were repeatedly air at a rate of 1.5–2 L/min for two days through the cham- augmented with specimens obtained from the BeneWcial ber and a glass column (14 £ 1.3 cm OD) Wlled with 150 mg Insects Introduction Research Laboratory, United States of Porapak Q (50–80 mesh, Waters Associates Inc., Mil- Department of Agriculture, Agricultural Research Service, ford, Massachusetts, USA). Volatiles were eluted from Newark, Delaware. To facilitate mating in G. Xavicoxis, 10 Porapak Q volatile traps with re-distilled pentane (2 ml). females and 30 males were placed in plastic mesh cages The extracts were concentrated under a stream of nitrogen (10 £ 10 £ 6cm) (Hu et al., 1986), and provisioned with cot- such that 10 l of extract contained one female hour equiv- ton wicks (1 £ 10 cm; Richmond Dental, Charlotte, North alent (FHE) of volatile acquisition ( D amount of volatiles Carolina) soaked in sugar water solution. Oviposition cages released by 1 female during 1 h). A. Danci et al. / Biological Control 39 (2006) 225–231 227 2.4. Y-tube olfactometer bioassays (J&W ScientiWc,
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