The Chemical Ecology of Cecidomyiid Midges (Diptera: Cecidomyiidae)

J Chem Ecol (2012) 38:2–22 DOI 10.1007/s10886-011-0053-y REVIEW ARTICLE The Chemical Ecology of Cecidomyiid Midges (Diptera: Cecidomyiidae) David R. Hall & Lakmali Amarawardana & Jerry V. Cross & Wittko Francke & Tina Boddum & Ylva Hillbur Received: 30 May 2011 /Revised: 21 November 2011 /Accepted: 11 December 2011 /Published online: 4 January 2012 # Springer Science+Business Media, LLC 2011 Abstract The family of cecidomyiid midges (Diptera: Key Words Cecidomyiidae . Diptera . Pheromone . Cecidomyiidae) exhibits diversified patterns of life history, Semiochemical . Synthesis . Biosynthesis . Olfaction . behavior, host range, population dynamics and other ecolog- Monitoring . Traps . Control ical traits. Those that feed on plants include many important agricultural pests; most cultivated plants are attacked by at least one midge species. Several features of the reproductive Introduction biology of cecidomyiid midges point to an important role for chemical communication, with this topic last reviewed com- The family of cecidomyiid midges (Diptera: Cecidomyiidae) prehensively 12 years ago. Here, we review progress on exhibits diverse patterns in life history, behavior, host range, identification of sex pheromones, chemicals involved in loca- population dynamics and other ecological traits (Yukawa and tion of host plants, the neurophysiology of reception of volatile Rohfritsch, 2005). There are more than 5,000 species chemicals, and application of semiochemicals to management described, although this is probably a “small fraction of the of pest species of cecidomyiid midges that has occurred during number that must exist” (Gagné, 1989). Their diverse feeding the last decade. We hope this review will stimulate and sustain habits include zoophagy, mycetophagy, as well as phytophagy further research in these fields. (Mamaev and Krivosheina, 1965). Those that feed on plants include many important agricultural pests, with most cultivated plants attacked by at least one midge species. As a result, most research has focused on phytophagous species, often referred Dedicated to the late Professor C.-H. Zhao. : to as gall midges, e.g., in the review of Harris and Foster D. R. Hall (*) L. Amarawardana (1999). However, in that not all cecidomyiid midges are Natural Resources Institute, University of Greenwich, phytophagous, and not all phytophagous midges form galls, Chatham Maritime, Kent ME4 4TB, UK this review will use the taxonomic definition. It is anticipated e-mail: [email protected] that the generalized conclusions will apply to the taxonomic family rather than to the behavioral groupings. J. V. Cross East Malling Research, New Road, East Malling, The Role of Chemical Communication in the Biology Kent ME19 6BJ, UK of Cecidomyiid Midges W. Francke The chemical ecology of cecidomyiid midges was last Institute of Organic Chemistry, University of Hamburg, Martin-Luther-King Platz 6, reviewed comprehensively by Harris and Foster (1999), 20146 Hamburg, Germany although Wicker-Thomas (2007) included a summary of : more recent work on the sex pheromones of Cecidomyiidae T. Boddum Y. Hillbur in her review of pheromonal communication in courtship Department of Plant Protection Biology, Swedish University of Agricultural Sciences, behavior of Diptera. As noted by these authors, several S-230 53 Alnarp, Sweden features of the reproductive biology of these midges point J Chem Ecol (2012) 38:2–22 3 to an important role for chemical communication, espe- Sex Pheromones of Cecidomyiidae cially as all exhibit sexual reproduction (Gagné, 1994). In general, adults are very small, with body and wing Demonstration of Presence of Sex Pheromones lengths <3 mm and body weight <2 mg (e.g., Bergh et al., 1990), and are weak fliers. The life span of adults is The presence of female-produced sex pheromones, using very short, sometimes only 1–2 days. Adult males laboratory bioassays and/or field experiments with live virgin emerge, take flight, find, and copulate with females. females or female extracts as baits, has been demonstrated in Females emerge with a full complement of mature eggs, 10 species of cecidomyiid midge: Douglas-fir cone gall generally mate once, and then search for host plants on midge, Contarinia oregonensis (Miller and Borden, 1984), which to oviposit (Gagné, 1989, 1994). Hessian fly, M. destructor (McKay and Hatchett, 1984), These features require efficient mechanisms for finding pea midge, C. pisi (Wall et al., 1985), pine gall midge, mates, such as the use of sex pheromones. Similarly, effec- Thecodiplosis japonensis (Lee and Lee, 1985), rice gall tive means of locating host plants are required. Cecidomyiid midge, Orseolia oryzae (C.-H. Zhao, pers. comm., 1982; Sain midges are generally monophagous or oligophagous and, and Kalode, 1985), blackcurrant leaf midge, Dasineura tetensi even in the latter, larval development is restricted to two or (Garthwaite et al., 1986), brassica pod midge, D. brassicae more plant species within a single genus or to species in (Williams and Martin, 1986), sorghum midge, Stenodiplosis different genera within a family. Polyphagous midges with a (Contarinia) sorghicola (Sharma and Vidyasagar, 1992), host range extending beyond one plant family are rela- orange blossom wheat midge, Sitodiplosis mosellana (Pivnick, tively rare, and several of these species in fact alternate 1993), and apple leaf midge, D. mali (Harris et al., 1996;Heath between specific hosts at different times of the year et al., 1998, 2005). (Harris et al., 2003; Yukawa and Rohfritsch, 2005). The family Cecidomyiidae usually is divided into Host plant ecology is crucial for the growth and surviv- three sub-families: the Lestremiinae, Porricondylinae, al of larvae. Yukawa (2000) outlined the importance of and Cecidomyiinae (Gagné, 1989, 1994). Only species synchronization of the emergence of adults and the in the Cecidomyiinae have so far been shown to produce sex availability and suitability of hosts. Furthermore, neonate pheromones. The Cecidomyiinae is divided into two super- larvae are small and generally unable to move from tribes: the Lasiopteridi and the Cecidomyiidi. The genera one plant to another (Gagné, 1989). As a result of all Dasineura and Mayetiola are in the former, while Contarinia, these factors, the propagation of a species depends upon Thecodiplosis, Orseolia, and Sitodiplosis are in the latter. adult female midges finding a suitable host at the correct stage of development in a short space of time (Åhman, 1985;Harris Identification of Sex Pheromones and Rose, 1989). A further intriguing feature of the biology of cecido- Components of the female sex pheromones of 16 species of myiid midges is the structure of the antenna, the site of cecidomyiid midge have been identified and shown to receptors for volatile chemicals. In addition to sensilla attract conspecific males in laboratory and/or field bioassays typically found on antennae of other insects, both males (Table 1). Pheromones have been isolated by solvent extrac- and females have curious, looped sense organs known tion of whole insects or excised glands (Table 1, entries 1, 2, as circumfila (Slifer and Sekhon, 1971; Lee and Lee, 6, 8, 9, 10, 11, 12), or by air entrainment onto Porapak 1985; Solinas and Nuzzaci, 1987). (Table 1, entries 3, 4, 5, 6, 7, 13, 14, 15, 16). The latter At the time of the review by Harris and Foster (1999), the procedure allows for easier processing of large numbers structure of only one component of the pheromone of one of insects and concentration of the collection prior to species of cecidomyiid midge had been identified, that of gas chromatographic (GC) analysis without contaminat- the major component of the female-produced sex pher- ing the column with involatile material, although in omone of the Hessian fly, Mayetiola destructor (Foster some cases it may be difficult to get females to exhibit et al., 1991a).Thisdiscoveryheraldedasurgeiniden- normal calling behavior in the laboratory (Hillbur, tification of pheromone components of other midges unpublished). and their use in pest management. Here, we review Cecidomyiid midges generally produce pheromone in progress on identification of sex pheromones, chemicals very small amounts. For example, in C. oregonensis (Gries involved in location of host plants, the neurophysiology et al., 2002) and the aphidophagous gall midge, Aphidoletes of reception of volatile chemicals, and application of aphidimyza (Choi et al., 2004), pheromone in extracts was semiochemicals to management of pest species of cecido- undetectable by a mass spectrometer. Gland extracts of C. myiid midges that has occurred during the last decade. pisi contained a few picograms per female (Hillbur et al., We hope this review will stimulate and sustain further 1999). Similarly, air entrainment of pheromone of D. mali research in these fields. gaveapproximately20pgperfemale(CrossandHall, 4 J Chem Ecol (2012) 38:2–22 Table 1 Pheromone components of cecidomyiid midges Species Pheromone components Reference Monoester unsaturated 1 Hessian fly Foster et al. (1991a) Mayetiola destructor (2S,10E)-2-Acetoxy-10-tridecene Andersson et al., (2009a) (2S)-2-Acetoxytridecane (2S,10E)-2-Acetoxy-10-tridecene (2S,8Z,10E)-2-Acetoxy-8,10-tridecadiene (2S,8E,10E)-2-Acetoxy-8,10-tridecadiene (2S,10E)-10-Tridecen-2-ol 2 Douglas fir-cone gall Gries et al. (2002) midge Contarinia (2S,4Z,7Z)-2-Acetoxy-4,7-tridecadiene oregonensis 3 Chinese Liu et al. (2009) chrysanthemum midge (2S,8Z)-2-Butyroxy-8-heptadecene Rhopalomyia longicauda 4 Honey locust

Load more