Proceedmqe of the 7 th Internatwnal Wm'kmg Conference on Stored- product Protection - Volume 2

Chemical, visual and acoustic stimuli in the courtship of Pyralid infesting stored products

Pasquale Trematerra'

Abstract mfestmg stored products such as Ephestia cautella (Walk), Ephestui elutella (Hubner.) and Plodia Research on sexual behavior has focused pnmanly on female and male behavioral responses to them inierpunctella (Hubner) was reported by Mullen and Tsao (1971), whilst the heanng ability of Although several researches on moth sex pheromones have Ephestia kuehniella demonstrated that the complete sequence of courtship Z was reported by Perez and Zhantiev (1976). Trematerra behavior also mvolves male pheromones and other types of and Pavan (1994 and 1995) have reported ultrasomc commurucation, relatively little work has been done on the emission m the matmg behavior of E. cautella, E connection between pheromones and extrusible organs or kuehmella and P. mterpunctella. with sound production Many msects have airborne sound The courtship of these phyticme moths has received receptors, which function pnmarily m mtraspecific attention m the literature. several studies have been made communication, whilst mothers heanng serves to warm a on the male orientation to the produced by the potential threat from a predator. Certam pyrahd moths callmg female, whereas other reports have dealt more WIth mfestmg stored food, such as the Achroia qnsel!« F., behavior after the male has located the female (Traymer , Galleria meIIonella L, and Corcyra cephalonica 1968; Kennedy and Marsh, 1974; Barrer and HIll, 1977a, b (Stamt) (Gallenmae) and the Ephestia cautella and 1980) ( Walker), Ephestw kuehmiella Zeller and Plodw Research on moth courtship behavior has focused mterpunctella Hubner (PhYCltmae) have acquired the pnmanly on female pheromones and male behavioral additional ability to generate sounds by wmg-fannmg for responses to them. Although several studies on moth sex intraspecific commumcation and pair formmg pheromones have demonstrated that the complete sequence The courtship of these Pyrahdae has been of courtship behavior also mvolves male pheromones and exammed and several studies have been made on the male other types of commumcation, relatively little work has onentation to the pheromone produced by the callmg female been done on the connection between pheromones and and also on the behavior of the male after the female has extrusible organs or WIth sound production (BIrch and been located. Hefetz, 1987; Spangler, 1988; Ewing, 1989; Quarteyand Coaker, 1993; Mankm and Hagstrum, 1995; Trematerra, 1995 and 1997). EVIdence for the use of ears in sexual communication has been established for noctuid and pyrahd species (Spangler, 1984, 1987 and 1988; Spangler et al. , Introduction 1984; Gwynne and Edwards, 1986; Surlykke and Gogala, 1986; Trematerra and Pavan, 1994 and 1995) The gallerune wax moths Achroui gr'LSellaF and Galleria Pyrahd moths typically have tympamc heanng organs melkmeila L. and the nee moth Corcyra cephalonuxi located on the pleural-ventral surface of the first abdommal (Stamt. ), have acquired the additional ability to generate segment (Agee, 1969; Mullen and Tsao , 1971a, b; Coro and sounds by wmg fannmg for intraspecific commurucation and Fernandez, 1972; Coro, 1973) The organ consists of a thin parr formmg (Spangler et al , 1984; Spangler, 1985 and tympanum of varymg transparency tightly stretched over a 1987; Trematerra, 1992 and 1997). In these species the cavity The antenor part of the tympanum usually consIsts male sound producmg organ IS located m front of the of a thIcker, less flexIble, opaque, papIllate membrane tegulae, rounded plates that cover the forewmg msertlOns. referred to as the counter tympanum, whIch gIves the The 'timbales' are fmely corrugated m A. gr'LSellaand G tympanum a sort of U shape rnellonella, or bear a senes of stnations, as m C. cephalonica The heanng abIlIty of other pyralId moths Pyralid moths communication lDepartment SA V A ,Umverslty of Mohse, EdlflClOFacolta dl Smce many moths have ears, they seem to have been Agrana, 1-86100 Campobasso, Italy predated to develop mtraspecific commumcatIon systems 1446 Proceedings of the 7th International Worhng Conference on Stored-product Protection - Yolurne 2 that use sound srgnals to wluch ears are sensitive (Roeder associated air chambers A qriseilc; and C. cepnalonica and Treat, 1957; Kay, 1969). In addition, It has been are two examples m which males use sound to attract suggested that night-flying moths may use echolocation to females. The most thoroughly investigated example IS A aVOIdobstacles (Hinton, 1955; Kay, 1969) However, only gnsella (GreenfIeld and Coffelt, 1983; Spangler, 1984; recently intraspecific communication has been demonstrated Spangler et al , 1984). Males take positions around the food in three species of Gallenmae moths. It IS suspected m resource (honeybee combs) and call contmuously WIthabout several more pyrahd and noctuid moth species m which 80 pulses sec -1 of 100 kHz sound. An unmated female males produce vanous patterns of sound at frequencies responds by movmg directly toward the male or some times received by female ears (Dahm et al , 1971; Wakamura, by circhng as she moves toward the male. The female 1977; Greenfield and Coffelt, 1983; Spangler et al , 1984; approach may end near a male (1 - 2 em}: then the male Spangler, 1985 and 1987; Zagatti, 1985; Gwynne and begms circlmg until contact is made. WIth their ability to Edwards, 1986; Surlykke and Gogala, 1986; Trematerra detect pulse repetition rates, female moths are apparently and Pavan, 1994 and 1995). able to distmguish the sound of callmg males from the Male-male communication is also a possibility for any echolocation sounds of msectrvorous bats on the basis of the species that produce sound A. grisella males start repetition rate of the pulses alone (Spangler et al. , 1984) producmg sound when another sound producer IS nearby Prehmmary studies suggest that C cephaumica males (Spangler et al. , 1984); while producmg sound they CIrcle attract females With their nearly contmuous production of about and ram one another (Greenfield and Coffelt, 1983). pulse trams (Spangler, 1987; Trematerra, 1992). Unmated G mellonelui males produce sound only in groups, or C cephalomca females appear to respond identically when when commg close to or contacting one other (Spangler, subjected to either simulation of male C. cephalonica sound 1985) Acoustical calling by C cephalonico. males also or similar temporal patterns WIthcontmuous sound replacing seems to stnnulate other males to call when they are near a the pulse tram. ThIS evidence suggests that females of this food resource (Spangler, 1987; Trematerra, 1988 and species have the abihty for either evasive fhght or attraction 1992) In these cases, sound commumcatton may have to identical sound pulse sequences On the other hand, male ansen as an adaptation to crowdmg near food, where many sound may cause evasive flight m moths competmg WIth C. males compete for females ready to mate (Greenfield, 1971; cephalonica for the same food source, thus helping to Greenfield and Coffelt, 1983; Spangler et aI., 1984). defend It. G. melloneila exhibits a second distmct type of pair- Sound production and behavioral responses forming system m wluch sound only mitiates the process and The sound-producmg organs of male Galleninae moths are pheromone takes over to attract females to males (Spangler, located antenorly on the tegulae. The "tunbals ' may be 1984) Males produce sound only when they interact WIth finely corrugated, as m A. grisella and G me llone lla other msects, ordmanly other G Mellonella males, within (Spangler et al. , 1984; Spangler, 1985). The surface may an enclosure of the type used by cavity-nestmg honeybees also appear to be free of fme corrugatIons but may bear a ( Spangler, 1986) The male sound, short phrases of senes of stnatIons, as m C. cephalonica (ZagattI, 1985; ultrasomc pulses, causes unmated females to beat their Spangler, 1987; Trematerra, 1992), the bumblebee wax wings. Males, senSItIve to the low-frequency sound of the moth, Aphomia sociella L., and the sugar cane borer, wing-beatmg female, elevate theIr pheromone release in Eldana sacchanna (Walker) (ZagattI, 1985). response to It ThIS sudden mcrease m pheromone release Sound productIon has been studIed m gallerllne A may permIt females to fmd callmg males even in confmed grisella, G. 'mellO'twlla, and C cephalO't~1,ca and m enVIronments WIth high ambient pheromone (Spangler, PhycitInae E. cautella, E. kuehn1,ella and P 1984) Males restmg outside an enclosure release a interpunctella. In Gallerunae, With the downstroke of the contmuous concentratIon of pheromone, WhIChmay enable forewmgs, males of all three species push down on a females to locate mdIV1dualmales, thus elimmatmg the need bladelike structure (tegule-wmg coupler) (Spangler et al. , for ultrasomc signals. However, the wing beat of a flymg 1984), causmg a tWIstmg actIon at the base of the tImbale female may cause a nearby male to flutter hIS wmgs to ( Spangler, 1986; Spangler and TakessIan, 1983) Since mcrease pheromone release. these moths produce sound by controllmg Wing poSItion, The courtshIp sequence proved to be qUlte SImIlaramong they are able to do so whIle standmg, but not whIle flymg E. cautella, E. kuehniella and P. mterpunctella. (Spangler et aI., 1984) G. mel101'wlla can also remam Males start Wing fannmg and females search on perceIvmg sIlent wlule fluttering its Wings, whIch It apparently does to chemIcal stImulI, as reported by Barrer and HIll (l977a) m release a pheromone (Spangler, 1984, 1986 and 1987). E. cautella In these moths the male Wing fanning slows A gnsella elevates its tegulae whIle callmg, probably by progressively when the genitalIa come mto dIrect contact. the use of a tegular process, and perhaps also by the The male comes to rest face to face WIththe female and then 1447 Proceedmgs of the 7th Internatumal Working Conference on Stored-product Protection - Yolume 2 proceeds WIth the mitral stages of copulation. 1981) . Dunng the entire phase of wing-fanmng ultrasomc pulses Removal of antennae and labial palps, the probable SItes of were detected m the three species (Trematerra and Pavan, odour perceptors, reduced the response m C. cephalomca 1994 and 1995) The wmg-fannmg males emit trains of (Trematerra, 1992). Evaluation of the reproductive success ultrasomc pulses With a frequency range of up to 80 kHz. m males or females of E. cauiella., E. kuehmiella and P. The recordings appeared similar WIth the pulse clearly mierpunctella WIthout antennae showed a lower recogmzable. Males With the tegulae removed apparently reproductive success in males WIth their antennae removed showed no modification m their activity and courtship (Trematerra and Pavan, 1994) SImilar results were behavior but ultrasomc emissions were not detected. Tests observed m A. grisella (Dahm et al., 1971) and m C. aimed at the evaluation of possible modificatrons in the cephalonica (Trematerra, 1992). E cautella and E reproductive success in muted males and m deaf females kuehmiella females without antennae showed no drop in revealed a lower reproductive success in muted males and m reproductive success, whereas P. uiierpunctella females deaf females than in intact ones. ThIS ISprobably related to had a 22% drop the suppression of the acoustic SIgnals. SImilar behavior and It IS conceivable that the pheromone components ermtted results were obtained m C. cephalonnca (Trematerra, by female phycitid species do not adequately provide 1992). interspecific distinction to the male responders. ThIS drawback IS readily overcome by specie-specific pheromone Factor releasing the copulation blends which are discharged from the androconia (glandular scent scales and tufts) of courting males and WhIChare attempt in E. cautella, E. kuehniella perceived by conspecific females Females of E. cautella, and P. interpunctella E. elutella, E. figulilella and P. interpunctella were found to rapidly cover their gemtal opening and thus prevent Grant et al (1975), working With the courtship behavior mating when heterospecifrc males exposed their abdommal of E. cautella, E. kuehmiella and P. uiterpumciella hairpencils (Grant et al. , 1975; Phelan and Baker, 1986). reported that the courtship was made up of a complex Finally, It should be remmded that different behavioral sequence which started at the female callmg configurations and ermssion rates of pheromones, recipient Although they did not mention the role of the scales, the responsiveness and behavior patterns as well as different results obtained by Ono (1981) show that the recognition of circadian rhythms of calhng m various species are mainly the scales by a male must be added to the courtship sequence mvolved m the reproductive isolation among storage as the releasing factor for the gemtal thrust (the copulation species. attempt). Grant et al. (1975) reported that the males of these species always put their head under the female prior to Conclusions the genital thrust. Trematerra (1992) observed similar behavIor me. cephalomca. Thus, it has been suggested that Among moths that use heanng for matmg communicatlon, the antennae and labial palps of the male perceived the two speCIes of gallernne males produce mate-calhng sounds stimulus from the scales that females recogmze and onent toward. In other gallernne Factors releasing the copulation attempt of these pyralid species, the male calls m association wIth other males. were exammed usmg various kmds of models, includmg Females respond to the collectIve sound by beatmg theIr dried whole bodies, rolls of paper covered With scales, and wmgs, whIch stimulates the male to mcrease productlon of flat surface covered with wmgs, in the presence of the sex pheromone. Odour attracts the female. pheromone (Dno, 1981; Trematerra, 1992) StudIes on pyrahds (Gwynne and Edwards, 1986) mdlcate ConSIderingthese facts together, the stimulus provided by that more commumcatIOnsystems are present. The systems the scales seems to be a tactlle one in these moths as well as function at ranges of up to 1 - 2 meters, i. e only in the m Phthonmaea operculella (Zell.). As mentloned above, Immediate area of the compact food resource. However, the copulatlon attempt of phYCItIdmoths may be released by recent dlscovenes suggest that some moths commumcate the scales, whIch act as non-specific tactile stlmulus. Smce WIth acoustical SIgnals over much longer ranges. Thus, there is no remarkable preference to the geometric acoustical commumcatlon m moths may function m a varIety confIguration of the object, It IS suggested that the male of ways. The use of low frequency (about 40 Hz) sound of moths of phycltld cannot discnmmate the species of mate m the female Wingbeat m mating by the greater wax moth, G. the step of the copulation attempt. Actually, they attempt mellonella (Spangler, 1984 and 1987) suggests another type copulation with any object that IScovered WIththe scales. In of communication that could occur extenSIvely. other words, the factors of the scales do not play a role in A. grisella and C cephalon~ca are two examples m reproductive Isolation among three phycitId speCIes (Dno, which males use sound to attract females, while G 1448 Proceedinqe of the 7th Internatwnal Worhng Conference on Stored-product Protectwn - Volurne 2

mellonelui exlubits a second type of pair-forming system m Ono , T 1981 Factors Releasmg the Copulation Attempt m which sound only uutiates the process and then pheromones Three Species of Phycrtidae (Lepidoptera. Phycmdae ) take over to attract the female to the male (Spangler, Apphed Entomology and Zoology, 16, 24 - 28. 1988) . Perez, M., and Zhantiev, R D. 1976 Functional orgaruzation of the tympana organ of the flour moth References Epheetia kuehniella. Journal of Insect Physiology, 22, 1267 -1273. Barrer , P. M., and Hill, R. J, 1977. Some aspects of the Quartey, G. K., and Coaker, T H. 1993. Role of sex courtship behavior of Ephestu: cautella (Walk) pheromone components m the orientation behavior of ( Lepidoptera. Phyticidae ) Journal of the Austrahan Ephestia cauteZla. Entomology Expenmentahsm et Entomological Society, 16, 301 - 312. Applicant, 66, 237 - 245. Barrer, P. M., and HIll, R J 1980. Insect onented Spangler, H. G. 1986. Functional and temporal analysis of locomotion responses by unmated females of Ephestu: sound production m Galleria mellonella (Lepidoptera: cautella (Walker) (lepIdoptera: Phyucidae ) ). Journal of Comparative Physiology, A, 159, International Journal of Invertebrate Repnnts, 2, 59 -72. 751-756. Belton, P, 1962 Responses to sound in pyrahd moths. Spangler, H G. 1987 Ultrasomc Commumcation m Corcyra Nature, 196, 1188 -1189. cephalonica (Stamton) (Lepidoptera. Pyrahdae) Journal BIrch, M. C. , and Hefetz, A. 1987. Expressible organs in of Stored Products Research, 23, 203 - 211 male moths and their role m courtship behavior. Bulletm of Spangler, H G. 1988. Moth heanng , defense, and the Entomological Society of America, 33, 222 - 229. communication. Annual Review of Entomology, 33, 59- Ewmg, A. W., ed., 1989. bioacoustics. 81. Neurobiology and Behavior. Edmburgh, Edimburgh Spangler, H G., and Hippenmeyer , C. L. 1987. Bmaural Uruversity Press, 1- 260 Phonotaxis m the Lesser Wax Moth, Achroia gnsella (F ) Greenfield, M. D. , and Coffelt, J A 1983. Reproductive (Lepidoptera: Pyrahdae). Journal of Insect Behavior, 1, behavior of the lesser wax moth, Achroui grisella 117-122. (Pyralidae: Gallerunae ): signalmg , pair formation, male Trayner, R. M. M. 1968. Sex attraction in the mteractions, and mate guardmg Behavior , 84, 287- Mediterranean flour moth Anagastra kuhrnella: Iocation of 315 the female by the male. Canadian Entomology, 100, 5- Mankin, R W., and Hagstrum, D W 1995 Three- 10. dimensional Onentation of Male Cadra cautella Trematerra, P 1997. Some aspects of the sexual behavior (Lepidoptera. Pyrahdae ) Flying to Callmg Females m a of the Lepidoptera Pyralidae mfestmg stored-products. Wmdless Environment. Environmental Entomology, 24, Anz Schadlmgskunde, Pflanzenschutz, Umweltschutz, 1616 -1626. 70,87-91 MIller, L A. 1983 How detect and aVOId bats In: Trematerra, P., and Pavan, G. 1994 Role of ultrasound Huber, F., and Markl , H., ed , Neuropathology and production and chemical SIgnals in the courtship behavior of Behavioral Physiology. Berlm, Springer-Verlag, 250 - Ephestia cautella (Walker), Ephestia kuehniella Zeller 266. and Piodia mterpunctella (Hubner) (lepIdoptera Mullen, M A. and Tsao, C. H 1971a. Tympamc organ of Pyrahdae). In: HIghley, E., Wnght, E. J., Banks, H. Indian meal moth, Plodw l,nterpunctella (Hubner), J., and Champ, B. R , ed., Proceedmgs of the 6th almond moth, Cadra cautella (Walker) and tobacco International Workmg Conference of Stored- product moth, Ephestia elutella (Hubner) (LepIdoptera: ProtectIOn, Canberra, Austraha, Apnl 1994. 1, 591 - Pyrahdae). International Journal of Insect Morphology and 594 Embryology, 1, 3 -10. Trematerra, P and Pavan, G. 1995. Ultrasound production Mullen, M. A. and Tsao, C. H. 1971b. Morphology of the m the COurtshIp behaVIOr of Cadra cautella (Walk.), Tympamc organ of the greater wax, Garnellonella Ephestia kuehn iella Z. and Plodw mterpunctella nwthlleria. Journal of GeorgIa EntomologIcal SocIety, 6, (Hubner.) (lepIdoptera Pyrahdae). Journal of Stored 124 -132. Products Research, 31 (1), 43 - 48

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