Olfactory Male Sensitivity and Its Variation in Response to Fluoranalogs of the Main Pheromone Component of Female Mamestra brassicae A. A. Nikonov, T. V. Tyazhelova, Ye. A. Nesterov, V. M. Rastegayeva, F. E. Ilyasov, P. V. Mashkin and B. G. Kovalyov Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow Region, 142292, Russia Z. Naturforsch. 49c, 508-515 (1994); received September 14, 1993/March 14, 1994 Electroantennogramme, Chemical Communication. Fluoranalogs, Mamestra brassicae According to the EAG study and the field trapping tests, fluoranalogs of the main phero­ mone component of Mamestra brassicae females have been found to possess disguising properties for males when used together with the main pheromone component itself. In males, at low concentrations of the above substances the diminishing of attractivity of these blends correlates with the absence of EAG responses to them. An unequal action of these substances has been revealed in different concentration ranges of odours. The mechanisms of the action of these substances are under discussion.

Introduction primary mechanisms of olfactory reception, in­ At present, an intensive search for effective bio­ cluding principles and mechanisms of odour infor­ logical ways of protecting plants from pests mation recognition; (ii) the changes in sensitivity is going on. One of the promising directions of this and those of distinguishing the odours by search is the use of natural pheromones as well as in natural conditions are weakly studied. their analogs, because their use in traps and other In this work we have studied electrical responses preparations has a weak toxicity and results in dis­ of antennae of Mamestra brassicae males to the turbances of sex communication of insects. So, it main pheromone component (Zll-16:OAc) and becomes possible to regulate the number of pests its fluoranalogs, as well as the attractivity of the (Campion, 1984). above substances for Mamestra brassicae males. On the other hand, some substances are known Materials and Methods to suppress the attraction of males of certain insect In the laboratory experiments the males of species to sex pheromones or their synthesized Mamestra brassicae were used for the study. analogs, effectively. These substances may be of Butterflies were bred out of larvae in the diapause the natural origin. Their presence in pheromone at 25 °C and at humidity of 70%. Mamestra bras­ blend appears to be necessary in the course of sicae with developed and intact antennae were interspecies communication of insects (Bogda­ kept at 10 °C after emergence and used 3-5 days nova, 1980; Christensen, 1990). They can be also old. synthesized de novo (Albans, 1984). The search for As pheromone we used a synthesized analog of these substances and their synthesis are rather ex­ the main component (Bestmann, 1978). Haloace- pensive. Investigations in this direction are per­ tate analogs of Mamestra brassicae pheromone formed for a long time (Roelofs, 1968). Here the were synthesized in the laboratory headed by possibility of a specific disturbance of the sexual Boris Kovalyov (Kovalev et al., 1979) (Research chain in some insect species without any marked Institute of Biological Methods of Plants Protec­ change in chemocommunication of the others is tion, Kishenev) as follows: 1) 16-fluor, (Z)-ll- very attractive. Although this problem seems to be hexadecenal- 1 -iltrifluoracetate easy, it has not been satisfactorily solved yet. The main reasons for this are; (i) little evidence on the (F 16,Z 11-16:OCOF3); 2) 16-fluor, (Z)-ll-hexa- decenal-l-ilacetate (F16,Z11 -16:OAc); 3) (Z)-l 1-hexadecenal-1 -iltrifluoracetate

Reprint requests to Dr. A. A. Nikonov. (Z 11-16: OCOF 3 ).

0939-5075/94/0700-0508 $ 06.00 © 1994 Verlag der Zeitschrift für Naturforschung. All rights reserved. A. A. Nikonov et al. • Fluoranalogs of the Main Pheromone Component of Female Mamestra brassicae 509

For morphological investigations the antennae of butterflies caught was counted every 3-4 days

were cut and fixed in 1.5% solution of glutar alde­ during 2 0 days in the summer of the second gener­ hyde at 4 °C for 2 h. Then after dehydration they ation of Mamestra brassicae (Buchko, 1985). The were embedded into resin “Spur” (Tiras and results obtained were statistically processed and Moshkov, 1978). represented as tables and diagrammes. Electrophysiological measurements were per­ formed at the Institute of Cell Biophysics (Push- Results chino) by using a standard electrophysiological de­ Electrophysiological study vice. According to Schneider’s method (Schneider, 1984), EAG was recorded from the ends of the The use for stimulation of antenna led to ap­ cut-off antenna by capillary electrodes filled with pearance of Z 11-16: OAc negative potential oscil­ an analog of hemolymph solution (Kaissling, lations (Fig. 1 A), the amplitude and the shape of 1986). Odour was pushed into the continuous flux which depended on concentration and duration of of purified air (v = 0.5 1/min) by using the system the stimulus. The first stimulation of the antenna allowing to avoid mechanical artefacts, as it had ( 1 0 “ 1 0 |!g per filter) always evoked a response of been described earlier (Minor and Vasilyeva, a greater amplitude than the subsequent ones used 1979). The exit end of the glass tube (4 mm in at the same or stronger concentrations. The con­ centration area of 1 0 “9 - 1 0 - 7 ^ig per filter was diameter) was at a distance of 1 0 mm off the an­ tenna plane. Paper filter bands (1 cm2) with 10 ^il characterized by small and stable amplitudes. A of the substance diluted in hexane served as a statistically significant increase of the amplitude of source of stimulating vapours. In different experi­ responses (1.05 ± 0.05 mV) was observed at ments the excitement duration was changed from higher concentrations (10 - 6 (ig per filter). A 0.1 to 0.5 sec. The time between excitements was further enhancement of the odour concentration 1-2 min. The parameters of stimuli (sequence fre­ resulted in a periodic increase of the amplitude of quency and push duration) were changed auto­ responses (Fig. 1 B). This dependence was not of a matically. The potentials were recorded and the typical linear character. The curve acquired an S- results obtained were statistically processed shaped form, on which a plateau in the region of (Zacks, 1971) under automatic conditions by using several concentration ranges as well as some de­ an extra developed device and software pro­ crease of the amplitude of EAG responses could grammes based on PC “Iskra-226”. be seen within the range between 1 0 _3 - 1 0 _ 1 ^ig The field trapping experiments were perform­ per filter. ed in 1988-1989 in the fields near Kishenev. The traps were hung about at a height of

1 . 2 m around vineyards and a pea field, placed in a line by blocks (5 traps in each line). The experiment was carried out in two variants: (i) the study of attractivity of used substances No. 1 (F 16,Z 11-16 :O CO F3), No. 2 (F16,Z 11-16: OAc) and No. 3 (Zll-16:OCOF3) and analog of main pheromone component (Z 1 1-16: OAc); (ii) the study of attractivity of used different mixture of the above-mentioned substances. For this purpose two capsules, the one with substance under study, the other with pheromone, were placed into each trap. Sometimes the capsule with substance under log CONCENTRATION ( |ig per filter ) study was placed near the trap filled with phero­ Fig. 1. A. Standard EAG response of Mamestra brassicae mone. The traps with uncharged capsules served males had been recorded after analog-digital converter. as a control. The distances between the traps were B. Dose-response curve for the main pheromone compo­ nent Z 11-16: OAc and fluoranalog of main pheromone as follows: 15 m in the block, 30 m between the component F 16,Z 11-16: OCOF 3 tested on males (n = blocks, 200 m between the variants. The number 10). Mean response ± SEM. 510 A. A. Nikonov et al. • Fluoranalogs of the Main Pheromone Component of Female Mamestra brassicae

Using fluoranalog No. 1 for stimulation, we ob­ in the concentration ranges of 1 0 ~ - 1 0 ~ 4 (ig per served an EAG reaction of the antenna of Mame­ filter. In this case the amplitude increase within stra brassicae males similar to the reaction to the 10“3 -1 0 - 2 (.tg per filter observed (Fig. 3). It is main pheromone component. However, the con­ noteworthy that introduction of the main phero­ centration curve of the main component lay above mone component ( 1 0 ~ 7 (ig) into the continuous that of fluoranalog No. 1 (Fig. 1 B). In this case sig­ air flux blowing over the antenna resulted in the nificant differences between them ranged from same dependence of the amplitude of responses

IO- 7 to 1 0 ” 3 (tg per filter while the beginning and on the concentration of fluoranalog No. 1 (Fig. 3). the end of the curves did not coincide with each Fluoranalog No. 2 at concentrations of 10“9- other. The activity of fluoranalogs No. 2 and No. 3 1 0 ~ 5 (ig did not make the response to the main showed a different picture. Substance No. 2 caused pheromone component disappear completely, yet two statistically distinguishable amplitudes of re­ the amplitude was small and constant (Fig. 4). sponses, relatively small in size, within concen­ tration ranges of 1 0 ~lo- 1 0 - 5 (tg and 1 0 _4 - 1 0 - 1 (ig per filter (Fig. 2). Fluoranalog No. 3 had one con­ centration region ( 1 0 - 9 (tg) where the antenno- gramme amplitude drastically rose. A similar in­ crease of the amplitude of responses took place upon approach of stimuli concentration to this re­ gion from both lower and higher concentrational ranges. A further increase of the concentration of fluoranalog No. 3 did not lead to any changes in the amplitude of responses (the amplitude was constant) (Fig. 2). To study the mechanisms of the influence of the above substances on the insect receptor system, Fig. 3. Dose-response curves for main pheromone component at the background of fluoranalog 1 - the pheromone was investigated at the back­ F16,Zll-16:OCOF3 (FI + main comp.) and ground of the fluoranalogs. In this case some dif­ F16,Zll-16:OCOF3 at the background of a main phero­ ferences in action of the substances were mone component (main comp. + FI). Background sub­ stances have been introduced into the continuous air observed. flux blowing over the insect antenna. Tested 10 males. Introduction of fluoranalog No. 1 into the con­ Mean response ± SEM. tinuous air flux ( 1 0 _ 1° - 1 0 “ 5 jig) led to disappear­ ance of statistically significant differences in the amplitudes of responses to the main component

2.00 Z ll - 16:OCOF3

.50

1 . 0 0

-11 -9 -7 -5 -3 -1 log CONCENTRATION ( [ig per filter ) 0.00 -12 -10 -8 -6 -4 -2 0 Fig. 4. Dose-response curves for main pheromone log CONCENTRATION ( per filter ) component at the background of fluoranalog 2 - F16.Z 11-16: OAc at different concentrations (solid line. Fig. 2. Dose-response curves for fluoranalogs of main 10- 9 [_ig. dashed line. 10 5 jag). Background substance pheromone component: F 16.Z 11-16: OAc and has been introduced into the continuous air flux blowing ZII-I 6 OCOF 3 tested on males (n = 10). Mean response over the insect antenna. Tested 8 males. Mean response ± SEM. ± SEM. A. A. Nikonov et al. • Fluoranalogs of the Main Pheromone Component of Female Mamestra brassicae 511

In the continuous air flux fluoranalog No. 3 at a other species inhabiting this territory. Fluoranalog concentration of 10 ~ 1 0 (ig changed the EAG re­ No. 3 turned out attractive for Mamestra oleracia sponses to the main pheromone component L. (Table I). (Fig. 5). A significant decrease of the amplitude of Fluoranalog No. 3, used in the trap together responses appeared at a concentration of 1 0 ~ 9 [ig with the main component (Table II), completely per filter. The enhancement of the concentration suppressed the attractivity of trap for Mamestra of fluoranalog No. 3 to 10 - 6 ^g changed the brassicae and Discestra trifolii Hufn. while the at­ character of responses: the amplitude decreased tractivity of this blend did not change for M ame­ and the dependence of the amplitude of responses stra oleracia L. In a similar situation fluoranalog on lgC disappeared. When the concentration of No. 1, used like No. 3 with the main component, fluoranalog No. 3 increased, the EAG response of suppressed the attractivity to Mamestra brassicae, males upon injection of the main component was and besides it enhanced the attractivity of the completely blocked in a wide range of concen­ blend for Discestra trifolii Hufn. Fluoranalog No. 2 trations (Fig. 5). changed the main component attractivity to none

of Mamestra brassicae (Fig. 6 ). Later on we paid Field trapping experiments our attention to fluoranalog No. 3 as the chief can­ The traps with odorants under study (2 mg of didate for suppression of attractivity of the main each substance on the cuts of a rubber hose) were pheromone component of Mamestra brassicae. hung about after Mamestra brassicae (the second In the series of 1989 we investigated the concen­ generation) had started their flight. The total num­ tration dependence of the influence of fluoranalog ber of Mamestra brassicae caught into the traps in 1988 are presented in Tables I and II. There were Table I. The number of male butterflies of different mainly two species of butterflies, which were species caught in the traps filled with pure substances. caught into the traps filled with the main phero­ Mean data for one trap are presented in brackets. mone component of Mamestra brassicae: a) Ma­ Variants of experiments mestra brassicae (its part in the total number Standard No. 1 No. 2 No. 3 was 49-65%) and b) Discestra trifolii Hufn. Mamestra brassicae L. 62 0 0 0 (28-39%). In the traps individual representatives (12.4 ± 3.1) Mamestra oleracia L. 0 0 0 106 of other species were present as well. Pure fluor- (21.2 ± 6.3) analogs No. 1 and No. 2 did not attract Mamestra Discestra trifolii Hufn. 50 3 0 0 (10.0 ± 3.6) brassicae and were practically of no interest for

log CONCENTRATION ( fig per filter )

Fig. 5. Dose-response curves for main pheromone Fig. 6 . Attractivity of pheromone traps with blends component at the background of fluoranalog 3 - of main pheromone component and fluoranalogs Z 11-16: OCOF 3 at different concentrations (solid line, for Mamestra brassicae (FI, main component + 10- 1 0 [xg, dashed line, 10~ 6 ^ig). Background substance F16,Zll-16:OCOF3; F2, main component + has been introduced into the continuous air flux blowing F16,Zll-16:OAc; F3, main component + over the insect antenna. Tested 8 males. Mean response Z 11-16: OCOF 3 ). The ordinate indicates the quantity of ± SEM. the caught insects normalized by control quantity. 512 A. A. Nikonov et al. ■ Fluoranalogs of the Main Pheromone Component of Female Mamestra brassicae

Table II. The number of male butterflies of different species caught in the traps filled with blends of substances. Mean data for one trap are presented in brackets.

Variants of experiments Noctuidae Standard No. 1 No. 2 No. 3

Mamestra brassicae L. 59 2 70 0 (11.8 ± 3.2) (14.0 ± 2.5) Mamestra oleracia L. 2 0 2 144 (29.7 ± 2.8) Discestra trifolii Hufn. 26 71 23 0 (5.2 ± 1.0) (14.2 ± 1.7) (4.6 ± 1.2)

2.0 ± SEM No. 3 in the field trapping experiments. Fig. 7 rep­ resents this dependence in a normalized form. It >> 1.5 should be noted that the concentrations of fluor- C 03 analog No. 3 from 0.1 to 0.001 mg per trap are cr TD rather effective in order to suppress attractivity for Ö 1.0 N Mamestra brassicae. However, this effectiveness only manifests itself if fluoranalog is in the trap. O c 0.5 Its presence becomes entirely ineffective when it is transferred out of the trap 40 cm to the right or

left or both up and down (Fig. 8 ). contr. +0.05F3 +0.001F3 +0.1 F3 +0.01F3 +0.0005F3 Discussion Fig. 7. Attractivity of pheromone traps with blend In conditions of our experiment with males of of main pheromone component and fluoranalog 3 (Zll-16:OCOF3) at different concentrations for M ame­ Mamestra brassicae we found a complicated form stra brassicae (control, the pure main pheromone com­ of dose-dependent EAG responses to the main ponent; +0.1 F3, added 0.1 mg of fluoranalog F3; +0.05 pheromone component (Z11-16: OAc). Unlike F3, added 0.05 mg of fluoranalog F3; +0.01 F3, added the dependence mentioned in the work of Boeckh, 0 . 0 1 mg of fluoranalog F3; + 0 . 0 0 1 F3, added 0 . 0 0 1 mg of fluoranalog F3: +0.0005 F3. added 0.0005 mg of fluor- Kaissling and Schneider (1965), we revealed an analog F3). S-shaped character of the amplitude upon an increase of the stimuli concentration. A similar dependence of the amplitude of responses was dis­ 1.5 + SEM cussed by Skirkyaviechus and Skirkyavichene (1988), who explained these effects by the pres­ ence of several types of receptor cells in one sen- 1.0 sillum. These receptor cells determined by an unequal biological role of the latter in this signal. Sexual pheromones of Mamestra brassicae are 0.5 multicomponent, polyfunctional blends. Our pre­ liminary morphological investigations also showed a great “populatedness” of the sensillum of Mame­ -li l l l i i l stra brassicae with different kinds of dendrites contr. 10cm 40cm bottom (Fig. 9). In the olfactory sensillum we found about blend 20cm 80cm top 9 dendrites, different in diameter. Proceeding from Fig. 8 . Influence of space separation of the main phero­ Schneider’s model (Schneider, 1962), an increase mone component and fluoranalog 3 - Zll-16:OCOF3 of the EAG response amplitude at increasing stim­ on the attractivity of pheromone traps for Mamestra brassicae. The abscissa indicates the variation of space uli concentrations could account for a growing separation. Control, the pure main component. number of cells involved into the reaction. A. A. Nikonov et al. • Fluoranalogs of the Main Pheromone Component of Female Mamestra brassicae 513

significant repeated threshold EAG reaction (Fig. 1 B). Similar responses were also revealed upon presentation of fluoranalogs No. 1 and No. 3. We think that this response reflects the reaction of “distant receptors”, which determine the region of behavioural thresholds of the above insects

( 1 0 - lo- 1 0 - 9 jig). The absence of significant EAG responses

within 1 0 _9 - 1 0 - 7 fig per filter may be due to auto­ adaptation found by Strausfeld and Kaissling (1986) (this assumption being indirectly supported by a greater amplitude of EAG response to an odour, after the antenna had been blown through with fresh air for a long time), or due to some decrease in antenna size on amputation which can lead to changes in the threshold of olfactory reac­ tions by 2 to 4 orders (Tamhancar et al., 1990). The maximal amplitudes of responses were typi­

cal for the concentration range of 1 0 - 7 - 1 0 - 3 jig. Fig. 9. Cross section of trichoid sensillum of Mamestra This concentrational region was also characterized brassicae. Nine different outer dendritic segments are enclosed in the dendritic sheath. Ultrathin sections were by the linear dependence of amplitudes on the obtained on Ultratom LKB-880 by using electron micro­ stimuli concentration as described earlier (Boeckh scope JEN-100 B. Bar = 1.1 fim. et al., 1965). Here the majority of receptor cells of Mamestra brassicae responded to odour, and In our case the periodicity of the amplitude in­ odour differentiation processes occurred in them. crease might be explained by a different threshold These responses are shown in Fig. 1. Significant sensitivity of individual cell communities to the differences between fluoranalog No. 1 and the main pheromone component. Olfactory receptor main pheromone component are peculiar to this proteins with different constants of binding to one concentration range. This indicates that these substance (camphor) were earlier revealed in substances interact with different receptors. Dif­ vertebrates (Fesenko et al., 1985). The olfactory ferent effects of this odour on receptor cells in system of insects may also include several classes, these two concentration ranges are, probably the differentiated by specificity of binding of olfactory reason for the loss of attractivity to main phero­ receptors and/or specific pheromone-binding pro­ mone component. teins of receptor lymph (Vogt and Riddiford, 1981; A joint action of the above substances on the Vogt et al., 1991) that allow an effective func­ insect antenna, which is demonstrated in Fig. 3, tioning of the analyzer in a wide concentration witnesses a greater specificity of these receptor to range. the main component within 10_ 7 -1 0 - 3 fig. By con­ High-sensitive “distant receptors”, which are trast to this, in the range of threshold concen­ present on the antennae of males, react to a little trations they most likely interact with similar re­ amount of female pheromone in the air. This is ceptors. This is supported by the equal amplitudes suggested by behavioural reactions of insects of responses. As these substances act in a different (wing vibration), which appear at odour concen­ manner within these concentration ranges, this trations usually insufficient for recording the EAG may be a reason of different behavioural re­ responses (Kaissling and Priesner, 1970). We suc­ sponses to them. ceeded in recording an electroantennographic re­ In the field tests fluoranalog No. 3 showed good sponse of the Mamestra brassicae receptor system disguising properties with respect to Mamestra to the first presentation of the main pheromone brassicae. In our opinion, the mechanism of its ac­ component at a rather low concentration, different tion, however, differs from fluoranalog No. 1. This by 4 orders from that giving rise to a statistically is indicated by a strong suppression of the EAG 514 A. A. Nikonov et al. • Fluoranalogs of the Main Pheromone Component of Female Mamestra brassicae response in both concentration ranges (Fig. 5). sidered definitive. It requires a confirmation by a Such a suppression could be interpreted as a com­ more direct method, i.e. by recording electric re­ petitive inhibition. However, the inhibition of sponses of single sensilla in the situations modulat­ EAG responses when fluoranalog No. 3 is used in ing field conditions. a pure state or when this mixed with pheromone, At present almost any change in pheromone makes such an assumption less possible. Field tests blend is known to result in a decrease of its at- have shown that fluoranalog No. 3 is attractive tractivity (Safonkin, 1991). However, the mecha­ for Mamestra oleracea L., whose main pheromone nism of this phenomenon still remains unclear on is composed of Zll-16Ac and Z11-160H and the cellular level (Kaissling, 1986; Christensen et al., is inactive for Mamestra brassicae L. (Subchev 1989). When analyzing the responses of cells on dif­ et al., 1989). ferent levels of olfactory analyzer of insects This effects might be explained by the influence (O'Connell, 1985; Kaissling et al., 1989), the authors of these substances on different receptor cells in conclude that an odour is received and coded on the sensillum. Such a way of suppressing the reactions level of receptor cells. Yet recognition of odour in­ to a sexual attractant is known and was mentioned formation occurs in the highest regions of the ner­ earlier (Bogdanova et al., 1980; Christensen et al., vous system. Most likely, different kinds of adap­ 1990). It is not excepted that this is heteroadap­ tation play the key role in the primary processes tation described by Strausfeld and Kaissling (Kapitsky and Gribakin, 1991). The change in EAG (1986). This heteroadaptation is not very long­ responses of the blend of pheromone-like sub­ term, which is confirmed by the data obtained in stances revealed by us in different concentration our behavioural experiments (Fig. 8 ). But this con­ ranges makes the picture highly diverse. The pre­ clusion made on the base of the study of antenna sent study demonstrates a possibility of investiga­ EAG responses and field tests may not be con- ting these processes on the antennographic level.

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