History of echolocation studies in noctuid moths

It was Howard Hinton who first suggested the possibility that moths orientate themselves by means of echolocation (Hinton, 1955). The same idea was also discussed by Roeder and Treat (1957) along with the demonstration of the ability to emit short ultrasonic clicks at a certain fixed phase of a wingbeat in Prodenia eridania Since noctuid moths were known to possess the ears sensitive to ultrasound the idea of echolocation seemed to be reasonable, even though it was generally beleived that the main function of hearing in moths was to detect a hunting bat's cries.

Later the possibility of echolocation in moths was discussed by Kay (1969) and Agee (1971). It was also proposed by G. Gornostaev, a Russian enthomologist, that an echolocation rather than bat detection was a primary function of moth's ears (Gornostaev, 1984).

Nevertheless, at that time the experimental studies of echolocation in noctuid moths had not evolved. Probably a low interest to the problem was due to the lack of appropriate methods. The first experimental data related to the echolocation capability of the noctuid moths were only obtained 22 years later (Lapshin et al., 1993a,b)

Our very first experiments were based on a simple idea that whatever the maximal range of moth's echolocation system would be it should detect the nearest objects to avoid collisions. Moth of a mean size has a forewing of 2-3cm long so we did assume the required lower distance of echolocator to be 2.5cm. An echo of the click reflected back to a moth from that distance will reach it's ears 0.15 ms after the click production. This interval seemed to be too small compared to the estimated temporal resolution of an auditory system. Measured by different authors, it ranges from 2.5 ms (Surlykke et al., 1988) to 3-4 ms (Lapshin, Fyodorova, 1996) that is, more than an order higher than the expected delay of an echo. In other words, the experimental facts at that time were against the possibility of echolocation in moths since there were no way to distinguish between an own click and its echo.

When designing our own experiments directed to the study of echolocation in moths we had to resolve several contradictions. The first and, probably, the most difficult question was how to distinguish between the forms of orientation based on vision and echolocation. If we prevent vision by applying some black dye to the eyes of a moth it would stop flying. In case we conduct our experiments in total darkness it would be rather difficult to record moth's behavior. It should be mentioned that moths are suspected to possess a sensitivity to infrared light (Kay, 1969). Although that assumption still has no experimental justification we prefered not to use infrared video equipment in our experiments.

A "carousel" setup

For our first experiments aimed to test the echolocation hypothesis we have designed a so-called "carousel" setup in which a moth fastened to a thin wire was flying in complete darkness between obstacles with different coefficients of acoustic reflectance.

It appeared that the probability of moth collision with an obstacle depended on the reflectance properties of the latter.

It is important that such a correlation was only observed in the presence of moth's clicks. Non-clicking moths did not distinguish between different obstacles. Thus, our first experiments supported the idea that noctuid moths are capable of echolocation (Lapshin et al, 1993b).

Vision and echolocation

During the preliminary studies we have found that moths tend not to click or even not to fly in a total darkness. Based on that we have made an attempt to study the interrelation between the vision and the echolocation. To give a tethered flying moth an adequate visual stimulation we have projected an image of approaching obstacle to a flat screen. The image contained a vertical bar imitating a trunk of a tree moving towards a moth. The whole setup might look like a virtual reality made for a flying insect. Simultaneously we have recorded moth's clicks and movements.

Such a visual stimulation caused a remarkable increase of click frequency, especially when the "tree" had already disappeared from the screen, while the motor responses were rather weak (Lapshin, 1996).

The retransmission method

In our experiments moths had no certain sign of response to the echo: they demonstrated either movement to the object which was detected by means of echolocation or detour manoeuvre, the changes of motivation occurring repeatedly during the experiment in some specimens. This variability of the insect behaviour introduced ambiguity in the results obtained and it became necessary to find more stable indicator of moth capability to perceive echo.

Earlier, similar problem arose and was solved in the course of studying responses to artificial stimuli in bats. It appeared that a good indicator of increased attention of a bat to biologically significant echolocation signals could be increased emission of the probing pulses (Grinnell, Griffin, 1958). Such changes were reproducible and could easily be registered. How do the noctuid moths behave in analogous situations? One could suggest that in moths, echolocation stimuli would evoke similar responses - increasing frequency of their own clicks.

We have verified this suggestion by using a restransmission method: the stimulus imitating an echo from a non-existent (virtual) obstacle was retransmitted towards a moth after a certain delay in relation to it's own click. There was a dialog between the moth and the stimulating apparatus (some kind of self-stimulation). What is most important is that such stimulation system did not contain any movable details and thereby guaranteed that the results obtained were independent of the visual and tactile sensitivity of an insect.

We had used the retransmission method twice: first, in 1993, during the preliminary studies of echolocation in moths and later (Lapshin et al., 1993), from 1997, to perform different measurements (Lapshin, Vorontsov, 1998, 2009). Due to its advantages this method had become our primary one during the following studies of echolocation.

It has been found that echo-stimulation evokes significant increase in mean emission rate of own clicks. This finding gave us another evidence that noctuid moths are capable to receive echo. As a rule, the stimuli having similar acoustic parameters but not correlated in time with own clicks a moth evoked an opposite response - suppression of acoustic activity.

Among the noctuid moths studied, the capability to perceive signals imitating echo of their own clicks was demonstrated most convincingly by Blepharita satura From the results obtained, it could be also concluded that, at present, variations in the rate of acoustic emission should be considered as the most reliable index of the insect behaviour response to echo.

The manouvres of a moth were recorded along with its clicks. Most specimens demonstrated a high variability of spontaneous motor activity. In the absence of any noticeable external stimuli, they often made abrupt manoeuvres or prolonged low frequency oscillations from side to side. On such variable manoeuvre background, it was rather difficult to consider the moth jerks aside as indication of response to the echo, even when such jerks were very well expressed.

Overcoming the temporal resolution problem

Even after the echolocation has been proven in different experiments still we had a very important problem unsolved: the temporal resolution of a moth's ear was insufficient to detect an echo shortly after perceiving its own, very loud compared to an echo, click. But, we knew that already, moths have somehow overcome this limitation.

Using the retransmission method described above we have measured the auditory thresholds at stimulus delays 0.2, 0.3, 0.5 and 1 ms in relation to the respective moth click. The results suggested that moths are able to perceive echoes of their own signals: the best (minimal) threshold values were obtained at 0.5 ms of the stimulus delay. To realise that ability a moth should suppress the response of its auditory receptors to the own click. The decrease in responses of auditory receptors to the loud stimuli was earlier described in noctuids (Perez and Coro, 1985). We believe that the own click of a moth causes paradoxical reaction of the tympanic auditory receptors, namely, the suppression of their activity.

More about echolocation

That is not the end of the story. In echolocation section you can find a more detailed description of our methods and results, as well as of other aspects of echolocation in moths. See also two separate sections about the sound production and the auditory system.

The problems that arose during the studies of echolocation in noctuids and the ways these problems had been solved were also reviewed in detail in a book "Echolocation system of nocturnal moths" (Lapshin, 2005, in Russian - Contents in English).

To be continued...

References

Hinton, H.E. (1955) Sound producing organs in the Lepidoptera. // Proc. Royal Entom. Soc. London. Ser. C, 80: 5 - 6.

Roeder K.D., Treat A.E. (1957) Ultrasonic reception by the tympanic organ of noctuid moths // J. Exp. Zool. V.134. P.127-158.

Kay R.E. (1969) Acoustic signalling and its possible relationship to assembling and navigation in the moth Heliothis zea // J. Insect. Physiol. V.15. P.989-1001.

Agee H.R. (1971) Ultrasound produced by wings of adults of Heliothis zea // J. Insect. Physiol. V.17, N7. P.1267-1273..

Gornostaev, G.N. (1984) An introduction to the ethology of photoxenic insects (insect flight to artificial light), Proceedings of the All-Union Entomological Society, Leningrad: Nauka Publ, No. 66, 101-167 (In Russian).

Lapshin, D.N., Fyodorova, M.V. and Zhantiev, R.D. (1993a). Emission and perception of ultrasounds in some noctuid moths (Lepidoptera, Noctuidae). Sensory System of Arthropods. K. Wiese et al. (eds), Birkhauser Verlag Basel, Switzerland, 363-369.

Lapshin D.N., Fyodorova M.V., Zhantiev R.D. (1993b) Echolocation of noctuid moths (Lepidoptera, Noctuidae) // Zool. Zhurn. 1993. V.72. No9, P.93-104 (in Russian). Translation: D.N. Lapshin, M.V. Fyodorova, R.D. Zhantiev. Echolocation in Noctuidae (Lepidoptera) // Entomological Review, 1994. V.73. No 3. P.53-63

Surlykke A., Larsen O.N., Michelsen A. (1988) Temporal coding in the auditory receptor of the moth ear // J. Comp. Physiol. V.162, P.367-374.

Lapshin D.N., Fyodorova M.V. (1996) Responses of tympanic organs to ultrasonic pulses in noctid moths (Amphipyra perflua: Noctuidae) // Sensornye systemy 10(1) 5-17 (in Russian).

Lapshin D.N. Influence of vision stimuli upon the variation of acoustic emission in moth (Amphipyra perflua: Noctuidae) // Sensornye Systemy, 1996, V.10. No3, P.79-87 (in Russian). Translation: Effect of visual stimuli on the dynamics of acoustic emissions by noctuid moths (Amphipyra perflua:Noctuidae) // Sensory Systems. 1996. V.10. No3. P.207-214.

Grinnell A.D., Griffin D.R. (1958) Sensitivity of echolocation in bats // Biol. Bull. V.114. No1. P.10-22.

Lapshin D.N., Fyodorova M.V., Zhantiev R.D.. Echolocation of noctuid moths (Lepidoptera, Noctuidae) // Zool. Zhurn. 1993. V.72. 9, P.93-104 (in Russian). Translation: D.N. Lapshin, M.V. Fyodorova, R.D. Zhantiev. Echolocation in Noctuidae (Lepidoptera) // Entomological Review, 1994. V.73. 3. P.53-63

Lapshin D.N., Vorontsov D.D. (1998) Activation of echolocation signal emission by noctuid moths (Noctuidae, Lepidoptera) in response to retranslation of echo-Like stimuli // Doklady Biological Sciences, V.362. 4. P.448-450. Translation: Doklady Akademii Nauk, V.362, 4, P.567-569.

Lapshin D.N., Vorontsov D.D. (2009) The dependence of behavioral auditory thresholds on the delay of echo-like signals in noctuid moths (Lepidoptera, Noctuidae) // Journal of Integrative Neuroscience, V.8. 1. P. 1-12.

Lapshin D.N. Echolocation system of nocturnal moths. Ed. by N.A. Tamarina. Moscow: Nauka 2005. 206 p. (in Russian, Contents in English).