01757nas a2200097 4500008004100000245004900041210004700090520145100137100002101588856005001609 2003 eng d00aBats and moths: what is there left to learn?0 aBats and moths what is there left to learn3 a

Over 14 families of moths have ears that are adapted to detect the ultrasonic echolocation calls of bats. On hearing a bat, these moths respond with an escape response that reduces their chances of being caught. As an evolutionary response, bats may then have evolved behavioural strategies or changes in call design to overcome the moth's hearing. The nature of this interaction is reviewed. In particular, the role of the echolocation calls of bats in the shaping of the structure, neurophysiology and behavioural responses of moths is discussed. Unresolved issues, such as the structural complexity of the moth's auditory system, the nature of temporal integration and the role of the non‐auditory B cell, are described. Issues in which the interactions between bats and moths may be of more general interest to biologists, such as noise filtering within the central nervous system, protean behaviours and coevolution between predator and prey, are also discussed. The interaction between bats and moths has much to interest general biologists, and may provide a useful model in understanding the neurophysiological basis of behaviour, including protean escape behaviours. The validity of the term coevolution as applied to this system is discussed, as there is no doubt that the auditory system of moths is a response to the echolocation calls of bats, although the evolutionary response of bats to moths is more ambiguous.

1 aWaters, Dean, A. uhttp://www.blackwell-synergy.com/toc/pen/28/401898nas a2200133 4500008004100000245006000041210005900101520143500160100003101595700002601626700002601652700001901678856006701697 2006 eng d00aKeeping up with Bats: Dynamic Auditory Tuning in a Moth0 aKeeping up with Bats Dynamic Auditory Tuning in a Moth3 a

Many night-flying insects evolved ultrasound sensi- tive ears in response to acoustic predation by echolo- cating bats [1–10]. Noctuid moths are most sensitive to frequencies at 20–40 kHz [6], the lower range of bat ultrasound [5, 11–13]. This may disadvantage the moth because noctuid-hunting bats in particular echo- locate at higher frequencies shortly before prey cap- ture [7, 11–13] and thus improve their echolocation and reduce their acoustic conspicuousness [6–10, 12–16]. Yet, moth hearing is not simple; the ear’s non- linear dynamic response shifts its mechanical sensi- tivity up to high frequencies. Dependent on incident sound intensity, the moth’s ear mechanically tunes up and anticipates the high frequencies used by hunt- ing bats. Surprisingly, this tuning is hysteretic, keep- ing the ear tuned up for the bat’s possible return. A mathematical model is constructed for predicting a lin- ear relationship between the ear’s mechanical stiff- ness and sound intensity. This nonlinear mechanical response is a parametric amplitude dependence [17, 18] that may constitute a feature common to other sen- sory systems. Adding another twist to the coevolu- tionary arms race between moths and bats, these re- sults reveal unexpected sophistication in one of the simplest ears known and a novel perspective for inter- preting bat echolocation calls.

1 aWindmill, James, Frederick1 aJackson, Joseph, Curt1 aTuck, Elizabeth, Jane1 aRobert, Daniel uhttps://linkinghub.elsevier.com/retrieve/pii/S096098220602321902286nas a2200121 4500008004100000245007100041210006700112520188600179100002002065700001502085700002302100856004102123 1989 eng d00aThe neuroethology of acoustic startle and escape in flying insects0 aneuroethology of acoustic startle and escape in flying insects3 a

The acoustic startle/escape response is a phylogenetically widespread behavioral act, provoked by an intense, unexpected sound. At least six orders of insects have evolved tympanate ears that serve acoustic behavior that ranges from sexual communication to predator detection. Insects that fly at night are vulnerable to predation by insectivorous bats that detect and locate their prey by using biosonar signals. Of the six orders of insects that possess tympanate hearing organs, four contain species that fly at night and, in these, hearing is sensitive to a range of ultrasonic frequencies found in the biosonar signals of bats. Laboratory and field studies have shown that these insects (including some orthopterans, lepidopterans, neuropterans and dictyopterans), when engaged in flight behavior, respond to ultrasound by suddenly altering their flight, showing acoustic startle or negative phonotaxis, which serve as bat-avoidance behavior. A neural analysis of ultrasound-mediated escape behavior was undertaken in the field cricket Telegryllus oceanicus. An identified thoracic interneuron, int-1, was shown to trigger the escape response, but only when the cell was driven (synaptically or electrically) at high spike rates, and only when the insect was performing flight behavior; avoidance steering only occurs in the appropriate behavioral context: flight. Thus, significant constraints operate upon the ability of int-1 to trigger the escape response. The integration of auditory input and flight central pattern generator output occurs in the brain. It is found that neural activity descending from the brain in response to stimulation by ultrasound is increased when the insect is flying compared to when it is not. Although the behavioral act of avoidance steering may appear to be a simple reflex act, further analysis shows it to be anything but simple.

1 aHoy, Ronald, R.1 aNolen, Tom1 aBrodfuehrer, Peter uhttps://bio.acousti.ca/it/node/5766801204nas a2200097 4500008004100000245009500041210006900136520083300205100002401038856004401062 1978 eng d00aResonant wing systems in the Australian whistling moth Hecatesia (Agarasidae, Lepidoptera)0 aResonant wing systems in the Australian whistling moth Hecatesia3 a

DARWIN described the sound made by the forewings of the nymphalid Ageronia feronia as a click of a spring catch on a toothed wheel. Descriptions of the sounds produced by the Agarasidae, which have similarly modified forewings, have repeatedly invoked the rubbing of either the antennae or foretibia on the ribbed forewing2,3. Nicholson4 suggested that the production of sound in the whistling moth Hecatesia was percussive, with the knobs of each forewing (castanets) striking each other at the top of the flight stroke. I have confirmed the existence of such a percussive system in two species of Hecatesia. Recordings of H. exultans Walker and H. thyridion Feisthamel from the coastal sand plain of Western Australia revealed two patterns of sound corresponding to the respective flight behaviour of the two species.

1 aBailey, Winston, J. uhttp://www.nature.com/articles/272444a002100nas a2200109 4500008004100000245006100041210006100102520173500163100002401898700002001922856004801942 1988 eng d00aTemporal coding in the auditory receptor of the moth ear0 aTemporal coding in the auditory receptor of the moth ear3 a

Temporal coding in the moth ear was inferred from the response of the auditory receptor to acoustic stimuli with different temporal characteristics.

1.Determinations of the threshold with different stimulus pulse durations showed that the moth ear behaves as an energy detector with a maximum time constant (the integration time) of 25 ms. Pulse durations beyond this value did not result in decreased thresholds (Fig. 1).

2.The synchronization to amplitude modulations was determined by stimulating the moth ear with amplitude modulated (AM) tones (carrier frequency: 40 kHz) and AM white noise presented as 450 ms pulses separated by pauses of similar length. The modulation depth was constant (100%) whereas the modulation frequency,fm, was varied. The maximumfm which the auditory receptors could follow was 200 Hz (P<0.05) (Figs. 2, 3, 4).

3.The relatively broad tuning of the only receptor which was functional at the relevant stimulus intensities suggested that AM detection could only be based on temporal cues. This was confirmed by the results showing the same degree of synchronization independent of carrier.

4.A minimum time constant for the receptor was also determined by interrupting a 400 ms noise pulse by a gap (Figs. 5, 6). The threshold for gap detection of the moth ear was ca. 2 ms on a 2.5% significance level (one sided test).

5.The temporal acuity reported here seems to be fine enough to explain the temporal resolution suggested by behavioral results from other insect species. The results are discussed in relation to acoustic communication in insects as well as in relation to temporal resolution in vertebrates.

1 aSurlykke, Annemarie1 aMichelsen, Axel uhttp://link.springer.com/10.1007/BF0060612301326nas a2200157 4500008004100000022001400041245010900055210006900164260001600233300001200249490000800261520073200269100001701001700001401018856013601032 1994 eng d a1471-295400aWingbeat-generated ultrasound in noctuid moths increases the discharge rate of the bat-detecting A1 cell0 aWingbeatgenerated ultrasound in noctuid moths increases the disc cOct-10-1995 a41 - 460 v2583 a

Some noctuid moths produce ultrasound in flight as a consequence of contact between the distal margins of the hindwings. The sound produced from a conspecific 10 mm from the subject increases the discharge rate of the moth’s A1 acoustic cell which functions primarily to detect the echolocation calls of bats. Wingbeat sounds are largely ultrasonic, and may provide background noise through which the moth must recognize bat echolocation calls. The sounds may also limit the lower sensitivity of the auditory system. Wingbeat sounds produced appear to be mismatched to the low-frequency hearing of bats which hunt by passive listening, and are unlikely to be a significant aid to passive aerial foraging by bats.

1 aWaters, D.A.1 aJones, G. uhttp://www.royalsocietypublishing.org/doi/10.1098/rspb.1994.0139https://syndication.highwire.org/content/doi/10.1098/rspb.1994.013902589nas a2200253 4500008004100000022001400041245009400055210006900149260002000218300001600238490000800254520170300262653003501965653003602000653001902036653003302055653002002088100002502108700002102133700002202154700002202176700001702198856012002215 2013 eng d a0022-094900aThe simple ears of noctuoid moths are tuned to the calls of their sympatric bat community0 asimple ears of noctuoid moths are tuned to the calls of their sy cFeb-04-20132149 a3954 - 39620 v2163 a

nsects with bat-detecting ears are ideal animals for investigating sensory system adaptations to predator cues. Noctuid moths have two auditory receptors (A1 and A2) sensitive to the ultrasonic echolocation calls of insectivorous bats. Larger moths are detected at greater distances by bats than smaller moths. Larger moths also have lower A1 best thresholds, allowing them to detect bats at greater distances and possibly compensating for their increased conspicuousness. Interestingly, the sound frequency at the lowest threshold is lower in larger than in smaller moths, suggesting that the relationship between threshold and size might vary across frequencies used by different bat species. Here, we demonstrate that the relationships between threshold and size in moths were only significant at some frequencies, and these frequencies differed between three locations (UK, Canada and Denmark). The relationships were more likely to be significant at call frequencies used by proportionately more bat species in the moths' specific bat community, suggesting an association between the tuning of moth ears and the cues provided by sympatric predators. Additionally, we found that the best threshold and best frequency of the less sensitive A2 receptor are also related to size, and that these relationships hold when controlling for evolutionary relationships. The slopes of best threshold versus size differ, however, such that the difference in threshold between A1 and A2 is greater for larger than for smaller moths. The shorter time from A1 to A2 excitation in smaller than in larger moths could potentially compensate for shorter absolute detection distances in smaller moths.

10aallotonic frequency hypothesis10aconstant-frequency echolocation10ahorseshoe bats10apredator–prey interactions10asensory ecology1 aHofstede, H., M. ter1 aGoerlitz, H., R.1 aRatcliffe, J., M.1 aHolderied, M., W.1 aSurlykke, A. uhttp://jeb.biologists.org/cgi/doi/10.1242/jeb.093294https://syndication.highwire.org/content/doi/10.1242/jeb.09329401003nas a2200133 4500008004100000245008700041210006900128300001000197490000600207520054100213100002600754700002000780856006900800 1993 eng d00aThe ultrasonic song of the moth Amyna natalis (Lepidoptera:Noctudidae: Acontiinae)0 aultrasonic song of the moth Amyna natalis LepidopteraNoctudidae  a89-970 v53 a

In Malaysia, males of the noctuid moth Amyna natalis were observed producing a continuous ultrasonic song of high intensity (about 102 dB SPL measured at a distance of 10cm). The frequency spectrum of the sound impulses had its peak between 60 and 80 kHz. During song production the animals were perching on plants and moving their wings up and down quickly. Simultaneously, by twisting the wings it seems likely that a male-specific “bubble'' in the forewing functions as a tymbal, resulting in sound production.

1 aHeller, Klaus-Gerhard1 aAchmann, Roland uhttp://www.tandfonline.com/doi/abs/10.1080/09524622.1993.9753231