Naturwissenschaften 86, 276–279 (1999) Springer-Verlag 1999 Why Do Diurnal Moths Have Ears? James H. Fullard Department of Zoology, Erindale College, University of Toronto, 3359 Mississauga Rd., Mississauga, Ontario L5L 1C6, Canada Jeff W. Dawson Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada Received: 14 September 1998 / Accepted in revised form: 11 December 1998 Introduction Ears exist in moths primarily for the purpose of detecting hunting bats at night to avoid predation. The ears of four species of day-flying Nearctic moths are as sensitive as those of a common, night-flying genus to the frequencies emitted by sympatric bats and show no evidence of being vestigial. We determined that all of the day-flying moths spend 44–73% of their 24-hour cycles active at night when bats hunt. Two of the moths tested are sound-emitting species and may use their ears during intraspecific communication. We conclude that the functions of bat detection and social communication are the only selective forces acting on moth ears, and that in their absence these sensory structures degenerate. Most moths have simple ears on various parts of their bodies that they use to detect the echolocation calls of aerially hunting, insectivorous bats [1]. Where bats are numerous and diverse (e.g., the tropics), the ears of sympatric moths are more sensitive to a broader range of frequencies than those that live in areas of lower bat diversity (e.g., temperate regions) [2]. Certain habitats exist that are spatialCorrespondence to: J.H. Fullard e-mail: [email protected] Tel.: c1-905-828-5416 Fax: c1-905-828-3792 276 ly and/or temporally bat free (i.e., places and/or times that bats do not exist), and some of the moths in these habitats exhibit ears with varying levels of auditory degeneration (e.g., oceanic island moths [3], wintermoths [4]). Other moths experience release from bat predation and corresponding auditory degeneration by means of extreme behavioral changes (e.g., flightlessness [5–8]). For temporal bat release a pronounced example of auditory degeneration exists in certain members of the Dioptinae, a group of diurnal Neotropical moths [9]. If diurnal habits result in bat-free environments, we should expect auditory degeneration in day-flying moths, assuming that they do not use their ears for other purposes (e.g., social communication). We examined the auditory, activity, and acoustic characteristics of four species of Nearctic dayflying moths to test this hypothesis. Materials and Methods From June until September 1998 we collected the following noctuoid moths from wild populations as they flew during the day at the Queen’s University Biology Station in eastern Ontario, Canada: (Arctiidae) Cycnia tenera, Ctenucha virginica; (Lymantriidae):Lymantria dispar (males only, females do not fly); and (Noctuidae): Caenurgina erechtea. We used standard techniques [9] to expose and re- cord from the auditory nerve of moths placed 20 cm from a Technics loudspeaker (EAS-10TH400B). The preparations were exposed to 10 ms (1 ms rise/fall time) sound pulses at frequencies of 5–100 kHz at 5-kHz increments generated by a WaveTek function generator (model 23), shaped by a Coulbourn S84-04 envelope shaper and amplified (National Semiconductor LM1875 T). The presentation of the pulses was randomized by a MS-DOS program (written by J.W.D.). The thresholds of the most sensitive receptor cell (A1) were recorded as the stimulus intensity (dB SPL) required to elicit two action potentials to at least three stimulus pulses in a row. To determine the 24-h activity patterns of the moths we placed moths (not the same as those used for the auditory analyses) in 15.2-cm-tall semicylindrical (6.5 cm diameter) screened chambers that were supplied with microcentrifuge tubes filled with dilute sucrose and visually separated from each other. The chambers were placed in a 221!273!202 cm screen enclosure in a partially open forest so that they were exposed to ambient temperatures and light levels and isolated from human disturbance. The chambers were placed 60 cm before a video camera capable of automatically switching from the use of ambient light during the day to a built-in source of near infra-red (wavelengthp980 nm) light during the night (Sanyo VDC-9212). The camera’s output was fed into a VCR in another room, and the moths’ 24 h activities were recorded using 10-h video tapes (BASF T-200). Activity was scored as the number of minutes of a 10-min bin in which the moth expressed at least one movement of a body length or more that was accompanied by vigorous wing beats during the minute. Sounds were recorded from the moths using standard high-frequency analogue recording techniques [10]. Moths were placed 5 cm in front of a 1/4 in. Brüel and Kjær (type 4135) condenser microphone (coupled to a Naturwissenschaften 86 (1999) Q Springer-Verlag 1999 Brüel and Kjær measuring amplifier, type 2206) and tactually stimulated. Sounds were recorded onto a RACAL Store 4D instrumentation tape recorder and analyzed with a Windows-based fast Fourier transformation program (ScopeDSP, Version 3.5, Iowegian International Corp., ~http://www.iowegian.com 1 ). Results Auditory Analyses Figure 1 (left) compares the auditory sensitivity curves (audiograms) of the four day-fliers that we sampled to the median audiogram of underwing moths, Catocala spp., species that were collected at ultraviolet lights during the night [11]. All but one of the day-fliers that we sampled have audiograms resembling that of Catocala spp. and all appear similarly tuned to the frequencies most commonly emitted by insectivorous bats (heavy bar in the audiograms). Activity Analyses The actograms of Fig. 1 (right) illustrate that all of the moths spent a large portion of their 24-h cycle flying during nighttime. Using sunrise/sunset times of 0540 and 2030 hours, respectively (the average times for the summer months at this site (Herzberg Institute of Astrophysics, ~http:/ /www.hia.nrc.ca 1 ), the average percentage time spent nocturnally active in all of the individuals were: Cycnia tenera: 47.5%; Ctenucha virginica: 44.0%; Lymantria dispar: 53.9%; Caenurgina erechtea: 72.8%. Fig. 1. Left, the audiograms of the day-flying moths sampled in our study (np5 for all species). Thin lines, individuals; thick lines, the median curves for each species. Included are the median audiograms (broken line) of common, night-flying noctuids, Catocala spp. Thick bar, bandwidth of predominant frequencies emitted by this area’s most common bats [22]. Right, 24-h actograms of the moths (np5 for all species, not the same as those used for the audiograms). Thin bars, ranges within each 10 min bin, thick bars are the mean values; shaded boxes, night hours for the site used in this study Acoustic Analyses Figure 2 illustrates the time-amplitude and frequency analyses of these sounds. The arctiids Cycnia tenera and Ctenucha virginica emit sounds when tactually stimulated, but Lymantria dispar and Caenurgina erechtea are silent. The sounds of the arctiids consist of trains of short clicks with predominant frequencies of 68–75 kHz (C. tenera) and 34–37 kHz (C. virginica), all within the best hearing range of their ears. Discussion The first explanation for ears in diurnal moths is that they are vestigial and serve no present function. Since there are only one (Notodontidae) to two (e.g., Noctuidae) auditory receptors in the ears of noctuoid moths, there would be little advantage for these organs to quickly disappear following the relaxation of selection pressure compared to more complex Naturwissenschaften 86 (1999) Q Springer-Verlag 1999 organs such as eyes [12]. Symptoms of auditory degeneration in bat-released insects include insensitivity to high ( 1 50 kHz) frequencies and increased threshold variability (e.g., oceanic island moths [3, 13, 14], flightless preying mantids [15], diurnal South American moths [9], wintermoths [4, 8]). Only one of the moths in the present study, Ctenucha virginica, exhibits any evidence of high frequency insensitivity compared to the audiograms 277 Fig. 2. a) Oscillograms and frequency analyses (fast Fourier transformations) of the sounds emitted by C. tenera and C. virginica. The sounds consist of trains of short clicks emitted as the sound-producing organ, the tymbal, first experiences a musculated buckling producing the active modulation half-cycle (AMHC) followed by a passive series of clicks emitted as the tymbal elastically returns to its original position producing the passive modulation half-cycle (PMHC) [10]. The fast Fourier transformations are composites of each click in the AMHC of the nocturnal Catocala spp. but C. virginica appears to offset this with high sensitivity at bat specific frequencies. The absence of overall insensitivity and high threshold variability in the day-flying moths of our study leads us to conclude that their ears are adaptively [16] functional. The second explanation for ears in diurnal moths is that the moths spend 278 at least part of their 24 h cycle flying at night when it is necessary to detect bats. The actograms suggest that all of the moths that we studied spend a considerable amount of time flying when bats are active. Surveys made at a local colony of 800–1000 Little Brown bats (Myotis lucifugus) indicate that nightly foraging for this common species begins between 2011 and 2132 hours, times that overlap the 24-h activities of the moths we tested. The day/night activities of moths may also depend upon their geographical distribution. Cycnia tenera, for example, ranges from central Ontario south to Florida where it may fly more during the relatively warmer nights. Genetically linked northern populations may favor more diurnal (i.e., warmer) activity patterns while retaining the auditory defenses of their more nocturnal conspecifics. The third reason for ears in diurnal moths is that they use them to listen for conspecific social sounds (e.g., mating calls [17]). The audiograms of both C. tenera and C. virginica appear tuned to the specific predominant frequencies of their clicks but are also sensitive to sympatric bat frequencies. The audiograms of C. virginica, the most diurnal of the moths that we tested, appear more narrowly tuned than those of the other moths, suggesting that this moth’s ears listens more for conspecific sounds than bats, an explanation offered for the sensitive ears of the diurnal Australian whistling moth, Hecatesia thyridion [18]. The sounds of C. tenera have been implicated in both social [19] and anti-bat [20] behaviors, but the purposes of the sounds of C. virginica are presently unknown. In conclusion, diurnal moths have physically evident ears for one or more of the following reasons: (a) the ears are vestigial, (b) the moths, although active during the day, still fly at night and use them for bat detection, (c) the moths use their ears for detecting social sounds. All of the moths in our study have sensitive and apparently functional ears, and probably use them as defense against bats when flying at night while two species (C. tenera and C. virginica) may additionally use them for detecting social sounds. We reject the possibility that day-flying moths have ears as a general auditory sense to detect unspecified predators other than bats for the following reasons: (a) the majority of exclusively diurnal, nonacoustic Lepidoptera (i.e., butterflies) are earless (the reported ears of certain nymphalids [21] seem adapted for intraspecific communication), (b) in cases in which exposure to bats has been drastically reduced, there is severe auditory degeneration (e.g., wingless/ earless moths [5]) and, (c) the behavior of diurnal predators is characterized by stealth rather than the emission of loud sounds as they approach an intended prey. While eyes rather than ears appear to be a diurnal insect’s greatest sensory defense, for most insects that are active for during even a small portion of a bat-inhabited night, the opposite seems true. We thank Queen’s University for permission to use their facilities, Kathleen Pendlebury, Nadia Napoleone, Alessandro Mori, and Tarah Harrison for assistance in the field and Drs. W. Conner, B. Fenton, and A. Surlykke for comments on the manuscript. This study was funded by a research grant from the Natural Sciences and Engineering Research Council of Canada. 1. Roeder KD (1967) Nerve cells and insect behavior. Harvard University Press, Cambridge 2. Fullard JH (1998) The sensory coevolution of moths and bats. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, Berlin Heidelberg New York, pp 279–326 3. Fullard JH (1994) Auditory changes in noctuid moths endemic to a bat-free habitat. J Evol Biol 7 : 435–445 4. Surlykke A, Treat AE (1995) Hearing in wintermoths. Naturwissenschaften 82 : 382–384 5. Heitmann H (1934) Die Tympanalorgane flugunfähiger Lepidopteren und die Korrelation in der Ausbildung der Flugel und der Tympanalorgane. Zool Jahrb Anat Ontogen 59 : 135–200 6. Sattler K (1991) A review of wing reduction in Lepidoptera. Bull Br Mus Nat Hist (Entomol) 60 : 243–288 7. Cardone B, Fullard JH (1988) Auditory characteristics and sexual dimorphism in the gypsy moth. Physiol Ent 13 : 9–14 8. Rydell J, Skals N, Surlykke A, Svennson M (1997) Hearing and bat defence in Naturwissenschaften 86 (1999) Q Springer-Verlag 1999 9. 10. 11. 12. geometrid winter moths. Proc R Soc Lond B 264 : 83–88 Fullard JH, Dawson JW, Otero LD, Surlykke A (1997) Bat-deafness in day-flying moths (Lepidoptera, Notodontidae, Dioptinae). J Comp Physiol A 181 : 477–483 Fullard JH (1992) The neuroethology of sound production in tiger moths (Lepidoptera, Arctiidae). I. Rhythmicity and central control. J Comp Physiol A 170 : 575–588 Faure PA, Fullard JH, Dawson JW (1993) The gleaning attacks of the northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths. J Exp Biol 178 : 173–189 Jones R, Culver DC (1989) Evidence for selection on sensory structures in a cave population of Gammarua minus (Amphipoda). Evolution 43 : 688–693 Naturwissenschaften 86, 279–280 (1999) 13. Fullard JH (1984) Acoustic relationships between tympanate moths and the Hawaiian hoary bat (Lasiurus cinereus semotus). J Comp Physiol A 155 : 795–801 14. Surlykke A (1986) Moth hearing on the Faroe Islands, an area without bats. Physiol Entomol 11 : 221–225 15. Yager DD (1990) Sexual dimorphism of auditory function and structure in preying mantises (Mantodea; Dictyoptera). J Zool (Lond) 221 : 517–37 16. Yack JE, Fullard JH (1993) What is an insect ear? Ann Ent Soc Amer 86 : 677–682 17. Sanderford MV, Coro F, Conner WE (1998) Courtship behavior in Empyreuma affinis Roths (Lepidoptera, Arctiidae, Ctenuchinae): acoustic signals and tympanic organ response. Naturwissenschaften 85 : 82–87 Springer-Verlag 1999 Mitochondrial DNA Sequence Relationships of the Newly Described Enigmatic Vietnamese Bovid, Pseudonovibos spiralis S.E. Hammer, F. Suchentrunk Research Institute of Wildlife Ecology, Vienna Veterinary University, Savoyenstrasse 1, A-1160 Vienna, Austria R. Tiedemann, G.B. Hartl Institut für Haustierkunde, University of Kiel, Olshausenstrasse 40–60, D-24118 Kiel, Germany A. Feiler Staatliches Museum für Tierkunde, Dresden, Königsbrucker Landstrasse 159, D-01109 Dresden, Germany Received: 19 October 1998 / Accepted in revised form: 17 December 1998 Only recently several new ungulate species from Southeast Asia have been described [1–4]. From one of these, the mysterious Vietnamese ungulate “Linh Duong” (Pseudonovibos spiralis), living individuals have been observed only by local hunters, but horns have become available to the Correspondence to: S. Hammer (e-mail: hammer6zoo.univie.ac.at, Tel.: 43-1-31336-1309, Fax: c43-1-31336-778) scientific community [3, 5]. Prior to the description of this enigmatic new species, such horns had already been catalogued at the Kansas Museum of Natural History in the United States, but erroneously attributed to Bos sauveli [5]. Consultations of old Chinese encyclopedias, compilations, and textbooks from the Ming and early Qing dynasties revealed a drawing of a goatlike ungulate, roughly matching the horn morphology of Pseudonovibos spiralis [6]. This illustration sug- Naturwissenschaften 86 (1999) Q Springer-Verlag 1999 18. Surlykke A, Fullard JH (1989) Hearing in the Australian whistling moth, Hecatesia thyridion. Naturwissenschaften 76 : 132–134 19. Conner WE (1987) Ultrasound: its role in the courtship of the arctiid moth, Cycnia tenera. Experientia 43 : 1029–1031 20. Fullard JH, Simmons JA, Saillant PA (1994) Jamming bat echolocation: the dogbane tiger moth Cycnia tenera times its clicks to the terminal attack calls of the big brown bat Eptesicus fuscus. J Exp Biol 194 : 285–298 21. Swihart SL (1967) Hearing in butterflies (Nymphalidae: Heliconius, Ageronia). J Insect Physiol 13 : 469–476 22. Fullard JH, Fenton MB, Furlonger CL (1983) Sensory relationships of moths and bats sampled from two Nearctic sites. Can J Zool 61 : 1752–1757 gests morphological relationships of this species with at least three genera of Bovidae; the gazelles (Procapra), the gorals (Nemorhaedus) and the saigas (Saiga) [6]. Given the scanty information of reliable data on this species, we sequenced a 415-bp fragment of the mitochondrial cytochrome b gene of P. spiralis. DNA from horn fragments of the paratypus B18480 [3] was extracted [10] and PCR amplified with two oligonucleotide primers, L14724 and H15149 [11]. Both strands were automatically sequenced on a LICOR 4000, and all steps, from DNA extraction to sequencing, were independently repeated once, yielding an unambiguous sequence. A phylogenetic analysis was carried out by including the following taxa (Genebank accession numbers in parenthesis): Bison bonasus (Y15005), Bos javanicus (D34636), Bos taurus (V00654, J01394), Bubalus bubalis (D34638), Bubalus mindorensis (D82895), Budorcas taxicolor (U17868), Capra falconeri (D84202), Capra hircus (X56289), Capricornis crispus (D32191), Gazella granti (AF028820), Hemitragus jemlahicus (U17866), Nemorhaedus caudatus (U17861), Ovibos moschatus (U17862), Ovis aries (X56284), Ovis dalli (U17860), Saiga tatarica (U17864). The “maximum-likeli279
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