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The Relationship Between Echolocation-Call Frequency and Moth Predation of a Tropical Bat Fauna

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425 The relationship between echolocation-call frequency and moth predation of a tropical bat fauna C.R. Pavey, C.J. Burwell, and D.J. Milne Abstract: The allotonic frequency hypothesis proposes that the proportion of eared moths in the diet should be highest in bats whose echolocation calls are dominated by frequencies outside the optimum hearing range of moths i.e., <20 and >60 kHz. The hypothesis was tested on an ecologically diverse bat assemblage in northern tropical Australia that consisted of 23 species (5 families, 14 genera). Peak frequency of signals of bats within the echolocation assemblage ranged from 19.8 to 157 kHz but was greatest between 20 and 50 kHz. A strong positive relationship existed between peak call frequency and percentage of moths in the diet for a sample of 16 bats from the assemblage representing 13 genera (R2 = 0.54, p = 0.001). The relationship remained strong when the three species with low-intensity calls were excluded. When the two species with high duty cycle, constant-frequency signals were removed, the relationship was weaker but still significant. In contrast to previous research, eared moths constituted only 54% of moth captures in light traps at bat foraging grounds, and eared moths were significantly larger than non-eared individuals. These results show that the pattern of moth predation by tropical bats is similar to that already established for bat faunas in subtropi- cal and temperate regions. Résumé : L’hypothèse de la fréquence allotonique veut que la proportion de papillons de nuit à organes tympaniques soit maximale dans le régime alimentaire des chauves-souris dont les appels d’écholocation sont dominés par des fré- quences hors du registre d’audition optimal des papillons, c.-à-d. <20 et >60 kHz. Nous avons évalué cette hypothèse sur un peuplement écologiquement diversifié de chauves-souris dans le nord de l’Australie tropicale qui comprend 23 espèces (5 familles, 14 genres). Les pics des fréquences des signaux des chauves-souris dans l’ensemble d’écholocation varient de 19,8 à 157 kHz, mais le maximum se situe entre 20 et 50 kHz. Il existe une forte relation positive entre le pic des fréquences des appels et le pourcentage de papillons de nuit dans le régime alimentaire dans un échantillon de 16 chauves-souris du peuplement et appartenant à 13 genres (R2 = 0,54, p = 0,001). La relation demeure forte, même lorsqu’on retire les trois espèces qui ont des appels de faible intensité. Lorsqu’on retire les deux espèces qui possèdent des signaux de cycle actif de haute fréquence constante, la relation est affaiblie, mais reste encore significative. Con- trairement à certaines études antérieures, les papillons de nuit à organes tympaniques ne représentent que 54 % des captures de papillons de nuit dans les pièges lumineux aux sites d’alimentation des chauves-souris et les papillons avec organes tympaniques sont significativement plus grands que les individus sans organes tympaniques. Ces résultats mon- trent que le patron de prédation par les chauves-souris tropicales est semblable à ceux qui ont déjà été établis pour les peuplements de chauves-souris des régions subtropicales et tempérées. [Traduit par la Rédaction] Pavey et al. 433 Introduction 1998; Miller and Surlykke 2001). Almost one-half of the world’s 200 000 species of moths belong to families that Hearing has evolved in a range of insect groups including possess ears and can hear ultrasound (Scoble 1992; Fullard the Neuroptera, Orthoptera, Dictyoptera, Coleoptera, and 1998). These 92 000 species of moths have been shown to Lepidoptera (Miller and Surlykke 2001). Among moths, ul- be abundant at bat foraging grounds across the globe. Spe- trasonic hearing functions primarily as a defence against the cies from eared families contribute ≥85% of species richness echolocation calls of foraging bats (Spangler 1988; Fullard of Macrolepidoptera in light-trap catches at sites in Europe, North America, Africa, and Australia, in environments rang- Received 12 October 2005. Accepted 17 January 2006. ing from temperate woodland to upland tropical rain forest Published on the NRC Research Press Web site at http:// (Fenton and Fullard 1979; Usher and Keiller 1998; Kitching cjz.nrc.ca on 17 March 2006. et al. 2000; Schoeman and Jacobs 2003). C.R. Pavey.1 Biodiversity Conservation, Parks and Wildlife The hearing of eared moths is most sensitive to frequen- Service, P.O. Box 1120, Alice Springs, 0871, Australia. cies between 20 and 50 kHz, a range that coincides with the C.J. Burwell. Queensland Museum, P.O. Box 3300, South peak call frequencies of most echolocating bats (Fullard Brisbane, 4101, Australia. 1987, 1998). Moths from regions with high bat diversity, D.J. Milne. Biodiversity Conservation, Parks and Wildlife where the bandwidth of echolocation frequencies is greater, Service and Tropical Savannas Cooperative Research Centre, show increased sensitivity at high and low frequencies com- P.O. Box 496, Palmerston, 0831, Australia. pared with moths from less diverse bat environments 1Corresponding author (e-mail: [email protected]). (Fullard 1982). However, although some moths can hear Can. J. Zool. 84: 425–433 (2006) doi:10.1139/Z06-010 © 2006 NRC Canada 426 Can. J. Zool. Vol. 84, 2006 over a wider range of frequencies, sensitivity falls off gradu- Study site ally above 55 kHz (Fullard 1987). Although non-eared The study region is the tropics of the Northern Territory moths have evolved a suite of behavioural responses to re- of Australia, north of the 18°S parallel. This area is domi- duce bat predation (Soutar and Fullard 2004 and references nated by eucalypt savanna woodland and encompasses therein), the ability to hear combined with a variety of de- approximately 340 000 km2. Maximum mean weekly tem- fensive flight maneouvres enables eared moths to increase perature ranges between 32 and 39 °C and mean annual rain- their chances of avoiding bat predation by up to 40% fall between 360 and 1720 mm. Rainfall is highly seasonal, (Roeder 1967; Acharya and Fenton 1999). almost all precipitation occurring from November to April. Some echolocating bats are able to avoid detection by Topographic relief is relatively low; maximum elevation is eared moths either by emitting low-intensity calls that are al- 553 m. most imperceptible to moths or by calling at frequencies above and below the optimum hearing range of moths Echolocation frequency (Fullard 1998). Such frequencies are referred to as allotonic Data on the structure and frequencies of search-phase (i.e., frequencies are mismatched between moths and bats). echolocation signals of bats were obtained from 53 sites in a The allotonic frequency hypothesis proposes that the propor- variety of environments throughout the study area. Voucher tion of eared moths in the diet will be highest in bats whose calls were taken from free-flying bats in the field. echolocation calls are dominated by frequencies outside the We recorded calls of free-flying bats using a hand-held optimum hearing range of moths, i.e., <20 and >60 kHz Anabat® II bat detector (Titley Electronics, Ballina, N.S.W.) (Fenton and Fullard 1979). connected to an Optimus CTR-115 tape recorder (Sony The hypothesis is supported by research showing a high Chrome UX tapes). The person recording the calls usually proportion of moths in the diet of bat species calling at sat on the roof of a stationary 4WD vehicle at this time. allotonic frequencies (e.g., Rydell and Arlettaz 1994) and When a bat was heard through the Anabat® speaker, the tape by a positive relationship between peak frequency of echo- recorder was manually switched on via the Anabat® tape location calls and quantity of moths incorporated in the diet switch. A spotlight (12 V, 100 W) was switched on to locate for bat assemblages with frequencies >20 kHz. The latter ev- the bat and better track its movements. On some occasions idence is available for meta-analyses of bats with specific the bat was then collected. Each specimen was identified and echolocation strategies (Jones 1992) and call frequencies numbered. We also recorded calls of bats that were released (Bogdanowicz et al. 1999), and for foraging guilds (Pavey after capture in mist nets and harp traps. and Burwell 1998) and local bat communities in temperate The Anabat® system uses frequency division and zero- and subtropical regions (Jacobs 2000; Schoeman and Jacobs crossing analysis to construct frequency/time graphs from 2003). Although some results must be treated with caution detected signals (de Oliveira 1998). The frequency range of because data were collected in different ways at different the microphone on the detector is 10–200 kHz with a peak times (Schoeman and Jacobs 2003), overall the findings sug- frequency response at 50 kHz. The system responds to the gest that the allotonic frequency hypothesis is valid for a dominant harmonic, regardless of which one it is. If another wide range of bat assemblages. However, the hypothesis has harmonic is strongly represented, the system will repeatedly not been tested for bat faunas in the tropics, a major short- jump between the two harmonics and neither will be accu- coming given that bat diversity is concentrated in tropical re- rately represented. This situation rarely occurs (de Oliveira gions (Findley 1993) and, consequently, the echolocation 1998). In this study, peak call frequency for high duty cycle assemblages experienced by moths in the tropics are ex- (i.e., constant frequency) bats is defined as the maximum tremely diverse (e.g., Fullard 1998). frequency of the call, whereas for low duty cycle species it Here we report the results of a test of the allotonic fre- is defined as the frequency at the end or at the flattest por- quency hypothesis in the tropics of the Northern Territory of tion of the call (refer to Fig.
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