3808 The Journal of Experimental Biology 211, 3808-3815 Published by The Company of Biologists 2008 doi:10.1242/jeb.023978 Surviving cave bats: auditory and behavioural defences in the Australian noctuid moth, Speiredonia spectans James H. Fullard1,*, Matt E. Jackson1, David S. Jacobs2, Chris R. Pavey3 and Chris J. Burwell4,5 1Department of Biology, University of Toronto, 3359 Mississauga Road, Mississauga, Ontario, Canada L5L 1C6, 2Department of Zoology, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa, 3Biodiversity Conservation Division, Department of Natural Resources, Environment and the Arts, P.O. Box 1120, Alice Springs, 0871 Australia, 4Queensland Museum, P.O. Box 3300, South Brisbane, 4101 Australia and 5Griffith School of Environment, Griffith University, Nathan, 4111 Australia *Author for correspondence (e-mail: [email protected]) Accepted 13 October 2008 SUMMARY The Australian noctuid moth, Speiredonia spectans shares its subterranean day roosts (caves and abandoned mines) with insectivorous bats, some of which prey upon it. The capacity of this moth to survive is assumed to arise from its ability to listen for the batsʼ echolocation calls and take evasive action; however, the auditory characteristics of this moth or any tropically distributed Australian moth have never been examined. We investigated the ears of S. spectans and determined that they are among the most sensitive ever described for a noctuid moth. Using playbacks of cave-recorded bats, we determined that S. spectans is able to detect most of the calls of two co-habiting bats, Rhinolophus megaphyllus and Miniopterus australis, whose echolocation calls are dominated by frequencies ranging from 60 to 79 kHz. Video-recorded observations of this roost site show that S. spectans adjusts its flight activity to avoid bats but this defence may delay the normal emergence of the moths and leave some ʻpinned downʼ in the roosts for the entire night. At a different day roost, we observed the auditory responses of one moth to the exceptionally high echolocation frequencies (150–160 kHz) of the bat Hipposideros ater and determined that S. spectans is unable to detect most of its calls. We suggest that this auditory constraint, in addition to the greater flight manoeuvrability of H. ater, renders S. spectans vulnerable to predation by this bat to the point of excluding the moth from day roosts where the bat occurs. Key words: bat echolocation, moth ears, predator, prey, sensory ecology. INTRODUCTION Granny’s Cloak noctuid moth, Speiredonia spectans Guenée, in Many moths possess ears that enable them to detect the echolocation subterranean day roosts with insectivorous bats, including the calls of hunting insectivorous bats and avoid predation (Roeder, Eastern horseshoe bat, Rhinolophus megaphyllus Gray and the 1967). This now classic neuroethological story was originally set Little Bent-winged bat, Miniopterus australis Tomes (Pavey and in the open skies where free-flying bats locate and attack their prey Burwell, 2005). S. spectans lives in large numbers with these bats by what is known as aerial hawking. Further studies suggested that [Pavey and Burwell counted 1090 live moths in six sites (Pavey substrate-gleaning bats who find their prey by orienting towards the and Burwell, 2005)] but in contrast to Roeder and Fenton (Roeder prey’s incidental sounds (e.g. wing fanning) may be at an advantage and Fenton, 1973), they found moth wings on the floors of the in capturing eared moths owing to the reduced intensity as well as roosts implying that co-habiting bats prey upon S. spectans. A to the higher frequency of their calls (Fenton and Fullard, 1979; report of cave-foraging in bats by Lacki and Ladeur described Faure et al., 1990; Faure et al., 1993). Roeder and Fenton introduced the Big-eared bat, Corynorhinus rafinesquii (Lesson) capturing another potential arena for the arms-race between these two moths in a cave in Kentucky, USA by both aerially hawking them opponents, viz. subterranean roosts such as caves and mines in which and by gleaning them from the surface of the cave (Lacki and bats and moths co-habit (Roeder and Fenton, 1973). In a North Ladeur, 2001). Pavey and Burwell suggested that in spite of the American mine, the noctuid moth, Scoliopteryx libatrix (Linnaeus) risk of predation, S. spectans co-habits with bats by being able overwinters with hibernating bats [Myotis spp and Eptesicus fuscus to detect their echolocation calls and escaping to the walls of the (Beauvois)] and although it can hear the calls of these bats, it does day roosts (Pavey and Burwell, 2005). The echolocation calls of not react behaviourally to them. This apparent anomaly was R. megaphyllyus and M. australis contain frequencies of explained by the possibility that this moth inhibits its normal 60–70kHz (Jones and Corben, 1993; Fenton et al., 1999; Reinhold avoidance flight response to ultrasound to remain in the relative et al., 2001), which although not frequency-matched (syntonic) safety of the roosts, protected from abiotic (e.g. freezing) and biotic are theoretically within the bandwidth of sensitivity of tropical dangers (e.g. predation by birds). This study also reported that bats moths (Fullard, 1988) and should be detectable by S. spectans. did not appear to eat the moths, perhaps because of the physical By contrast, subterranean day roosts occupied by the Dusky inability of aerially hawking bats to attack insects in the narrow leafnosed-bat (Hipposideros ater Templeton) contained S. confines of the mines. spectans wings but no live moths (Pavey and Burwell, 2005), Pavey and Burwell further developed this story of ‘lambs laying suggesting that the very high frequency of this bat’s echolocation down with lions’ by describing the co-habitation of the Australian calls [>150 kHz (Fenton, 1982; Crome and Richards, 1988)] THE JOURNAL OF EXPERIMENTAL BIOLOGY Defences in a cave-dwelling moth 3809 renders them less audible (allotonic) to the moths and allows this sympatry with S. spectans, distributions of Australian bats were bat to prey more heavily on S. spectans. taken from maps in Churchill (Churchill, 1998). The purpose of the present study was to examine the auditory capability of S. spectans to address the hypothesis proposed by Pavey Bat echolocation and Burwell (Pavey and Burwell, 2005) that this moth can hear the We characterized the acoustic environment of the mines with respect echolocation calls of R. megaphyllus and M. australis but not those to bat echolocation by remotely recording echolocation calls of bats of H. ater in underground roosts. In addition, we examine the as they flew in the mines. We used an ultrasonic microphone hypothesis that S. spectans avoids roost predation by adjusting its (Avisoft condenser microphone type CM16; frequency response, flight activity to minimize encounters with bats by testing the 10–200kHz) and digitizer (Avisoft UltrasoundGate 416, Avisoft prediction that there will be an absence of flight overlap between Bioacoustics, Berlin, Germany; sampling rate, 16bit, 500kHz) to the cave exits of the moths and the bats. record the calls and then analyzed sequences of calls using BatSound Pro software (v. 3.20, Pettersson Elektronik AB, Upsala, Sweden). MATERIALS AND METHODS Although we cannot ascertain the actual number of individuals used Bat/moth flight activity in our acoustic analyses, we believe that the massive exodus of the This study was conducted in three abandoned mines in coastal bats from the caves at night effectively rules out the possibility of Queensland, Australia (Fig.1), two of which were located at Camp pseudoreplication. Only one sequence from each file was selected Mountain, west of Brisbane, in sub-tropical Queensland and for measurement and these sequences were chosen on the following contained the bats, Rhinolophus megaphyllus and Miniopterus criteria: (1) only sequences with calls with a high signal-to-noise australis. The other mine was at Bramston Beach, south of Cairns, ratio (i.e. oscilloscope signal from the bat was at least three times in the wet tropics of north Queensland and at the time of our study, stronger than the background noise as displayed on a linear time- contained the bats R. megaphyllus, H. ater and Hipposideros voltage window) were analyzed; (2) only calls that were not semoni Matschie [H. semoni is a rare species (van Dyck and Strahan, saturated were analyzed (Fenton et al., 2001); (3) only calls that did 2008) whose 108kHz calls are readily distinguishable from those not overlap with other calls were analyzed. For each call in a of H. ater; however, this species was recorded only once in the sequence, we measured the peak frequency (PF) from the power Bramston Beach site and is, therefore, not considered further in this spectrum (1024-point FFT), call duration, inter-pulse interval (IPI) study]. Bats and moths were observed in the Camp Mountain sites and inter-onset interval (time from the onset of one call to the onset by illuminating the mine shafts with a near infra-red (NIR) light of the next call in the sequence) from the oscillogram, and minimum source (Extreme CCTV Surveillance Systems, model EX12LED, frequency of the frequency modulated (FM) tails for R. megaphyllus Scottsdale, AZ, USA) at wavelengths of 850–940nm, to which and H. ater from the spectrogram. Minimum frequency (which can Lepidoptera are insensitive (Horridge, 1977), and videotaping them be calculated by subtracting the bandwidth from peak frequency in with a NIR-sensitive camera (Swann Communications Pty., Table1) for M. australis was taken as the value –20dB below peak Richmond, Victoria, Australia) as they flew in the mine. frequency whereas for R. megaphyllus and H. ater, this was taken The distribution of S. spectans was established by collating as the lowest frequency of the FM component of the call as measured collection locality data from preserved specimens in the following from the BatSound Pro spectrogram (time/frequency plot, 512-point Australian insect collections: Australian National Insect Collection, FFT, resolution=19.36ms per plot).