The adaptive function of tiger moth clicks against echolocating bats: an experimental and synthetic approach

Abstract

The authors apologise for this mistake and any inconvenience caused to readers. 4689The evolutionary arms race between insectivorous echolocating bats and moths has long fascinated biologists (Roeder, 1967;Fullard, 1998;Miller and Surlykke, 2001;Jones and Rydell, 2003;Waters, 2003). The primary purpose of the moth's simple ear -to detect bat echolocation callshas made this a particularly useful model for study (Fullard, 1988;Waters, 2003). The ears of moths have evolved as a direct result of selective pressure by bats; they are broadly tuned to the frequency ranges of sympatric insectivorous bat communities and inform the central nervous system to initiate erratic flight behaviours and/or stop flying (Fullard, 1988;Hoy et al., 1989). As part of the acoustic startle response, some species of tiger moths (family Arctiidae) produce clicks using thoracic tymbals that appear to deter attacks from nearby bats (Dunning and Roeder, 1965; Hirstov and Conner, 2005a). Many arctiid species contain sequestered or synthesized defensive chemicals (Rothschild et al., 1970;Weller et al., 1999;Nishida, 2002) unpalatable to a variety of predators, including bats (Dunning, 1968;Coutts et al., 1973;Goss, 1979;Boppré, 1990;Hristov and Conner, 2005b).The clicks of arctiid moths have been proposed to function as acoustic aposematic signals (Blest et al., 1963;Dunning and Roeder, 1965;Dunning, 1968;Hristov and Conner, 2005a) and as signals that interfere with information processing facilitating escape, by startling the bat (deimatism) and/or jamming echolocation (Bates and Fenton, 1990;Fullard et al., 1979Fullard et al., , 1994Miller, 1991;Masters and Raver, 1996;Tougaard et al., 1998Tougaard et al., , 2004. These functional hypotheses are not mutually exclusive although they are often portrayed as such (e.g. Surlykke and Miller, 1985;Fullard et al., 1994;Waters, 2003; Hristov and Miller, 2005a). Until recently (Hristov and Conner, 2005a), all laboratory studies had used (1) synthetic bat echolocation calls and stationary moths, (2) synthetic arctiid clicks and stationary bats or (3) free-flying bats capturing mealworms while synthetic clicks were broadcast >1·m away from the prey trajectory (see Waters, 2003 and We studied the efficiency and effects of the multiple sensory cues of tiger moths on echolocating bats. We used the northern long-eared bat, Myotis septentrionalis, a purported moth specialist that takes surface-bound prey (gleaning) and airborne prey (aerial hawking), and the dogbane tiger moth, Cycnia tenera, an eared species unpalatable to bats that possesses conspicuous colouration and sound-producing organs (tymbals). This is the first study to investigate the interaction of tiger moths and wild-caught bats under conditions mimicking those found in nature and to demand the use of both aerial hawking and gleaning strategies by bats. Further, it is the first to report spectrograms of the sounds produced by tiger moths while under aerial attack by echolocating bats. During both aerial hawking and gleaning trials, all muted C...

Tempo and mode of antibat ultrasound production and sonar jamming in the diverse hawkmoth radiation

“…In contrast, Cycnia tenera, a tiger moth that may possess limited jamming ability, has a duty cycle of ∼8% (8,12), and the sound-producing tiger moth Euchaetes egle, which appears to be unable to jam sonar, has a duty cycle of only ∼3% (12). Duty cycle, or sound per unit time, is likely related to jamming efficacy (35,36).…”

“…Of the nearly 140,000 moth species (4), more than half may possess ultrasonically sensitive bat-detecting ears (5). Moth ears are connected to neuronal circuits that steer the animals away from bats at low sonar call intensities, trigger aerobatic evasive behaviors-such as directed turns, loops, spirals, and power dives (3)-and elicit ultrasound production at high sonar intensities (6)(7)(8). Ultrasonic ears are known to have independently evolved at least 18 times in seven insect orders (9) and possibly 10 or more times in Lepidoptera (5).…”

Sonar jamming in the field: effectiveness and behavior of a unique prey defense

“…Depending on whether a species is chemically defended and the amount of sound it produces, moth clicks serve as acoustic aposematic (Hristov and Conner, 2005a;Hristov and Conner, 2005b;Ratcliffe and Fullard, 2005), mimetic (Barber and Conner, 2007;Barber et al, 2009) or sonar-jamming signals (Corcoran et al, 2009;Corcoran et al, 2010;Corcoran et al, 2011;Conner and Corcoran, 2012). In some cases these defenses may be combined; for example, a small degree of sonar jamming may enhance bat learning of aposematic signals (Ratcliffe and Fullard, 2005).…”

Variability in Sensory Ecology: Expanding the Bridge Between Physiology and Evolutionary Biology

“…While bats emit highintensity ultrasonic pulses and use echoes to locate and track flying prey, some Arctiid moths can direct ultrasonic clicks back at the echolocating bat. The function of these clicks remains unclear; they may serve either to warn the bat that the moth is distasteful (Spangler 1988) or to jam its echolocating system (Fullard et al 1979), or perhaps both (Ratcliffe and Fullard 2005). In more general terms, the remarkable diversity in insect ears suggests that predator-prey interactions between bats and insects have played a key role in the evolution of insect auditory systems (Hoy and Robert 1996).…”