David D. Yager

Structure, development, and evolution of insect auditory systems

This paper provides an overview of insect peripheral auditory systems focusing on tympanate ears (pressure detectors) and emphasizing research during the last 15 years. The theme throughout is the evolution of hearing in insects. Ears have appeared independently no fewer than 19 times in the class Insecta and are located on various thoracic and abdominal body segments, on legs, on wings, and on mouth parts. All have fundamentally similar structures—a tympanum backed by a tracheal sac and a tympanal chordotonal organ—though they vary widely in size, ancillary structures, and number of chordotonal sensilla. Novel ears have recently been discovered in praying mantids, two families of beetles, and two families of flies. The tachinid flies are especially notable because they use a previously unknown mechanism for sound localization. Developmental and comparative studies have identified the evolutionary precursors of the tympanal chordotonal organs in several insects; they are uniformly chordotonal proprioceptors. Tympanate species fall into clusters determined by which of the embryologically defined chordotonal organ groups in each body segment served as precursor for the tympanal organ. This suggests that the many appearances of hearing could arise from changes in a small number of developmental modules. The nature of those developmental changes that lead to a functional insect ear is not yet known. Microsc. Res. Tech. 47:380–400, 1999.

UNDERWATER ACOUSTIC COMMUNICATION IN THE AFRICAN PIPID FROG XENOPUS BOREALIS

ABSTRACT The totally aquatic African pipid frog Xenopus borealis produces a range of acoustic signals underwater at night. The repertoire of males in heightened reproductive condition consists of three call types. All of the calls are composed of the same impulsive, click-like components. The clicks have a rise-time of 0.5 msec, a duration of 2–5 msec, and most of their energy concentrated at 2600 Hz with a secondary peak at 1100 Hz. The sound pressure levels average 109 dB SPL at 1 meter. The advertisement call is characterized by interclick intervals of 300–600 msec (depending on temperature) and very low coefficients of variation—3%-10%. Phonotaxis experiments confirm that it is effective in attracting females. The approach call, produced when swimming toward or clasping another frog, has interclick intervals averaging 105 msec. Males show pronounced agonistic behavior accompanied by series of clicks with interclick intervals averaging 43 msec. Unreceptive females sometimes produce a very weak release ...

Predator detection and evasion by flying insects

Echolocating bats detect prey using ultrasonic pulses, and many nocturnally flying insects effectively detect and evade these predators through sensitive ultrasonic hearing. Many eared insects can use the intensity of the predator-generated ultrasound and the stereotyped progression of bat echolocation pulse rate to assess risk level. Effective responses can vary from gentle turns away from the threat (low risk) to sudden random flight and dives (highest risk). Recent research with eared moths shows that males will balance immediate bat predation risk against reproductive opportunity as judged by the strength and quality of conspecific pheromones present. Ultrasound exposure may, in fact, bias such decisions for up to 24 hours through plasticity in the CNS olfactory system. However, brain processing of ultrasonic stimuli to yield adaptive prey behaviors remains largely unstudied, so possible mechanisms are not known.

Characterization of auditory afferents in the tiger beetle,Cicindela marutha Dow

We have identified a nerve carrying auditory afferents and characterized their physiological responses in the tiger beetle, Cicindela marutha.1.The tympana are located at the lateral margins of the first abdominal tergum. The nerve carrying the tympanal afferents is a branch of the dorsal root from the first abdominal ganglion.2.Both male and female auditory afferent responses are sharply tuned to 30 kHz with sensitivities of 50–55 dB SPL.3.The auditory afferents show little adaptation and accurately code the temporal characteristics of the stimulus with the limit of a resolution of 6–10 ms.4.The difference in threshold between contralateral and ipsilateral afferents for lateral stimuli is greatest at 30 kHz and is at least 10–15 dB.5.Ablation studies indicate that the floppy membrane in the anterolateral corner of the tympanum is crucial for transduction while the medial portion of the tympanum is less important.6.The tiger beetle and acridid (locust and grasshopper) ears have evolved independently from homologous peripheral structures. The neural precursor of the tympanal organs in both animals is likely the pleural chordotonal organ of the first abdominal segment.

Behavioral responses of big brown bats to dives by praying mantises

SUMMARY Insectivorous echolocating bats face a formidable array of defenses employed by their airborne prey. One such insect defense is the ultrasound-triggered dive, which is a sudden, rapid drop in altitude, sometimes all the way to the ground. Although many previous studies have investigated the dynamics of such dives and their effect on insect survival rate, there has been little work on how bats may adapt to such an insect defense employed in the middle of pursuit. In this study we investigated how big brown bats (Eptesicus fuscus) adjust their pursuit strategy when flying praying mantises (Parasphendale agrionina) execute evasive, ultrasound-triggered dives. Although the mantis dive occasionally forced the bat to completely abort its chase (25% trials), in a number of cases (75% trials) the bat followed the mantis into the dive. In such cases the bat kept its sonar beam locked onto the target and maneuvered to maintain the same time efficient strategy it adopted during level flight pursuit, though it was ultimately defeated by the dive. This study suggests that although the mantis dive can be effective in evading the bat, it does not always deter the bat from continuing pursuit and, given enough altitude, the bat can potentially capture diving prey using the same flight strategy it employs to intercept prey in level flight.

Serially homologous ears perform frequency range fractionation in the praying mantis, Creobroter (Mantodea, Hymenopodidae)

Unlike most praying mantises that have a single region of auditory sensitivity, species in the genus Creobroter have equally sensitive hearing at 2–4 and at 25–50 kHz and and are relatively insensitivity at 10–15 kHz — they have a W-shaped audiogram. Ultrasonic sensitivity originates from an auditory organ in the ventral midline of the metathorax that closely resembles the ear of other mantises. Ablation experiments demonstrate that low frequency sensitivity derives from a serially homologous mesothoracic auditory organ. Extracellular recordings suggest that these two ears operate largely, if not entirely, independently of one another in the thorax. The low frequency response has a longer latency, more action potentials per stimulus, and different patterns of change with increasing SPL than the high frequency response. Separate interneurons mediate responses in the two frequency ranges, but our evidence suggests that they are two serially homologous sets of cells. Neither auditory organ shows any physiological evidence of directional sensitivity. Ultrasound triggers a set of behaviors in flying hymenopodid mantises much like those in other mantises, but the behavioral significance of low frequency hearing in these animals is still unknown.

Wind generated by an attacking bat: anemometric measurements and detection by the praying mantis cercal system.

SUMMARY The wind-sensitive cercal system, well-known for mediating terrestrial escape responses, may also mediate insect aerial bat-avoidance responses triggered by wind generated by the approaching bat. One crucial question is whether enough time exists between detection and capture for the insect to perform a successful evasive maneuver. A previous study estimated this time to be 16 ms, based on cockroach behavioral latencies and a prediction for the detection time derived from a simulated predator moving toward a simulated prey. However, the detection time may be underestimated since both the simulated predator and prey lacked certain characteristics present in the natural situation. In the present study, actual detection times are measured by recording from wind-sensitive interneurons of a tethered praying mantis that serves as the target for a flying, attacking bat. Furthermore, using hot-wire anemometry, we describe and quantify the wind generated by an attacking bat. Anemometer measurements revealed that the velocity of the bat-generated wind consistently peaks early with a high acceleration component (an important parameter for triggering wind-mediated terrestrial responses). The physiological recordings determined that the mantis cercal system detected an approaching bat 74 ms before contact, which would provide the insect with 36 ms to perform a maneuver before capture. This should be sufficient time for the mantis to respond. Although it probably would not have time for a full response that completely evades the bat, even a partial response might alter the mantids trajectory enough to cause the bat to mishandle the insect, allowing it to escape.

Broad versus narrow auditory tuning and corresponding bat‐evasive flight behaviour in praying mantids

Most praying mantids possess a single tympanal ear located in the ventral midline between the metathoracic legs. The auditory system is generally most sensitive to ultrasound in the 25–50 kHz range. Flying males exhibit a short-latency, stereotyped, multi-component response to ultrasound that allows them to escape from attacking bats. This study describes a small subset of species that differs in three major respects from the majority of mantis species: (1) their auditory tuning is 1.5–2 times broader; (2) they are sensitive to frequencies above 60 kHz (up to 130 kHz in some species) with thresholds as low or lower than at 25–50 kHz; (3) the behavioural response of the broadly tuned (BT) species includes 10–50 times more flight cessations and can be far less stereotyped, i.e. more ‘evitable’, than that of narrowly tuned (NT) species. However, BT species do not differ from NT species in overall sensitivity. Two species from one subfamily, the Amelinae (family Mantidae), stand out because they are among the least sensitive of any hearing mantids so far tested. Although the two amelines differ from one another in tuning curve shape, they are both more broadly tuned than most mantids. The occurrence of BT species does not follow any obvious phylogenetic pattern; they are patchily distributed among the mantis families, and both BT and NT species can be found in the same subfamily or tribe. We suggest that BT species are responding to a shared ecological pressure. Based on their tuning, the nature of their behavioural response, and their geographic distribution, we hypothesize that high duty cycle (HDC) bats (Rhinolophidae and Hipposideridae) pose a special danger to BT mantids in addition to the threat that all flying mantids face from the more common and widely distributed low duty cycle (LDC) bats.

Nymphal development of the auditory system in the praying mantis Hierodula membranacea Burmeister (Dictyoptera, Mantidae)

Like other praying mantises, Hierodula membranacea has a single midline ear on the ventral surface of the metathorax. The ear comprises a deep groove with two tympana forming the walls. A tympanal organ on each side contains 30–40 scolopophorous sensillae with axons that terminate in the metathoracic ganglion in neuropil that does not match the auditory neuropil of other insects.

Ontogeny and phylogeny of the cyclopean mantis ear

Many praying mantises have a well‐developed auditory sense mediated by a single, midline ear that hears only ultrasound. Hearing appears gradually in praying mantis nymphs. The neural elements of the peripheral auditory system are in place at hatching. The tympanum is represented only by a small slit and the ear components face posteriorly. The adult medial orientation is achieved by progressive rotation of the walls and broadening of the slit into a membrane. Increasing auditory sensitivity corresponds to the progressive development of impedance‐matching tympanal air sacs. There are four major patterns of auditory structure and function among the 2000 mantis species. (1) Most mantises have a single ear and good ultrasonic hearing. (2) In a third of the species males have a functional ear, but females do not. (3) Mantises of one subfamily have not one, but two ears. The ears are serial homologs that hear in entirely different frequency ranges. (4) A few groups of mantises are deaf and have ‘‘ears’’ almost...