The praying mantis ear is not only in a strange place on the body, but it also has an unusual structure. It is basically a deep slit, and there is an eardrum (tympanum) in each wall. This means that the two tympana are very close (0.1-0.2 mm) and face each other. The shape of the tympana and of the air space between them is complex, so it has been difficult to predict any advantages or disadvantages of having an ear built this way. However, one of our Honors undergraduates showed indirectly using neurophysiological recordings that the slit increases the sensitivity of the system, but does not alter its frequency selectivity. One obvious disadvantage of have a single ear in the middle of the body is that mantises cannot tel what direction a sound comes from.

An ear is useless unless the vibration of the tympana can be changed into neural signals for processing in the CNS. We don't yet know how this is accomplished in the mantis ear—it's one of the major puzzles we are tackling. There are two sensory structures attached to each slit wall; one of them has 35-45 neurons, the other 2 neurons. Although neither of them looks superficially like a particularly good candidate, we know that one or both of them sends information about sounds (and other stimuli) to the CNS. With the help of a colleague in Denmark, we hope to unravel the mystery using laser vibrometry and neurphysiological recordings.

By placing electrodes in the nervous system, we have established that most mantis species hear only ultrasound (30-50 kHz) and that they are almost certainly tone deaf. Any information besides the simple presence of ultrasound must come from the loudness and/or the temporal pattern (rhythm) of the sound.

Praying mantises, like all insects, have relatively few neurons in their CNS. The neurons can be recognized as individuals that look the same and perform the same function in every mantis. We know about at least 6 bilaterally symmetrical pairs of neurons that process auditory information, and we have intensively studied one of these, called 501-T3. This neuron has a very large axon that goes to the head, so it is easy to record the activity of 501 using extracellular electrodes. We now know that 501 is not very good at reproducing temporal patterns, for instance, and does not respond well to frequncy sweeps, but it gets information about intensity to the brain very quickly and is certainly a key player in auditory behavior.

It is possible to learn even more about the auditory processing by placing an electrode inside a neuron while presenting sounds of different types. This is the only reliable way to study the auditory neurons with small axons or no axons at all. Because we can inject dye into the cell, this technique also provides us with portraits of the neurons.

So far we have focused primarily on understanding how sounds are processed, but more recently graduate student Aaron Cook began looking at how the CNS starts and regulates the complex evasive response. Insects have small brains ('ganglia') in each body segment that control activities in that segment, so the first question was whether the ganglion controlled the behavior locally without requiring descending commands from the brain. Aaron found that the overall behavior of decapitated mantises was normal is most respects (obviously they couldn't eat or see), but ultrasound did not trigger the normal behavioral response. Therefore, the brain is necessary for the evasive behavior.

There are about 2000 species of mantis. They are all totally predatory and have big eyes, but otherwise there is a tremendous diversity of sizes, shapes, and lifestyles. We want to know how much diversity in ear structure and function also occurs among all these species.

The answer is a resounding 'Yes'—we have discovered six patterns of hearing among the mantises, and there may be others. Briefly:

1. The normal ultrasonic hearing by the cyclopean ear.

2. Primitively deaf species. These lineages never evolved ears.

3. Auditory sexual dimorphism in which males hear well, but the females of the same species are deaf.

4. Ultra-high frequency hearing up to 120 kHz in some species.

5. Nymphal deafness. Baby mantises gradually acquire their hearing during the second half of their development.

6. Auditory Bicyclops. These mantises have evolved two independent, serially homologous auditory systems, i.e. both midline ears. One ear hears only ultrasound and the other listens exclusively to 3-5 kHz.

Most mantises hear only ultrasound, and the dominant source of ultrasound in the environment is the echolocation cries of hunting bats. We have demonstrated both in the lab and in the field that flying mantises can escape from an attacking bat as long as it can hear. Deaf mantises or hearing mantises that couldn't hear the frequencies used by a particular bat species were invariably caught and eaten.

The reason that hearing mantises escape is clear: they respond to the bat's ultrasound with a complex aerial maneuver that leads to a spiraling power dive. The bats are not able to turn as tightly, and they can't dive as close to the ground as the mantises without crashing. These experiments continue in a large indoor flight room where we can stage bat-mantis encounters and film them with high-speed video cameras.

Grad student Aaron Cook showed that the brain is necessary for the escape behavior, and also used high-speed video to look at the relative timing of the individual movements that make up the response. Several undergraduates in the Integrative Neuroscience Summer Intern Program have worked together to record electromyograms from the muscles involved giving even more precise timing information.

Graduate student Jeff Triblehorn has recently succeeded in recording the activity in interneuron 501 during an attack by a flying bat in the flight room. He positioned an electrode so that it could record action potentials in 501 while the mantis was hanging in the center of the room. A bat flying in the room detected the mantis and began its stereotyped attack sequence. Besides the obvious flight toward the mantis, this consists of a changing pattern of echolocation clicks culminating in a 'buzz' just before contact. 501 proved very good at reporting the pattern of echolocation clicks to the brain up until the buzz, but then fell silent for the last 200-300 msec of the mantis' life. This is a very unexpected result that we don't yet understand. Perhaps this interneuron triggers the escape behavior, but then passes control to other neurons or even other sensory sensory systems. Jeff is hard at work trying to find the answer and learn more about the descending control of the evasive maneuvers.

There are no mantis fossils or mantises in amber that tell us anything about the evolution of their ear, so we must rely on indirect evidence. The comparative studies mentioned above have allowed us to make an 'auditory phylogeny' for the mantises. So little is known, however, about mantis evolution in general that this exercise yields more questions than answers.

Our comaparative approach to understanding the changes in the body and the CNS that allow the acquisition of a new type of information (airborne sound, in this case) has broadened to include two other insects. Cockroaches have proven very valuable since they are the mantis' closest relatives and do not have an ear (don't waste your money on ultrasonic roach repellers …). Thus they provide detailed 'before and after' comparisons. Thanks to the work of several undergraduate students in the lab, we know, for instance, that cockroaches have a nerve identical to the auditory nerve in mantises, and they even have a 501-T3 interneuron. Since there is no ear, we are very curious to know exactly what this 'pre-auditory' system does.

We also study tiger beetles, an insect much like the mantis in its ecological niche—a highly visual, diurnal, top-of-the-food-pyramid predator with a night life. Hayward Spangler at the USDA in Tuscon first discovered tiger beetle ears, and we since have collaborated on several studies. TBs have fairly conventional ears in a very unconventional location: the top of the abdomen under the wings. Although we don't yet know much about how the auditory works, we do know that TBs only hear ultrasound. They also have a complex in-flight response that looks likea bat evasion strategy, with a twist. In addition to changes in flight path, they click back at the bats.

Evolutionary change requires changes in developmental programs, so we have begun looking closely at ear development in mantises and cockroaches. We are focusing especially on the timing of hormonal signals that control maturation. For instance, grad student Amy Harron succeeded in selectively altering ear development by administering appropriately timed doses of juvenile hormone. These studies are just beginning and hold great promise.

Mantises have evolved the ability to hear, but that is far from the whole story. The hearing must be associated with behaviors that help the animal survive and mate. We have been looking at many species of mantises and tiger beetles from all over the world to find out how widespread the behaviors are, to find out if different species have different auditory behaviors, to see if there are ecological correlates to the presence of the behaviors. We have just begun, but so far we are finding that the auditory behaviors of both insects are extremely widespread geographically and ecologically and that the behaviors don't differ across those ranges. These comparative studies also provide a good excuse for field work in exotic places.