How Some Insects Detect and Avoid Being Eaten by Bats: Tactics and Countertactics of Prey and Predator.

EVOLUTIONARILY SPEAKING, INSECTS HAVE RESPONDED TO SELECTIVE PRESSURE FROM BATS WITH NEW EVASIVE MECHANISMS, AND THESE VERY RESPONSES IN TURN PUT PRESSURE ON BATS TO "IMPROVE" THEIR TACTICS

Some insects have evolved audition and evasive behaviors in response to selective pressure from bats, and other insects were preadapted to detecting ultrasonic signals. Some bats have evolved in turn, improving the range or resolution of sonar signals and serendipitously making them less detectable by insects. In other words, there is a kind of evolutionary escalation going on between bats and insects. Our aim with this review is to present the complex interactions between echolocating bats and insects with bat-detecting ears and show how these interactions may be advantageous for predator or prey. To document our examples, we cite mostly newer studies and reviews in which the reader can find references to original works.

Insects occupied all terrestrial habitats at least 300 million years ago, long before bats appeared in the Eocene, about 50 million years ago. Ears have appeared independently 19 times in the class Insecta. In the period before bats, ears and complex acoustical behaviors appeared independently in at least seven orders of insects (Hoy et al. 1989, Robert et al. 1992) Yager 1999). Antibat tactics, which must have appeared in insects since the Eocene, are now known in members of four orders: Lepidoptera (moths and nocturnal butterflies), Orthoptera (crickets), Dictyoptera (praying mantids), and Neuroptera (green lacewings), and possibly also in the Diptera (flies) and Coleoptera (beetles).

Insect tympanal organs, or ears, consist basically of an external, thin membrane (the tympanum) and associated internal air sacs, or tracheae. The auditory (sensory) cells attach to the tympanum or to an internal membrane (Yager 1999). Tympanal organs of most modern tympanate insects respond to a wide band of frequencies extending well into the ultrasonic range (above 20 kHz), as was probably true for pre-Eocene tympanate insects as well. Tympanate insects are physically small animals that can produce high-frequency sounds more efficiently; hence, high frequencies are used by many insects for acoustical communication between conspecifics. Consequently, many sonorous insects were preadapted to the evolution of bats (Hoy 1992).

According to one possible scenario, a vast larder of nocturnal, flying insects awaited exploitation, and a flying mammal, the microchiropteran bat, was one successful exploiter. Echolocation, or biosonar, was a prerequisite for success in darkness, and even the first nocturnal bats probably used it (see Hoy 1992). Most of the nearly 700 microchiropteran bat species eat insects that they detect using biosonar (Schnitzler and Kalko 2001). However, bat biosonar has two major disadvantages: attenuation and forewarning.

The frequencies used by echolocating bats range generally from 20 kHz to 100 kHz, with some outliers using frequencies below 10 kHz or above 200 kHz. Higher frequencies improve resolution, but they attenuate at a greater rate (Surlykke 1988) and the detection distance is reduced accordingly. The source level is the sound pressure level (SPL relative to 20 [micro]Pa), in decibels (dB), measured 10 cm in front of the bat's mouth. A bat using a source level of 110 dB at 20 kHz could detect the echo from an object the size of a moth at more than 5 m. Detection would occur at no more than 2.4 m if the bat used 100 kHz (Surlykke 1988). From the insects' perspective, bats advertise their presence with the ultrasonic pulses used to stroboscopically probe the environment. Thus, insects are forewarned if they can hear ultrasound. This coincidentally exerts considerable selection pressure against those insects that either cannot hear or do not react (Miller 1982).

Thus, the stage was set in the Eocene for an evolutionary escalation between bats and insects. Evasive behaviors in existing tympanate insects (presumably crickets, locusts, and mantids) probably appeared in response to selection pressure by bat predation (Hoy 1992). The same selection pressure generated new auditory and motor mechanisms in presumably earless insects (green lacewings and moths). Bats, too, could have developed countermeasures, for example, shifting signals out of the prey's hearing range (Fenton and Fullard 1981) or modifying hunting behaviors (Miller and Olesen 1979).