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).

Avoidance behaviors

Preadaptation. Preexisting auditory systems in insects may have been preadaptively sensitive to bat echolocation. Tympanate insects that were normally diurnal may also have become active at night. Crickets, locusts, and inantids are considered here because they were probably some of the earliest insects with hearing and they are mostly active during the day, but often fly (migrate or disperse) at twilight and at night. However, all crepuscular and nocturnal insects are potential prey for bats.

Crickets. The most intensively studied insect auditory system is that of field crickets (Figure la, left). The majority of these studies concern intraspecific communication. The tibia of each foreleg contains an ear (Figure la, middle). For example the maximum sensitivity of the cricket Gryllus bimaculatus occurs at about 5 kHz as measured lectrophysiologically from the auditory nerve. This is also the frequency of the calling song. However, the ear is sensitive to sound frequencies up to 100 kHz at least.

Popov and Shuvalov (1977) first reported that dispersing crickets avoid being hunted by bats. Since then Ron Hoy at Cornell, Andrej Popov in St. Petersburg, and their colleagues have documented avoidance behavior in several species of crickets both behaviorally and neurophysiologically (see Hoy et al. 1989). Crickets in stationary flight steer away from the source of ultrasound (negative phonotaxis), with the most effective frequencies lying between about 10 kHz and 80 kHz (Figure la, right). An interneuron in Teleogryllus oceanicus (Int 1) initiates evasive behavior (Hoy et al. 1989), and its homologue in Gryllus bimaculatus ([AN.sub.2]; Popov et al. 1994) presumably does the same. The threshold for [AN.sub.2] at 20 kHz is about 20 dB less than that of the behavior (Figure la, right), meaning that the neural response is more sensitive than the behavior. Some mole crickets hear ultrasound, in part with special neuronal pathways, and free-flying crickets show avoidance to batlike sounds (Mason et al. 1998).

Bush crickets (Figure lb, left), like field crickets, have their ears and associated acoustic tracheae in the tibia of the forelegs (Figure 1b, middle). Some species communicate entirely in the ultrasonic range. Many bush crickets can hear bats, but few seem to react to bat echolocation. However, the bush cricket, Neoconocephalus ensiger, shows an acoustic startle response during tethered flight in the laboratory (Faure and Hoy 2000). When the insects hear intense katlile sounds with frequencies from 15 kHz to at least 60 kHz (Figure lb, right), they dive. However, they exhibit no directionality with respect to the sound source, even though bush crickets have directional hearing. A large prothoracic interneuron, the T-neuron, participates in mediating the behavior (Faure and Hoy 2000). The T-neuron is most sensitive to frequencies higher than those of the calling song (13 kHz peak frequency) for the species. The threshold is about 50 dB less than that of the behavior at 20 kHz (Figure lb, right).

Locusts. Another primarily diurnal orthopteran, the locust Locusta migratoria (Figure 1c, left), has a pair of general purpose abdominal ears (Figure 1c, middle) that are well studied anatomically, physically, and physiologically. However, the role of hearing in the life of this locust remains poorly understood. One function of hearing may be to mediate negative phonotaxis in response to batlike signals, although to our knowledge there are no published reports of locusts responding to bats. A locust in stationary flight rudders with its abdomen and increases the wingbeat frequency, both of which produce turning in the direction opposite to the sound source (Robert 1989). Negative phonotactic behavior occurs only at frequencies above 10 kHz (Figure 1c, right). Romer et al. (1988) found interneurons sensitive to high frequencies that selectively receive input from auditory afferents. These interneurons control head and abdominal movements and are candidates for controlling negative phonotaxis. Figure 1c (right) shows the auditory sensitivity of one of these (SN-5).

Praying mantids. Praying mantids (Figure ld, left) are primarily diurnal, but many make dispersal…