Echolocating Bats and Hearing Moths: Who Are the Winners?

Abstract

Predator-prey coevolution does not always involve gradual and parallel morphological changes, as Darwin (1859) anticipated. Among large terrestrial mammals, for example, fossil evidence shows that, over Tertiary time, there has been long periods of near stasis or slow evolution among predators, resulting in considerable adaptive lags in the development of their weapons. Most of the time, the defence or escape mechanisms of the prey animals evolved much faster, which made them relatively immune to predation for long periods, usually until new and more efficient predators arrived by immigration (Bakker 1983). A similar situation may prevail among some insects and their bat predators. Predation pressure from echolocating bats seems to be the principal selective force behind the evolution of tympanate organs (ears) in some nocturnal insects, including many families of moths (Lepidoptera) as well as some lacewings (Neuroptera) and mantises (Dictyoptera). These insect ears are tuned to the acoustic frequencies used by echolocating bats, and registration of sound pulses at these frequencies by the insects normally elicits evasive flight manoeuvers (Roeder 1967, Miller and Olesen 1979, Fullard 1987, Surlykke 1988, Yager et al. 1990). Some moths also emit ultrasonic clicks in response to bat echolocation calls, but the function of such behaviour is still contentious; they may serve as aposematic signals (Dunning 1968, Dunning et al. 1992), they may startle the predator (Bates and Fenton 1990), or they may interfere with bat echolocation (Fullard et al. 1994). In many moths and lacewings, the ears appear to have no other function than to detect approaching bats (Bailey 1991, Fullard and Yack 1993). There is no doubt that moths with ears have an advantage over those without ears when encountering foraging bats. Their chance of surviving an attack is about 40% higher (Roeder 1967, Acharya 1992). Some foraging strategies currently used by insectivorous bats are thought to have evolved through diffuse coevolution in response to the evolution of ears in insects. For example, the relatively fast flying aerial-hawking bats, that search for insects in open air space, require intense echolocation pulses for long-range detection of prey (Barclay and Brigham 1991). Such calls are likely to be easily detected by most tympanate insects, provided the frequencies fall within their hearing range. Therefore, the use of frequencies that fall below or above the insects' best range of hearing by some species of bats may represent such a strategy (Novick 1977, Fenton and Fullard 1979, Fullard 1987, Jones 1992). Likewise, gleaning bats, some of which may use short, broadband echolocation calls of relatively low intensity, or which even may rely entirely on passive listening or vision to find their prey (e.g. Bell 1982, 1985, Anderson and Racey 1991), may also be relatively inconspicuous to tympanate insects (Faure et al. 1990). The interaction between bats and tympanate insects, particularly moths, has served as a textbook example of evolutionary arms races between predators and prey. Hence, it is important to consider the evidence by examination of the available field data. We compare the diet between species of European bats in relation to their foraging strategies and echolocation call frequencies, taking advantage of the fact that a great deal of new data on echolocation and feeding ecology of bats in Europe has accumulated in the last few years in response to recent methodological developments in ultrasonic monitoring and radio telemetry. The frequencies of best hearing in insects presumably correspond to the echolocation call frequencies used by the bats that have imposed the greatest predation pressure on these insects over evolutionary time. Assuming that the tympanate organs provide efficient protection against these bats, their appearance in insects may subsequently have forced the bats to switch to other insect groups, because the profitability of tympanate prey species may have declined drastically relative to those without ears. Therefore, tympanate insects may not necessarily be exploited heavily by these bats at present. Indeed, bat spe-