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The Evolution of Echolocation for Predation

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The Evolution of Echolocation for Predation Symp. zool. Soc. Land. (1993) No. 65: 39-63 The evolution of echolocation for predation J. R. SPEAKMAN DepartmentofZoowgy University of Aberdeen Aberdeen AB9 2TN, UK Synopsis Active detection of food items by echolocation has some obvious advantages over passive detection, since it affords independence from ambient light and sound levels. For predatory animals, however, echolocation would also appear to have a significant disadvanrage-i-the echolocation calls might alert prey to the predator's presence. Surprisingly, therefore, all but two of the different groups of vertebrates that have evolved echolocation are predatory. Despite the diversity of predatory taxa in which echolocation has evolved it is still a relatively uncommon form of perception. It has been suggested that a major constraint on the evolution of echolocation is its high energy cost, due to rapid attenuation of sound in air. The cost of producing echolocation calls has been measured in insectivorous bats, whilst hanging at rest. These measures confirm that echolocation is extremely costly. However, bats normally echolocate in flight which also has a high cost. How bats cope with the high cost of echolocation, when it is combined with flight, is therefore of extreme interest. Measures of the energy cost of flight of small echolocating bats ggest that the cost is no greater than that for non-echolocating birds and bats. The son for this apparent economy is that the same muscles which flap the wings also tilate the lungs, and produce the pulse of breath which generates the echolocation For a bat in flight, therefore, the additional cost of echolocating is very low, sr for a bat on the ground, and presumably other terrestrial vertebrates, the cost ry high. The release from the energetic constraint may explain the proliferation cholocation systems amongst flying predators and their paucity amongst trial predators. This model for the evolution of echolocation has some 'cant probiems-s-norably the absence of echolocation amongst predatory birds fruit bats. Possible solutions to these problems include the lack of an advantage iurnal predators and phylogenetic constraints in both the ventilatory and tual systems of these animals. ~Jversity of echolocators al systems can be divided into two fundamentally different Copyrlghr © 1993 lhe Zoological SocietJ of London All r-ightsof reproduction in any form reserved 40 evolution of echolocation for predation 41 categories. There are passive systems, where the animal passively receive Ie 1. Major taxonomic groups in which echolocation has evolved, their inputs of sensory information. This is the system that we use, and it is also cipal prey, and an indication of whether echolocation is used for prey detection used by most other animals. Alternatively, an animal may actively sense its dentation environment. Using this latter type of system the animal does not wai Detection of passively until there is an input of sensory information, but rather create Prey prey Reference that input itself. Two different active sensory systems have evolved. The fir method involves the production of bio-electricity. By generating a potential mals Cetacea-toothed whales Fish Yes Norris et al. (1961) difference between one end of its body and the other, the animal produces and dolphins an electric field around itself. When objects, which differ in their resistivity Phocidae-e-seals Fish ?Yes Renouf & Davis (1982) Sales & Pye (1974) to the environment, come into this field, they affect the flow of current, and Tenrecidae-i-renrecs Invertebrates ? Soriddae-shrew Invertebrates ?No Forsman & Malmquist can therefore be actively detected by the animal. Since air is a good electrical (1988) insulator this method can only evolve in water, and it has been found i Rodenria-s-rat Omnivorous No J. W. Anderson (1954) No Roberts (1975) several species of fish (e.g. Gymnarchus spp.: Machin & Lissmann 196 Megachiropteran bats Fruit -Rousettus which live mostly in turbid water. Probably the most widespread and w< Microchiropreran bats Diverse diets Griffin (1958) known method of active perception, however, is the system of produci including: sounds and perceiving the environment by interpreting the returnin Insects Yes Fish Yes echoes---ealled echolocation (Griffin 1958). Small mammals Sometimes Active systems of perception have one major advantage over passivi Amphibia ?Yes systems: they allow the animal a substantial degree of independence fro Reptiles ?Yes Fruit/Nectar ?No variations in the amount of passive information that is available from t environment. A useful analogy in this context is to consider the advantag Insects No Novick (1959) of possessing a torch when walking around in complete darkness. T Insects No Griffin (1953) independence from the level of ambient illumination that a torch confers is clear advantage. Despite the benefits of active systems of perception, a serious disadvantage atory animals, exploiting a wide variety of different prey species may be imposed on predators which employ the system to detect prey: the ugh not necessarily using echolocation to detect their prey). Most of signal generated by the predator might alert the prey to the predator' redators that have evolved echolocation feed either on fish or on presence and allow it to avoid capture (Suthers & Wenstrup 1987) ts. There are very few echolocating predators that feed on mammals, Retaining the analogy of using a torch, in a group of people at night, the on¢ es or amphibians, and none that feed on birds. In part these trends who carries the torch is not only the one who can see most easily, but also ct the temporal separation of the activity times of different groups. For the one that is most easily seen. Furthermore, predatory animals must often pie, the birds are almost exclusively diurnal. Probably echolocation detect their prey from relatively large distances. Studies of the attenuation of not evolved in diurnal predators that prey on birds because possessing the information content of sound signals propagated in air suggest that the location confers little or no advantage on predators that are seeking loss of information increases exponentially as distance over which the sign in daylight, when there is a lot of passive information present (see also is transmitted increases (Griffin 1971; Lawrence & Simmons 1982). Sin below). non-predatory animals can commonly approach their food much m n contrast to the birds, many small mammals and tropical reptiles and closely than predators, there would appear to be a valid argument t phibians are nocturnal. Some of these fall prey to echolocating echolocation should have evolved more frequently amongst non-predato rochiropteran bats. Most nocturnal predatory bats preying on these animals than amongst predators. imals, however, do not use echolocation to search for prey. It is possible Yet examination of the groups of animals where echolocation has evolvi the problem of alerting the prey pf the predator's presence has been an (Table 1) reveals that of the seven major taxa which include species th rtant influence on the evolution of echolocation in predators specializing have evolved echolocation (Sales & Pye 1974), all but two of them, t these groups of animals. Small mammals in particular are very sensitive fruit-bat (Rousettus spp.) and rats (Rattus spp.) are predominant high-frequency sounds, and use ultrasound calls for communication 42 J. R. Speakman The evolution of echolocation for predation 43 (Sales & Pye 1974). Detailed examinations of the behaviours of echolocating bats when feeding on these prey support this hypothesis. Some echolocating The energetic constraint hypothesis bats feed predominantly on small mammals and amphibians, but appear to Dawkins (1986) suggested that the paucity of echolocating species is use echolocation primarily to orientate themselves in the environment. principally a consequence of the very high cost of producing an echolocation Trachops cirrhosus, the New World frog-eating bat, locates its major prey signal of practical use over any effective distance. Suthers & Wenstrup from the singing calls of the males (Tuttle & Ryan 1981), and, although it (1987) also indicated that the energy costs of echolocation might have been may occasionally echolocate during the approach to the prey (Barclay et al. an important factor influencing the secondary reduction in use of 1981) this does not appear to be necessary for successful prey capture. The echolocation in some bats. This high cost normally outweighs the benefit pallid bat (Anthrozous pallidus), which occasionally feeds on small in terms of increased rewards and hence the system is rarely favoured in mammals, relies heavily on passive sound cues to locate its prey (Bell 1982). selective terms. There are several lines of evidence supporting this The secondary reduction in the use of echolocation by bats when feeding on hypothesis. First, a simple consideration of the physics of sound propagation these vertebrate prey, in the wild, strongly suggests that alerting the prey of reveals that a sound signal will decline rapidly in intensity as it spreads out the predator's presence has been an important constraint on the development in the environment. The reflected echo from an object a certain distance of echolocation in the predatory animals which specialize on these prey away will in theory have an intensity that is a function of twice the distance species. In support of this hypothesis, Fiedler (1979) found experimentally to that object squared, if it is perfectly reflected. More often in practice the in the laboratory that the false vampire bat Megaderma lyra would always echo intensity is found to fall as the cube or even fourth power of distance use echolocation to detect dead mice, but reduced its use of echolocation (Morse 1948). Therefore to obtain an echo with sufficient intensity the when presented with live mice as prey, and almost half the approaches to original signal must be very loud. prey were completely silent. This is particularly the case in air, where the conductivity for sound is Echolocation appears to have developed most frequently among predators very poor.
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