Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-21T21:04:08.731Z Has data issue: false hasContentIssue false

Signal strength, timing, and self-deafening: the evolution of echolocation in bats

Published online by Cambridge University Press:  08 February 2016

M. B. Fenton
Affiliation:
Department of Biology, York University, North York, Ontario, M3J 1P3, Canada
D. Audet
Affiliation:
Departement de biologie, Universite de Sherbrooke, Sherbrooke, Quebec, J1K 2R1, Canada
M. K. Obrist
Affiliation:
Swiss Federal Institute for Forest, Snow, and Landscape Research, CH-8903 Birmensdorf, Switzerland
J. Rydell
Affiliation:
Department of Zoology, University of Aberdeen, Aberdeen AB9 2TN, United Kingdom

Abstract

We propose that the ancestors of bats were small, nocturnal, sylvatic gliders that used echolocation for general orientation. Their echolocation calls were short, low intensity, broadband clicks, which translated into a very short operational range. In the lineage that gave rise to bats, a switch to stronger, tonal signals permitted the use of echolocation to detect, track, and assess flying insects in subcanopy settings. We propose that these animals hunted from perches and used echolocation to detect, track, and assess flying insects, which they attacked while gliding. In this way, the perfection of echolocation for hunting preceded the appearance of flapping flight, which marked the emergence of bats. Flapping flight had appeared by the Eocene when at least eight families are known from the fossil record. Stronger signals and adaptations to minimize self-deafening were central to the perfection of echolocation for locating flying prey. Echolocation constituted a key innovation that permitted the evolution and radiation of bats. At the same time, however, its short effective range imposed a major constraint on the size of bats. This constraint is associated with flight speed and the very small time intervals from detection of, and contact with a flying target. Gleaning and high duty cycle echolocation are two derived approaches to hunting prey in cluttered situations, places where echoes from background and other objects arrive before or at the same time as echoes from prey. Both had appeared by the Eocene.

Type
Research Article
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Anderson, M. E., and Racey, P. A. 1993. Discrimination between fluttering and nonfluttering moths by brown long-eared bats, Plecotus auritus. Animal Behaviour 46:11511155.CrossRefGoogle Scholar
Au, W. W. L. 1993. The sonar of dolphins. Springer, New York.CrossRefGoogle Scholar
Barclay, R. M. R. 1991. Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. Journal of Animal Ecology 60:165178.CrossRefGoogle Scholar
Barclay, R. M. R., and Brigham, R. M. 1991. Prey detection, dietary niche breadth, and body size in bats: why are aerial insectivorous bats so small? American Naturalist 137:693703.Google Scholar
Bell, G. P. 1982. Behavioral and ecological aspects of gleaning by a desert insectivorous bat, Antrozous pallidus (Chiroptera: Vespertilionidae). Behavioral Ecology and Sociobiology 10:217223.CrossRefGoogle Scholar
Bell, G. P. 1985. The sensory basis of prey location by the California leaf-nosed bat Macrotus californicus (Chiroptera: Phyllostomidae). Behavioral Ecology and Sociobiology 16:343347.CrossRefGoogle Scholar
Bell, G. P., and Fenton, M. B. 1984. The use of Doppler-shifted echoes as a flutter detection and clutter rejection system: the echolocation and feeding behavior of Hipposideros ruber (Chiroptera: Hipposideridae). Behavioral Ecology and Sociobiology 15:109114.CrossRefGoogle Scholar
Buchler, E. R. 1976. The use of echolocation by the wandering shrew, Sorex vagrans. Animal Behaviour 29:428432.CrossRefGoogle Scholar
Campbell, K. A., and Suthers, R. A. 1988. Predictive tracking of horizontally moving targets by the fishing bat, Noctilio leporinus. Pp. 501506in Nachtigall, P. E. and Moore, P. W. B., eds. Animal sonar: processes and performance. Plenum, New York.CrossRefGoogle Scholar
Caple, G., Balda, R. P., and Willis, W. R. 1983. The physics of leaping animals and the evolution of preflight. American Naturalist 121:455467.CrossRefGoogle Scholar
Casseday, J. H., and Covey, E. 1992. Frequency tuning properties of neurons in the inferior colliculus of an FM bat. Journal of Comparative Physiology A319:3450.Google Scholar
Coles, R. B., Guppy, A., Anderson, M. E., and Schlegel, P. 1989. Frequency sensitivity and directional hearing in the gleaning bat, Plecotus auritus (Linnaeus 1758). Journal of Comparative Physiology A165:269280.CrossRefGoogle Scholar
Dear, S. P., Simmons, J. A., and Fritz, J. 1993. A possible neuronal basis for representation of acoustic scenes in auditory cortex of the big brown bat. Nature (London) 364:620623.CrossRefGoogle ScholarPubMed
Faure, P. A., Fullard, J. H., and Dawson, J. W. 1993. The gleaning attacks of the northern long-eared bat, Myotis septentrionalis, are relatively inaudible to moths. Journal of Experimental Biology 178:173189.CrossRefGoogle ScholarPubMed
Fenton, M. B. 1974. The role of echolocation in the evolution of bats. American Naturalist 108:386388.CrossRefGoogle Scholar
Fenton, M. B. 1984. Echolocation: implications for ecology and evolution of bats. The Quarterly Review of Biology 59:3353.CrossRefGoogle Scholar
Fenton, M. B. 1990. The foraging behaviour and ecology of animal-eating bats. Canadian Journal of Zoology 68:411422.CrossRefGoogle Scholar
Fenton, M. B., Acharya, L., Audet, D., Hickey, M. B. C., Merriman, C., Obrist, M. K., Syme, D. M., and Adkins, B. 1992. Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruption in the Neotropics. Biotropica 24:440446.CrossRefGoogle Scholar
Fiedler, J. 1979. Prey catching with and without echolocation in the Indian false vampire bat (Megaderma lyra). Behavioral Ecology and Sociobiology 6:155160.CrossRefGoogle Scholar
Fuzessery, Z. M., Buttenhoff, P., Andres, B., and Kennedy, J. M. 1993. Passive sound localization by the pallid bat (Antrozous p. pallidus). Journal of Comparative Physiology A171:767777.CrossRefGoogle Scholar
Griffin, D. R. 1958. Listening in the dark. Yale University Press, New Haven.Google Scholar
Griffin, D. R., and Simmons, J. A. 1974. Echolocation of insects by horseshoe bats. Nature (London) 250:731732.CrossRefGoogle Scholar
Habersetzer, J. 1981. Adaptive echolocation sounds in the bat Rhinopoma hardwickei: a field study. Journal of Comparative Physiology A144:559566.CrossRefGoogle Scholar
Habersetzer, J., and Storch, G. 1989. Ecology and echolocation of the Eocene Messel bats. Pp. 213233in Hanak, V., Horacek, I. and Gaisler, J., eds. European bat research 1987. Charles University Press, Praha, Czechoslovakia.Google Scholar
Hall, L. S., and Richards, G. C. 1979. Bats of eastern Australia. Queensland Museum Booklet no. 12.Google Scholar
Henson, O. W. Jr., Schuller, G., and Vataer, M. 1985. A comparative study of the physiological properties of the inner ear in Doppler shift compensating bats (Rhinolophus rouxi and Pteronotus parnellii). Journal of Comparative Physiology A157:587607.CrossRefGoogle Scholar
Honeycutt, R. L., and Adkins, R. M. 1993. Higher level systematics of eutherian mammals: an assessment of molecular characters and phylogenetic hypotheses. Annual Review of Ecology and Systematics 24:279305.CrossRefGoogle Scholar
Jen, P. H-S., and Suga, N. 1976. Coordinated activities of middle ear and laryngeal muscles in echolocating bats. Science 191:950952.CrossRefGoogle ScholarPubMed
Jepsen, G. L. 1970. Bat origins and evolution. Pp. 164in Wimsatt, W. A., ed. Biology of bats, Vol. 1. Academic Press, New York.Google Scholar
Jones, G. 1990. Prey selection by the greater horseshoe bat (Rhinolopohus ferrumequinum): optimal foraging by echolocation? Journal of Animal Ecology 59:587602.CrossRefGoogle Scholar
Jones, G., and Rayner, J. M. V. 1989. Foraging behavior and echolocation of wild horseshoe bats, Rhinolophus ferrumequinum and Rhinolophus hipposideros (Chiroptera: Rhinolophidae). Behavioral Ecology and Sociobiology 25:183191.CrossRefGoogle Scholar
Kalko, E., and Schnitzler, H-U. 1993. Plasticity of echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection. Behavioral Ecology and Sociobiology 33:415428.CrossRefGoogle Scholar
Kick, S. A. 1982. Target-detection by the echolocating bat, Eptesicus fuscus. Journal of Comparative Physiology A145:431435.CrossRefGoogle Scholar
Kingdon, J. 1974. Mammals of East Africa, an atlas of evolution, Vol. IIA. Academic Press, London.Google Scholar
Krull, D. 1992. Jagdverthalten und Echoortung bei Antrozous pallidus (Chiroptera: Vespertilionidae). Ph.d. Dissertation. Fakultat fur Biologie der Ludwig-Maximilians Universitat, Munchen.Google Scholar
Lancaster, W. C. 1993. Saving energy by flying: the economy of echolocation in flight. Bat Research News 33:23.Google Scholar
Lawrence, B. D., and Simmons, J. A. 1982. Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocating bats. Journal of the Acoustical Society of America 71:585590.CrossRefGoogle Scholar
Linares, O. J. 1986. Murciélagos de Venezuela. Cuadernos Lagoven. Caracas.Google Scholar
Link, A., Marimuthu, G., and Neuweiler, G. 1986. Movement as a specific stimulus for prey catching behavior in rhinolopid and hipposiderid bats. Journal of Comparative Physiology A159:403413.CrossRefGoogle Scholar
McKitrick, M. C. 1993. Phylogenetic constraint in evolutionary theory: has it any explanatory power? Annual Review of Ecology and Systematics 24:307330.CrossRefGoogle Scholar
Nachtigall, P. E., and Moore, P. W. B., eds. 1988. Animal sonar: processes and performance. Plenum Press, New York.CrossRefGoogle Scholar
Neuweiler, G. 1990. Auditory adaptations for prey capture in echolocating bats. Physiological Reviews 70:615641.CrossRefGoogle ScholarPubMed
Neuweiler, G., and Fenton, M. B. 1988. Behavior and foraging of echolocating bats. Pp. 536549in Nachtigall, P. E. and Moore, P. W. B., eds. Animal sonar: processes and performance. Plenum, New York.Google Scholar
Neuweiler, G., Bruns, V., and Schuller, G. 1980. Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system. Journal of the Acoustic Society of America 68:741753.CrossRefGoogle Scholar
Neuweiler, G., Singh, S., and Sripathi, K. 1984. Audiograms of a south Indian bat community. Journal of Comparative Physiology A154:133142.CrossRefGoogle Scholar
Neuweiler, G., Metzner, W., Heilman, U., Rubsamen, R., Eckrich, M., and Costa, H. H. 1987. Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Behavioral Ecology and Sociobiology 20:5367.CrossRefGoogle Scholar
Novacek, M. J. 1985. Evidence for echolocation for the oldest known bats. Nature (London) 315:140141.CrossRefGoogle ScholarPubMed
Norberg, U. M. 1985. Evolution of vertebrate flight: an aerodynamic model for the transition from gliding to flapping flight. American Naturalist 126:303327.CrossRefGoogle Scholar
Norberg, U. M. 1989. Ecological determinants of bat wing shape and echolocation call structure with implications for some fossil bats. Pp. 197211in Hanak, V., Horacek, I. and Gaisler, J., eds, European bat research 1987. Charles University Press, Praha, Czechoslovakia.Google Scholar
Norberg, U. M. 1990. Vertebrate flight. Springer, Berlin.CrossRefGoogle Scholar
Norberg, U. M., and Fenton, M. B. 1988. Carnivorous bats? Biological Journal of the Linnean Society 33:383394.CrossRefGoogle Scholar
Nowak, R. M. 1991. Walker's mammals of the world, 5th ed.Johns Hopkins University Press, Baltimore.Google Scholar
Obrist, M., Fenton, M. B., Eger, J. L., and Schlegel, P. A. 1993. What ears do for bats: a comparative study of pinna sound pressure transformation in Chiroptera. Journal of Experimental Biology 180:119152.CrossRefGoogle Scholar
Payne, J., Francis, C. M., and Phillipps, K. 1985. A field guide to the mammals of Borneo. World Wildlife Fund Malaysia, Kuala Lumpur.Google Scholar
Pettigrew, J. D.In press. Flying primates: crashed or crashed through? The case for diphyly. In Racey, P. A. and Swift, S. M., eds. Recent advances in bat biology. Oxford University Press.Google Scholar
Pollak, G. D. 1993. Some comments on the proposed perception of phase and nanosecond time disparities by echolocating bats. Journal of Comparative Physiology A172:523531.CrossRefGoogle Scholar
Pollak, G. D., and Casseday, J. H. 1989. The neural basis of echolocation in bats. Springer, Berlin.CrossRefGoogle Scholar
Pye, J. D. 1968. How insects hear. Nature (London) 218:797.CrossRefGoogle Scholar
Reeve, H. K., and Sherman, P. W. 1993. Adaptation and the goals of evolutionary research. Quarterly Review of Biology 68:132.CrossRefGoogle Scholar
Rubsamen, R., Neuweiler, G., and Sripathi, K. 1988. Comparative collicular tonotopy in two bat species adapted to movement detection, Hipposideros speoris and Megaderma lyra. Journal of Comparative Physiology A163:271285.CrossRefGoogle Scholar
Rydell, J. 1989. Food habits of northern (Eptesicus nilssoni) and brown long-eared (Plecotus auritus) bats in Sweden. Holarctic Ecology 12:1620.Google Scholar
Schmidt, S. 1988. Evidence for a spectral basis of texture perception in bat sonar. Nature (London) 331:617619.CrossRefGoogle ScholarPubMed
Schnitzler, H-U. 1987. Echoes of fluttering insects: information for echolocating bats. Pp. 226243in Fenton, M. B., Racey, P. A. and Rayner, J. M. V., eds. Recent advances in the study of bats. Cambridge University Press.Google Scholar
Schnitzler, H-U., and Henson, O. W. Jr. 1980. Performance of airborne animal sonar systems. I. Microchiroptera. Pp. 109182in Busnel, R.-G. and Fish, J. F., eds. Animal sonar systems. Plenum, New York.CrossRefGoogle Scholar
Schuller, G., and Pollak, G. 1976. Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats: evidence of an acoustic fovea. Journal of Comparative Physiology A132:4754.Google Scholar
Schumm, A., Krull, D., and Neuweiler, G. 1991. Echolocation in the notch-eared bat, Myotis emarginatus. Behavioral Ecology and Sociobiology 28:255261.CrossRefGoogle Scholar
Siegel, S. 1956. Nonparametric statistics. McGraw-Hill, New York.Google Scholar
Simmons, J. A. 1993. Evidence for perception of fine echo delay by phase by the FM bat Eptesicus fuscus. Journal of Comparative Physiology A172:533548.CrossRefGoogle Scholar
Simmons, J. A., and Stein, R. A. 1980. Acoustic imaging in bat sonar: echolocation signals and the evolution of echolocation. Journal of Comparative Physiology A135:6184.CrossRefGoogle Scholar
Simmons, J. A., Kick, S. A., and Lawrence, B. D. 1984. Echolocation and hearing in the mouse-tailed bat, Rhinopoma hardwickei: acoustic evolution of echolocation in bats. Journal of Comparative Physiology A154:347356.CrossRefGoogle Scholar
Simmons, J. A., Saillant, P. A., and Dear, S. P. 1992. Through a bat's ear. Institute of Electrical, and Electronic Engineers Spectrum March:4648.Google Scholar
Smith, J. D. 1972. Systematics of the chiropteran family Mormoopidae. University of Kansas Museum of Natural History, Miscellaneous Publication, no. 56:1132.Google Scholar
Smith, J. D. 1976. Chiropteran evolution. Pp. 4169in Baker, R. J., Jones, J. K. Jr., and Carter, D. C., eds. Biology of bats of the new world family Phyllostomatidae. Special Publication, The Museum. Texas Tech University Press, Lubbock.Google Scholar
Speakman, J. R. 1993. The evolution of echolocation for predation. Pp. 3963in Dunston, N. and Gorman, M. L., eds. Mammals as predators. Oxford University Press.CrossRefGoogle Scholar
Speakman, J. R., and Racey, P. A. 1991. No cost of echolocation for bats in flight. Nature (London) 350:421423.CrossRefGoogle ScholarPubMed
Stucky, R. K., and McKenna, M. C. 1993. Mammalia. Pp. 739771in Benton, M. J., ed. The fossil record. Chapman & Hall, London.Google Scholar
Suga, N. 1978. Specialization of the auditory system for reception and processing of species specific sounds. Federation Proceedings 37:23422354.Google ScholarPubMed
Sum, Y. W., and Menne, D. 1988. Discrimination of fluttering targets by the FM-bat Pipistrellus stenopterus? Journal of Comparative Physiology A163:349354.CrossRefGoogle Scholar
Surlykke, A., Miller, L. A., Møhl, B., Andersen, B. B., Christensen-Dalsgaard, J., and Jogensen, M. B. 1993. Echolocation in two very small bats from Thailand: Craseonycteris thonglongyai and Myotis siligorensis. Behavioral Ecology and Sociobiology 33:112.CrossRefGoogle Scholar
Turtle, M. D., and Ryan, M. J. 1981. Bat predation and the evolution of frog vocalizations in the neotropics. Science 214:677678.Google Scholar
Tuttle, M. D., Ryan, M. J., and Belwood, J. J. 1985. Acoustical resource partitioning by two species of phyllostomid bats (Trachops cirrhosus and Tonatia sylvicola). Animal Behaviour 33:13691371.CrossRefGoogle Scholar
Vater, M. 1987. Narrow-band frequency analysis in bats. Pp. 200225in Fenton, M. B., Racey, P. A. and Rayner, J. M. V., eds. Recent advances in the study of bats. Cambridge University Press.Google Scholar
Vaughan, T. A. 1977. Foraging behaviour of the giant leaf-nosed bat (Hipposideros commersoni). Journal of East African Wildlife 15:237249.CrossRefGoogle Scholar