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Vibration and animal communication: A review
American Zoologist, Nov 2001 by Hill, Peggy S M
Vibration and Animal Communication: A Review1
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SYNOPSIS. Vibration through the substrate has likely been important to animals as a channel of communication for millions of years, but our awareness of vibration as biologically relevant information has a history of only the last 30 yr. Morphologists know that the jaw mechanism of early amphibians allowed them to perceive vibration through the substrate as their large heads lay on the ground. Although the exact mechanism of vibration production and the precise nature of the wave produced are not always understood, recent technical advances have given answers to increasingly sophisticated questions about how animals send and receive signals through the substrate. Some of us have been forced to explore the use of vibration when all other attempts to manipulate animals in the field have failed, while others began to think about vibration to explain some of the puzzling behaviors of species they were studying in other contexts. It has thus become clear that the use of vibration in animal communication is much more widespread than previously thought. We now know that vibration provides information used in predator-prey interactions, recruitment to food, mate choice, intrasexual competition and maternal/brood social interactions in a range of animals from insects to elephants.
Studies of vibration in animal communication cast a small shadow in comparison with investigations into airborne signals and their interpretation. Yet, vibration perception as a sensory channel clearly predates that of the vertebrate ear mechanism. Extinct amphibians were able to detect vibrations through their jaw in contact with the ground, and conduction through the quadrate bone of the jaw to the inner ear via bony tissue (Hildebrand, 1995). A reduced hyomandibula associated with the quadrate in a fish's visceral skull evolved to form the ear ossicle called the stapes, or columella (Hildebrand, 1995). Even today, tetrapods that are in direct contact with the substrate over much of their body surface, such as non-anuran amphibians and reptiles, lack a tympanum and middle ear cavity. Caecilians, urodeles and some anurans, snakes, amphisbaenians and some lizards have a stapes, which may be attached to the shoulder girdle or skin, and are well suited to detecting low frequency vibrations from the substrate (Hildebrand, 1995). Thus, long before the temporo-mandibular joint that gives humans so much pain freed up the articular and quadrate bones for new duty as ear ossicles, tetrapods had an apparatus in place for detecting substrate vibrations.
Massive ear ossicles are seen in large mammals that acquire acoustic information through bone-conducted vibration at the expense of auditory acuity at higher frequencies (Reuter et al., 1998). For example, true seals have ossicles weighing from 160 to 320 mg, while the horse's ossicles weigh 74 mg, less than half that of the smaller seals. Elephants have massive ossicles with total weight in the Indian elephant of approximately 650 mg (Reuter et al., 1998). Modem-day golden moles (family Chrysochloridae) have specialized structures for hearing low-frequency sounds emitted by their prey, including a complex hyoid apparatus in contact with their tympanic bulla, and many have massive ear ossicles (Mayer et al., 1995). Frogs that are exceptionally sensitive to seismic stimuli appear to use the saccule of the ear to detect these vibrations (Narins and Lewis, 1985), and sandfish lizards that use vibration to locate prey also have a very large saccule (Hetherington, 1989).
Processing of vibrational signals by animats does not require a traditional hearing pathway. Somato-sensory mechanisms are also well known (Kalmring, 1985): mechanoreceptors in sensillar hairs (Zachariassen, 1977; Kristensen and Zachariassen, 1980) and subgenual organs (Rupprecht, 1968; Bell, 1980a; Hutchings and Lewis, 1983; Kalmring et al., 1997) of insects, basitarsal compound-slit sensilla of scorpions (Brownell and Farley, 1979a, b), and tricobothria and metatarsal lyriform organs of spiders (Barth, 1982). Snakes have simple nerve endings for vibration perception (Proske, 1969) and Herbst corpuscles in birds (Dorward and McIntyre, 1971) and Pacinian corpuscles in Eutherian mammals (Hunt, 1961; Caine and Pallis, 1966) allow for perception of vibrations. Gregory et al. (1986) found similar lamellated corpuscles in the legs of macropod marsupials, which suggests that these animals can detect ground-to-bone vibration produced by approaching predators. The blind subterranean mole rat, Spalax ehrenbergi, processes sensory information from vibrations produced by its head-banging neighbors through a somatosensory channel that is independent of the auditory mechanism (Nevo, 1990; Nevo et al., 1991; Klauer et al., 1997). Yet, they also lay their jaws against their burrow walls in a behavior that appears to enhance bony conduction of vibrations to their inner ears (Rado et al., 1989, 1998). Whether or not both systems operate simultaneously is still under discussion (Rado et al., 1998).
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