© 2001 by The Society for Integrative and Comparative Biology
Seismic Signal Use by Fossorial Mammals1
1 Department of Physiological Science, UCLA, 405 Hilgard Avenue, Los Angeles, California 90095
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The subterranean environment is not favorable for the use of vision or the audition of airborne sounds as means of long-distance sensory perception. However, seismic vibrations have been shown to propagate at least an order of magnitude better than airborne sound between the burrow systems of the mole-rat Georychus capensis. The use of the seismic channel for communication underground is well documented for other species of bathyergids, as well as the spalacine mole-rat Nannospalax. It has recently been suggested that the golden mole Eremitalpa granti namibensis may also be sensitive to ground vibrations, in this case used in foraging in its desert habitat.
In this paper, the use of seismic signals among these and other fossorial mammals is reviewed from theoretical, behavioral and anatomical standpoints. The question of whether auditory or somatosensory means are used to detect vibratory signals is examined. Attempts to explain the distribution of seismic sensitivity and communication mechanisms among fossorial mammals are considered. The potential influences of different soil type and digging methods are discussed, and it is proposed that digging mechanisms involving the head might preadapt a fossorial mammal towards the development of seismic sensitivity.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONBEHAVIORAL EVIDENCE FOR THE...AUDITION OR SOMATOSENSATION?ANATOMICAL ADAPTATIONS...DISCUSSIONEVOLUTION OF SEISMIC SENSITIVITYReferences |
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There are several families of mammals that contain members that lead a largely subterranean existence (Nevo, 1979
). The term fossorial is here applied to those species that possess unusual anatomical or physiological adaptations towards burrowing, and that spend a considerable amount of their lives underground. Among the order Rodentia, the fossorial mammals considered here include the pocket gophers (family Geomyidae) and the ctenomyids (family Ctenomyidae) of the Americas, the bathyergid mole-rats (family Bathyergidae) of Africa and the spalacine mole-rats (family Muridae, subfamily Spalacinae) of Eurasia and North Africa. Among the Insectivora, many of the talpid moles (order Insectivora, family Talpidae) of Eurasia and North America are fossorial. The golden moles (family Chrysochloridae), which also are fossorial, have often been included within the Insectivora, although recent molecular studies group these animals within a clade of endemic African mammals (Springer et al., 1997; Stanhope et al., 1998). The only Australian fossorial mammal is the marsupial mole, Notoryctes typhlops (order Notoryctimorphia, family Notoryctidae). These fossorial mammals are generally small, most weighing well under a kilogram. While the fossorial rodents are herbivores, typically feeding on roots and tubers, the talpid moles, golden moles and marsupial mole are largely insectivorous (see Nowak, 1999).
Most fossorial mammals construct permanent tunnel systems, for shelter and often for feeding, and these tunnels may be very elaborate. The energetic cost of burrowing is considerable (Vleck, 1979, 1981), and therefore a network of tunnels represents a valuable resource. Although intraspecific interactions among the many supposedly "solitary" fossorial mammals may be more common than generally supposed (Lacey, 2000), many species are extremely aggressive in defense of their burrows. In order to avoid costly conflicts, neighboring talpid moles avoid conspecifics by foraging in areas of range overlap at different times of the day (Stone and Gorman, 1985). Alternatively, some form of intraspecific communication may be used to warn intruders, or conversely to indicate that an animal is receptive to potential mates and is unlikely to attack during the breeding season. Some bathyergid mole-rats (Heterocephalus and Cryptomys species) are social and live in colonies of related individuals (Bennett and Jarvis, 1988b; Sherman et al., 1991; Bennett et al., 1994), and in these cases intraspecific communication will take on a different role in mediating the often complex social relationships between animals (Lacey et al., 1991; Pepper et al., 1991). In addition, all fossorial mammals presumably would benefit from a means of detecting approaching predators, and perhaps from a means of detecting food items.
Sensory perception among fossorial mammals will be restricted by the nature of the subterranean environment. Chemical signaling and the sense of smell are probably used extensively in fossorial species (see Burda et al., 1990; Francescoli, 2000), but terrestrial mammals all seem to use at least one other sense to gather information about their surroundings without the delay associated with chemical diffusion or the proximity required for touch or taste. Although some fossorial rodents that spend time on the surface may retain a reasonable degree of visual acuity (see review in Francescoli, 2000), vision is of very limited use in a dark tunnel, and the eyes of many other fossorial species are reduced or vestigial (e.g., Sweet, 1906, 1909; Gubbay, 1956; Eloff, 1958; Quilliam, 1966a, b; Hildebrand, 1985; Burda et al., 1990; Cooper et al., 1993; Hetling et al., 2000). It has been proposed that the nasal tentacles of the star-nosed mole Condylura cristata might be used for a form of electroreception underwater (Gould et al., 1993), although this has been disputed (Catania, 1995b). Electrical field detection is highly unlikely in air (Gould et al., 1993), so if present at all, this sensory modality is probably not widespread among fossorial mammals.
The attention of many researchers has naturally turned towards airborne sound as a medium for communication underground, particularly because of the prevalence of vocal communication among fossorial rodents. Nearly all of the fossorial rodents so far studied make vocal communication calls (Francescoli, 2000), the naked mole-rat Heterocephalus making at least seventeen different vocalizations (Pepper et al., 1991), the largest known repertoire of any rodent (Bennett and Faulkes, 2000). The blind mole-rat, Nannospalax, produces six different vocalizations (Capranica et al., 1974) and the bathyergid Cryptomys thirteen (Credner et al., 1997). However, the subterranean environment is not conducive to the propagation of airborne sound. In Nannospalax tunnels, low-frequency sound of around a few hundred Hertz has been shown to travel best, but airborne sound of all frequencies travels very poorly (Heth et al., 1986). There may also be substantial low-frequency background noise in subterranean tunnels (Roberts, 1995, in Wilkins et al., 1999). Perhaps because of these limitations, vocalizations in fossorial species tend to be restricted to low frequencies (below around 10 kHz) and are usually issued when animals are in close proximity to one another (Capranica et al., 1974; Heth et al., 1988; Pepper et al., 1991; Credner et al., 1997). Sensitivity to airborne sound in all fossorial rodents studied to date has been shown to be extremely poor, restricted to low frequencies (as might be expected) but with high thresholds at all frequencies (Bronchti et al., 1989; Heffner and Heffner, 1990, 1992, 1993; Brüchmann and Burda, 1997). Although audition in talpid moles has not been examined in such detail, data suggest that hearing in these animals may be similarly restricted (Aitkin et al., 1982; Konstantinov et al., 1987). Localization of airborne sound sources has also been shown to be very poor in those rodent species studied (Heffner and Heffner, 1990, 1992, 1993). There have been no direct studies of hearing in golden moles or in the marsupial mole.
All the vertebrate species for which vibrational signals have been measured to date have been shown to generate predominantly vertically-polarized surface (Rayleigh) waves (Narins, 2001). For example, these vibrations in the soil, referred to as seismic vibrations, have been shown to travel much better than airborne sound between the tunnels of the mole-rat Georychus (Narins et al., 1992). This suggests that the seismic channel, which may be relatively free of background noise (Frantii et al., 1962), might represent a useful medium for communication among fossorial mammals in general, over longer distances than airborne communication may be possible. Nevo et al. (1991, p. 1259) proposed that the "seismic communication modality may be the major long-distance communication channel in the evolution of...[the mole-rat Nannospalax]...and possibly in subterranean mammals generally." Seismic sensitivity might also be useful for the detection of prey, or for detection of potential predators. This paper reviews the evidence that seismic signals are used by fossorial mammals, and considers the various factors that might lead to the evolution of seismic sensitivity in different groups.
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BEHAVIORAL EVIDENCE FOR THE USE OF SEISMIC SIGNALS BY FOSSORIAL MAMMALS |
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There is considerable behavioral evidence to suggest that certain fossorial mammals do use the seismic channel to glean information about their surroundings. There are many anecdotal reports of fossorial mammals, including talpid moles, mole-rats and golden moles, being sensitive to vibrations, in many cases those made by an observer (Kriszat, 1940
; Copley, 1950; Eloff, 1951; Roberts, 1951; Harrison Matthews, 1952; Herter, 1957; Bateman, 1959; Walker et al., 1975; Kuyper, 1985; Skinner and Smithers, 1990; Catania, 1995b). However, the most extensively studied cases relate to either intraspecific communication or prey detection.
Several species of fossorial rodents use drumming behaviors for conspecific signaling. One example of such a rodent is an African mole-rat in the family Bathyergidae. The Cape mole-rat, Georychus capensis, spends the vast majority of its life underground, alone in its burrow, save for a short period during each breeding season. This monotypic genus appears to be most closely related to two other solitary mole-rat genera, Heliophobius and Bathyergus, and less closely related to the social Cryptomys and Heterocephalus within the Bathyergidae (Honeycutt et al., 1991). Males and females each construct complex burrow systems of approximately 130 m length and mean diameter 10 cm in sandy clay soils (DuToit et al., 1985; Narins et al., 1992). Burrow systems of Georychus approach within a few meters of each other and are rather evenly spaced (Davies and Jarvis, 1986; Bennett and Jarvis, 1988a). Individuals of Georychus produce sexually-dimorphic patterns of footdrumming (podophony) both in the laboratory and in the field (Bennett and Jarvis, 1988a; Narins et al., 1992). Bennett and Jarvis (1988a) suggest that foot-drumming serves to advertise the presence of an occupied burrow to neighboring animals, as well as to convey information pertaining to sex and reproductive condition.
Footdrumming signals contain both auditory and seismic components. Measurements within and at various distances from a natural Georychus burrow revealed that only the seismic component of the footdrumming signal is detectable in the substrate at distances corresponding to natural inter-burrow distances (3–4 m); the amplitude of the airborne component in an artificial burrow attenuates into the noise level within one meter of the source (Narins et al., 1992). Moreover, using an "artificial thumper" constructed from the solenoid of an electric typewriter, these workers established that the horizontal and vertical components of the surface wave produced by footdrumming attenuate differentially as they propagate through the sandy soil inhabited by Georychus. By comparing amplitudes of the two surface wave components, a Cape mole-rat could, in principle, determine the distance to the signaling individual, as has been suggested to occur in the scorpion Paruroctonus (Brownell, 1977; Brownell and Farley, 1979a, b, c).
The unrelated spalacine mole-rat Nannospalax (previously Spalax) ehrenbergi is highly solitary, extremely aggressive and lives in individual tunnel systems where it rarely encounters conspecifics except during the mating season (Nevo, 1961; Nevo et al., 1986). Instead of drumming with the feet, Nannospalax generates seismic signals by thumping the roof of its tunnel with the flattened anterodorsal surface of its head, in response to vibratory signals from conspecifics (Rado et al., 1987). Rado et al. (1987) demonstrated both with captive and wild Nannospalax that head drumming responses could be elicited by finger tapping and scratching by the experimenter on the substrate. Nannospalax can hear the airborne component of its head thumping signal over short distances (Nevo et al., 1991), but these mole-rats seem to respond mainly to the seismic component (Rado et al., 1987; Nevo et al., 1991). Most of the seismic energy is concentrated below 300 Hz, with main frequency around 100 Hz (Heth et al., 1987, 1991; Rado et al., 1987; Bronchti et al., 1989).
Seismic signaling in other species of fossorial mammals has been less well documented. Foot-drumming behavior has been noted in several other bathyergids: Bathyergus suillus, Bathyergus janetta, Cryptomys hottentotus and Cryptomys damarensis (Bennett and Jarvis, 1988a). Drumming does not occur in the naked mole-rat, Heterocephalus glaber (Bennett and Jarvis, 1988a; Pepper et al., 1991). Foot-drumming may occur in the Geomyidae (Reichman, personal communication in Bennett and Jarvis, 1988a), and Nagel (personal communication to Burda et al., 1990) observed head-knocking in ctenomyids, although other observers have not noticed these behaviors (see Francescoli, 2000). The East African rhizomyine Tachyorictes splendens taps the floor of its burrow with its upper incisors (Bennett and Jarvis, 1988a). Turning to non-rodents, Kuyper (1984, p. 765) notes that the male golden mole Amblysomus hottentotus issues "much chirruping vocalization, head bobbing and foot stomping." The foot stomping in this case appears to be a courtship signal made in close proximity to the female, potentially detectable by either seismic or airborne routes, rather than a long-distance communication signal. The females of certain Cryptomys species make analogous foot-stomping displays (Bennett and Jarvis, 1988b; Bennett et al., 1994). However, Amblysomus has also been said to knock its head on its burrow walls (Duckworth, personal communication to Hickman, 1990), and this might represent a genuine long-distance signal similar to that made by Nannospalax. There are no reports of any form of vibratory communication in talpid moles or in the marsupial mole.
Recent evidence suggests that the Namib desert golden mole, Eremitalpa granti namibensis, uses seismic sensitivity for prey detection. Fielden et al. (1990) observed that this animal moved along the surface of the desert in the areas in which it lives, occasionally submerging (dipping) its head and shoulders into the sand. Only moving prey items seemed to attract the attention of the golden moles. Fielden et al. speculated that Eremitalpa might be detecting substratum vibrations, using these to localize the prey. Narins et al. (1997) showed that Eremitalpa orients itself in a non-random manner towards the grassy hummocks in which prey items are to be found. These hummocks generate seismic signals nearly 30 dB greater in amplitude than those from adjacent flat areas, with a peak amplitude difference at around 300 Hz. This may be due to wind blowing in the dune grass on the mounds, but prey-generated vibrations are also detectable from a shorter range. Narins et al. (1997) suggested that the head-dipping behavior in Eremitalpa is a means of tightly coupling the head to the substrate, and, like Fielden et al. (1990), linked this behavior to localization of seismic signals.
It seems more intuitively likely that a carnivorous species would use seismic sensitivity for food source localization than a herbivorous species. However, the finding of Narins et al. that it is isolated clumps of grass that are apparently used as "acoustic beacons" by Eremitalpa raises the possibility that the herbivorous fossorial rodents might, in theory, use a form of seismic sensitivity to locate their food. In herbivorous species, the tunnel system may have to be continually enlarged in the search for subterranean vegetation (Andersen, 1988). A sensory-guided foraging strategy could reduce the energy costs of burrowing by targeting burrow direction towards a food source. However, although visual cues might be used to locate food sources by those species that visit the surface, and foraging may be concentrated in areas of high food abundance (see Busch et al., 2000 for a review), there is apparently no evidence that fossorial rodents can perceive the location of plants from a distance while underground (Vleck, 1981; Andersen, 1988; Williams and Cameron, 1990; Brett, 1991).
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AUDITION OR SOMATOSENSATION? |
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SYNOPSISINTRODUCTIONBEHAVIORAL EVIDENCE FOR THE...AUDITION OR SOMATOSENSATION?ANATOMICAL ADAPTATIONS...DISCUSSIONEVOLUTION OF SEISMIC SENSITIVITYReferences |
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Snakes spend much time closely juxtaposed to the substrate, and have been found to possess both an auditory and a somatosensory route for the reception of low-frequency ground vibrations (Hartline, 1971
). Similarly, a fossorial mammal might use either or both routes for the detection of seismic signals.
The nature of the modality underlying seismic sensitivity in the mole-rat, Nannospalax, has been the cause of particular controversy in the recent literature. In experimental situations, Nannospalax was found to hold its cheek and lower jaw against the walls of the tube in which it lived when a conspecific was head-tapping (Rado et al., 1989). These authors proposed that this mole-rat uses its auditory system to detect seismic signals, through a form of bone conduction (see later). Heth et al. (1991) and Nevo et al. (1991) examined the scalp-recorded potentials of anaesthetized Nannospalax mole-rats in response to seismic vibrations, and found responses even when white noise was used in an attempt to prevent the auditory route of detection. The latter authors stated that their neurophysiological results were verified by bilateral destruction of the middle and inner ears of their test animals, and that subsequent to this procedure the animals still showed the same responses (both electrophysiological and behavioral) to vibratory stimuli (Nevo et al., 1991). However these workers provided no methods or data regarding this verification procedure. The authors concluded that the detection of low-frequency seismic signals by Nannospalax is via an unknown somatosensory route.
Subsequently, Rado et al. (1998) challenged the results of the Heth and Nevo studies, denying that the somatosensory modality plays a major role in vibration detection in Nannospalax. They provided further evidence that the auditory system may be involved after all, showing that deafened animals did not show a normal response to seismic signals. Rado et al. (1998) suggested that Nevo et al. (1991) might have used too high a stimulation rate, leading to an attenuated auditory response, thus unmasking the residual (and relatively low-amplitude) somatosensory response.
Cortical mapping experiments have shown that the region of cortex corresponding to the auditory area in the star-nosed mole Condylura was responsive in Scalopus, another talpid mole, to light taps or scratches on the table on which the animal was positioned (Catania and Kaas, 1997a). These authors did not directly examine which component of the tapping (airborne or vibrational) evoked a cortical response, but purely airborne stimuli were ineffective at this task. These results suggest that the auditory system in Scalopus is responsive to substrate vibration. However, it is not absurd to imagine that the observed response to vibrations could instead have been mediated by a somatosensory mechanism, the cortical representation of which might be located in the region corresponding to the auditory cortex of other moles, e.g., Condylura. Cross-modal compensation associated with the degeneration of a sense organ has been described in the mole-rat Nannospalax. It was originally thought that auditory projections had invaded the visual area of the brain (Bronchti et al., 1989; Heil et al., 1991), but more recent work (Necker et al., 1992; Rehkämper et al., 1994) has shown that it is the somatosensory system that has expanded into the occipital cortex of the mole-rat. It is at least possible that the somatosensory system of Scalopus might have expanded in a similar way, concomitantly with a degeneration of audition.
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ANATOMICAL ADAPTATIONS SUBSERVING VIBRATORY SENSITIVITY IN FOSSORIAL MAMMALS |
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If seismic signals are detected using the auditory system, the means of detection would probably be a form of bone conduction. Bone conduction refers to the many routes by which vibrations applied to the skull might be transmitted to the inner ear (Tonndorf, 1966, 1972
). This may be a direct route to the inner ear through the cranial bones, or it may involve the middle ear. One mode of bone conduction that has elicited interest in recent years is ossicular inertial bone conduction. In this case, the auditory ossicles in the middle ear of the animal tend to remain in place due to inertia as the skull vibrates around them, resulting in relative movement of the stapes within the oval window (Bárány, 1938), which sets up a pressure wave in the cochlea in the usual way. The massively hypertrophied mallei found in some golden moles (Forster Cooper, 1928; Mayer et al., 1995; Mason, 1999) have raised the possibility that this ossicle might be used in a form of inertial bone conduction (Lombard and Hetherington, 1993). The desert-dwelling golden mole, Eremitalpa, possesses an especially enlarged malleus head (Van der Vyver Nolte, 1968; Mayer et al., 1995; Mason, 1999). However, an increased ossicular mass alone is not sufficient to augment inertial bone conduction, according to the Bárány (1938) model. To accomplish this, increased ossicular mass should be accompanied by the displacement of the center of mass from the rotatory axis. More detailed analyses suggest that the displacement of the center of mass of the ossicular chain, caused by the hypertrophy of the head of the malleus, is a highly significant feature of Eremitalpa and of other golden moles with enlarged ossicles: together with the increased mass, this unusual morphology is indeed consistent with a role in seismic sensitivity by inertial bone conduction (Mason, 1998, 1999; Mason and Narins, 2001).
Other species of fossorial mammals that have been shown to detect seismic signals, including Georychus and Nannospalax, do not possess hypertrophied ossicles like those of golden moles (Burda et al., 1992; Mason, 1999, 2001). It is therefore probable that the means of seismic sensitivity in these species are different. Rado et al. (1989) proposed that a non-inertial form of bone conduction was used in the detection of vibrations in the mole-rat Nannospalax. They suggested that vibrations pass from the substrate to the jaw, which are juxtaposed, and then pass via the jaw articulation to the incus and stapes. These authors cited certain anatomical peculiarities of this region of the skull in Nannospalax as potential adaptations towards this mode of bone conduction.
Roberts (1951) mentioned that the width of the cranium may be important in the detection of substrate vibrations in golden moles. Similarly, Wilkins and Cunningham (1993), having shown that fossorial rodents possess skulls of a range of widths, suggested that the broader skulls of Nannospalax and certain other species might be associated with the reception of seismic communication signals. These authors proposed no mechanism. However, Poduschka (1978, in Burda et al., 1990) has suggested that nerve endings in the large incisor teeth of mole-rats such as Cryptomys may be involved in the detection of vibrations. Poduschka's suggestion seems especially intriguing given that the root of the lower incisor in Nannospalax is contained within a raised bony projection of the mandible. This projection represents the most lateral point on the jaw (personal observation; see Stein, 2000). Could this underlie an alternative, somatosensory interpretation of the "jaw-listening" behavior observed in Nannospalax (Rado et al., 1989)?
Fossorial mammals are equipped with an extensive array of somatosensory receptors, among the best-studied being the Eimer's organs of the snouts of talpid moles (Armstrong and Quilliam, 1961; Quilliam, 1966a, c; Catania, 1995a, b). Eimer's organs differ in different species of moles, but the basic structure is the same. The raised epidermal papilla of each Eimer's organ contains several neural processes associated with the stacked epidermal cells, up to eight Merkel cell-neurite complexes, and within the dermis up to three lamellated corpuscles (Catania, 1995a, b). Based on the histology, it has been suggested that the lamellated corpuscle might be sensitive to vibrations, perhaps vibrations of the soil (Armstrong and Quilliam, 1961; Quilliam and Armstrong, 1963; Quilliam, 1966a, c). In more recent experimental studies, Eimer's organs have been shown to be responsive to a range of tactile cues such as the onset and offset of skin depression, sustained depression and rocking a glass probe on the surface (Catania and Kaas, 1996), but their response to vibration per se has apparently not been studied. Although Eimer's organs have not been found in any other fossorial mammal, Klauer et al. (1997) have demonstrated the presence of simple lamellated corpuscles and Meissner's corpuscles in the dermal papillae of the nose pad of the mole-rat Nannospalax. They believe these indicate a particular sensitivity of this region to vibrations. One possible interpretation of the large forepaw representation that is known to occur within the cortex of the talpid mole Condylura is that receptors in this limb might be sensitive to seismic vibrations (Catania and Kaas, 1995).
Changes in the air currents within the tunnels might warn a fossorial animal of an approaching conspecific, predator, obstacle or tunnel breach (Eloff, 1958; Olszewski and Skoczen, 1965; Quilliam, 1966a; Mellanby, 1971). Interestingly, Olszewski and Skoczen (1965) detected with an anemometer clear changes in air currents in the tunnels of Talpa europaea, brought about by the steps of a man walking on the surface nearby. Whether these pulsations of air were transmitted through ventilation ducts in the tunnel system, or passed into the tunnels through vibrations in the soil, was not addressed. Vibrissae are responsive to deflection (Catania and Kaas, 1995), and it has been suggested that, in Talpa, they may be sensitive to compression waves in the air of the tunnels (Quilliam, 1966a). Sensory hairs are evidently present in nearly all species of fossorial mammals (Godfrey and Crowcroft, 1960; Hildebrand, 1985; Klauer et al., 1997; Nowak, 1999), the possible exception being the marsupial mole, Notoryctes (Lyne, 1959; Hildebrand, 1985). Vibrissae are even present in the (otherwise) naked mole-rat Heterocephalus (Tucker, 1981; Jarvis and Bennett, 1991; Park et al., 2000); artificial deflection of these hairs has been shown to trigger head and body orientation responses (Crish et al., 2000). Eloff (1958) notes that the snout and cornea of certain bathyergid mole-rats are especially sensitive to air currents. The detection of air currents represents one potentially important indirect means by which vibratory signals in the ground might be sensed in fossorial mammals. Another is the radiation of airborne sound from the vibrating walls of the burrows, shown to occur in the burrows of the kangaroo rat Dipodomys spectabilis (Randall and Lewis, 1997).
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DISCUSSION |
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Because vocal communication is only effective over a short range underground, Narins et al. (1992)
suggested that seismic signaling among bathyergid mole-rats might be correlated with solitary lifestyles, when intraspecific communication must be efficient over longer distances. Indeed, communication switches from vocal to seismic as young Nannospalax mole-rats disperse and inhabit separate tunnel systems (Rado et al., 1991). Building on the observations of Narins et al. (1992), Francescoli (2000) identified three broad patterns pertaining to communication in subterranean rodents in general. First, social species (e.g., Heterocephalus and Cryptomys) primarily use vocal communication, effective over short distances. Second, solitary species that spend most of their lives in burrows (e.g., other bathyergids, Nannospalax) tend to use seismic signals for long-distance communication and vocalizations for close-proximity communication. Third, those species that are often active above ground (e.g., ctenomyids) retain good vision and hearing and use vocal communication. Although Francescoli only considered rodents, do other fossorial species follow similar patterns?
Many talpid moles, such as Talpa, Scalopus and Scapanus species, together with some golden moles such as Amblysomus species, are predominantly solitary and spend relatively little time on the surface (Godfrey and Crowcroft, 1960; Zyll de Jong, 1983; Kuyper, 1985; Stone and Gorman, 1985; Nowak, 1999). From the point of view of social structure and habits, they would fall into Francescoli's second category. Other talpid moles, such as Neurotrichus and Condylura, golden moles including Eremitalpa, Chrysochloris and Chrysospalax species, and the marsupial mole Notoryctes, seem to spend more time above ground (Soeuf and Burrell, 1926; Hamilton, 1931; Shortridge, 1934; Dalquest and Orcutt, 1942; Johnson, 1983; Zyll de Jong, 1983; Maddock and Hickman, 1985; Hickman, 1990; Nowak, 1999), so would be better placed in the third category. One might therefore predict that members of the former group would communicate using a combination of seismic and vocal signals, whereas members of the latter group might use vocal signals only. Indeed, both vocal and (possibly) seismic communication signals have been documented in Amblysomus hottentotus (see earlier). This species appears to show the intraspecific communication behaviors predicted for rodents falling into Francescoli's second category. However, Amblysomus does not have hypertrophied ossicles (Burda et al., 1992; Mayer et al., 1995; Mason, 1999, 2001) and it remains to be confirmed that this species in fact uses seismic signaling for intraspecific communication. No seismic communication signals have apparently been documented in any other species of golden moles, talpid moles, or the marsupial mole, and there are few reports of vocalizations in these animals (see Zyll de Jong, 1983; Nowak, 1999). This suggests that the pattern that Francescoli observed in fossorial rodents does not extend to the majority of other subterranean mammals. The means of intraspecific communication in the insectivorous fossorial mammals clearly needs to be examined in more detail and is not addressed further here. The remainder of this paper is devoted to an examination of the evolution of seismic sensitivity in those species to which it is apparently important.
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EVOLUTION OF SEISMIC SENSITIVITY |
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The physical properties of sand are such that the velocity of some forms of seismic signal propagation through it is very low, about a tenth of that in other natural substrates (Brownell, 1977
). Localization of seismic signals, if dependent on time-of-arrival, phase or intensity differences between two or more spatially-separated receptors, is therefore theoretically easier in loose sand than in many other substrates (Brownell, 1977; Brownell and Farley, 1979b). This might help to explain the apparent use of seismic sensitivity in prey localization by the desert-dwelling golden mole Eremitalpa, although the physiological mechanism underlying localization by this animal is unknown (Mason and Narins, 2001).
The structure of the middle ear of the marsupial mole Notoryctes, which shares a similar desert ecology and "sand-swimming" habits (Collins, 1973; Johnson, 1983; Nowak, 1999), is completely different from that of the golden mole (Mason, 1999). The ossicles, rather than being massively enlarged, are actually unusually small in Notoryctes (Mason, 2001). There is no evidence that Notoryctes makes use of seismic sensitivity in its foraging, but its natural behavior is little-known (Johnson, 1983). The means of prey localization in the enigmatic marsupial mole is an outstanding question that remains to be examined in the field. What is apparent from the comparison of Notoryctes and Eremitalpa is that similar ecologies do not necessarily give rise to homologous sensory adaptations.
Those fossorial species that construct permanent burrow systems necessarily do so in firmer soils, in which localization of seismic signals may be more difficult. Certain talpid moles are thought to rely on fortuitously "blundering into" their invertebrate prey during routine patrols of the burrow (Godfrey and Crowcroft, 1960; Mellanby, 1966; Quilliam, 1966a; Catania and Kaas, 1997b). Limited searching in the existing burrow walls with the nose may be more energetically economical than digging through soil in search of more distant prey (Jensen, 1986), so localization of prey at a distance may not be necessary. In the case of fossorial rodents, distance cues, in theory, may be obtained by the comparison of amplitudes of the various components of the surface wave generated by drumming conspecifics (Narins et al., 1992; see earlier). It may be sufficient to establish that the occupant of a neighboring burrow system is still alive, and to glean information about sex and receptivity, rather than to localize the neighbor accurately.
In primates, Pacinian corpuscles and Meissner's corpuscles within the skin confer vibrational sensitivity. The latter receptors are particularly sensitive to frequencies from 10 to 400 Hz, with maximum sensitivity between 100 and 300 Hz (Merzenich and Harrington, 1969; Williams et al., 1995). Lamellated corpuscles in the interosseous region of the leg of the cat respond to vibrational frequencies from 50 to 800 Hz (Hunt, 1961), and in the wallaby Thylogale billardierii to frequencies up to 1.3 kHz, with lowest threshold between 250 and 400 Hz (Gregory et al., 1986). Gregory et al. (1986) suggest that such receptors are used (in the wallaby) for the detection of seismic vibrations. Lamellated corpuscles capable of transducing vibrations are probably common among mammals in general (Quilliam and Armstrong, 1963). Given that similar structures must have been present in the ancestors of all fossorial species, how and why would a species become adapted to use its auditory system for the same purpose, rather than elaborating a pre-existing modality?
When burrowing, ctenomyids, pocket gophers and the bathyergid Bathyergus primarily use their forelimbs in a form of "scratch-digging," although their enlarged incisors may be used to loosen the soil or remove roots (Lehmann, 1963; Hildebrand, 1985; Nowak, 1999; Stein, 2000). Talpid moles do not use their heads in digging at all, but instead rely on "humeral-rotation digging" involving only the forearms (Hamilton, 1931; Skoczen, 1958; Godfrey and Crowcroft, 1960; Yalden, 1966; Hildebrand, 1985). Despite reports of footdrumming in the rodents, there is no firm evidence to suggest that any of these species possess any specific anatomical or behavioral adaptations towards the use of the auditory system for seismic detection. Bearing in mind that the limbs are used for burrowing, it is possible lamellated receptors in the limbs may be involved in vibration sensing.
Spalacid mole-rats use a form of "head-lift" digging to displace and compact the soil (Nevo, 1961; Gasc et al., 1985; Hildebrand, 1985; Stein, 2000). Golden moles and marsupial moles use upwards thrusts of their heads in combination with their forelimbs to move the soil (Bateman, 1959; Puttick and Jarvis, 1977; Gasc et al., 1985, 1986; Hildebrand, 1985; Kuyper, 1985). Most bathyergid mole-rats use their incisors in what is known as "chisel-tooth" digging, and may use their heads in a secondary capacity to move or compact soil (Eloff, 1958; Bateman, 1959; Hildebrand, 1985; Stein, 2000). It is within these groups that the best documented cases of seismic sensitivity and seismic communication are to be found. The heads of these animals, at some point in the digging cycle, are closely coupled to the substrate. Audition might already be biased towards low frequencies due to the nature of acoustic sound propagation underground (see Introduction). These animals might therefore be preadapted to augment a mode of bone conduction, to improve the transmission of low-frequency ground vibrations to the inner ear. Special "listening" behaviors, such as pressing the jaw to the tunnel wall in Nannospalax (Rado et al., 1989), or head-dipping in Eremitalpa (Fielden et al., 1990), would further improve detection of vibrations.
Given this apparent preadaptation, the advantages of using the auditory system over the somatosensory system could relate to the acute sensitivity, wide frequency range and sensitive frequency discrimination characteristic of the mammalian ear (Geisler, 1998). Limitations would include the unwanted noise conveyed to the inner ear when the head was exposed to self-generated vibrations, for example during digging, mastication or drumming behaviors. Middle ear muscles, which might otherwise constitute a protective mechanism, are reduced or missing in all fossorial species so far examined (Burda et al., 1992; Mayer et al., 1995; Mason, 1999; Wilkins et al., 1999). An inertial mode of bone conduction would probably be especially unfavorable to a head-drumming species, which may be why hypertrophied ossicles are not found in Nannospalax and why drumming behaviors have never been observed in any golden mole with hypertrophied mallei (Mason, 1999).
The possible association between digging with the head and seismic sensitivity implies an auditory route for seismic sensitivity, as described above. However, the use of the auditory system for the detection of substrate vibrations has not been established beyond doubt in any species of mammal. Future studies are required to examine the use of seismic signal detection in golden moles and to confirm that inertial bone conduction is involved. The question of whether an auditory or somatosensory pathway is used remains to be investigated in bathyergid mole-rats and has yet to be fully resolved in Nannospalax. The present authors reserve their judgement on this issue, but suggest that the somatosensory system must play a role in seismic sensitivity in all fossorial mammals, the differences relating to the relative importance of this modality in seismic sensitivity, and to the relative importance of seismic sensitivity to the animal.
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ACKNOWLEDGMENTS |
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With thanks to Dr. Adrian Friday. Part of this study relates to work undertaken as part of a Ph.D. dissertation (MJM) funded by the Biotechnology and Biological Sciences Research Council, with additional support from St. John's College, Cambridge. Manuscript preparation supported by NIDCD Grant no. DC00222 to PMN.
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FOOTNOTES |
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1 From the Symposium Vibration as a Communication Channel presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
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SYNOPSISINTRODUCTIONBEHAVIORAL EVIDENCE FOR THE...AUDITION OR SOMATOSENSATION?ANATOMICAL ADAPTATIONS...DISCUSSIONEVOLUTION OF SEISMIC SENSITIVITYReferences |
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