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First published online February 4, 2005
Journal of Experimental Biology 208, 647-659 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01396
Evidence for the use of reflected self-generated seismic waves for spatial orientation in a blind subterranean mammal
1 Department of Zoology, Faculty of Life Sciences, Tel-Aviv University, Tel
Aviv 69978, Israel
2 Department of Geophysics and Planetary Sciences, Faculty of Exact
Sciences, Tel-Aviv University, Tel Aviv 69978, Israel
* Author for correspondence at present address: Harvard University, Department of Molecular and Cellular Biology, 16 Divinity Avenue, Cambridge, 02138 MA, USA (e-mail: kimhi{at}fas.harvard.edu).
Accepted 15 November 2004
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Our field observations revealed that all the monitored mole-rats produced low-frequency seismic waves (250-300 Hz) at intervals of 8±5 s (range: 1-13 s) between head drums while digging a bypass to detour an obstacle. Using a computerized simulation model we demonstrated that it is possible for the mole-rat to determine its distance from an obstacle boundary (open ditch or stone) by evaluating the amplitude (intensity) of the seismic wave reflected back to it from the obstacle interface. By evaluating the polarity of the reflected wave the mole-rat could distinguish between air space and solid obstacles. Further, the model showed that the diffracted waves from the obstacle's corners could give the mole-rat precise information on the obstacle size and its relative spatial position.
In a behavioural experiment using a special T-maze setup, we tested whether the mole-rat can perceive seismic waves through the somatosensory system and localize the source. The results revealed that the mole-rat is able to detect low frequency seismic waves using only its paws, and in most cases the mole-rats determined accurately the direction of the vibratory source. In a histological examination of the glabrous skin of the mole-rat's paws we identified lamellate corpuscle mechanoreceptors that might be used to detect low frequency seismic waves.
The combined findings from these different approaches lead us to suggest that a specialized seismic `echolocation' system could be used by subterranean mammals to determine the most energy-conserving strategy with which to bypass an obstacle, as well as to estimate their distance from the surface, keeping their tunnels at the optimal depth.
Key words: spatial orientation, obstacle, echolocation, seismic signal, Spalax ehrenbergi, mole-rat, subterranean mammal
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Introduction |
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). The physical properties of the encountered obstacles
affected the burrowing distance from the obstacle edge: (a) for open ditches,
a side bypass 10-20 cm from the obstacle boundaries; or (b) for wood or stone
obstacles, a side bypass 3-8 cm from the obstacle boundaries. When the
obstacle was placed asymmetrically across the tunnel, the mole-rats always
burrowed their bypass around the shorter side, while they showed no preference
for a particular side in symmetrically placed ditches
(Kimchi and Terkel, 2003b).
These findings demonstrated the mole-rat's ability to estimate the size and
shape of the obstacle, its own exact position relative to the obstacle
boundaries and even the obstacle's density, through the soil medium.
How can one explain this remarkable spatial orientation ability? Whenever
possible, surface-dwelling mammals use vision to localize and assess obstacles
in their path (Schone, 1984).
Under dark conditions, when obstacles cannot be detected visually, animals
shift to an alternative, light-independent mechanism such as touch (using the
somatosensory system), if the obstacle is in close contact with their body
(Carvell and Simons, 1990). In
order to localize and assess more distant obstacles in the dark, a specialized
mechanism of orientation known as echolocation has been shown to be used by a
limited group of mammals (e.g. bats,
Schnitzler et al., 2003;
whales and dolphins, Purves and Pilleri,
1983). These animals emit ultrasonic (high frequency) sounds to
locate and estimate the size, distance and type of object ahead by detecting
the reflected sound waves from the object's interface (see
Busnel and Fish, 1980;
Griffin, 1974;
Nachtigall and Moore, 1988).
However, none of the above-mentioned mechanisms of orientation explain how a
blind mammal such as the mole-rat, with a hearing range limited to low
frequency sounds (Heffner and Heffner,
1992), detects and assesses distant buried obstacles, and also
accurately estimates and maintains its own optimum digging depth.
The mole-rat is adapted behaviourally, anatomically and physiologically to
transmitting and perceiving low frequency seismic signals (Rado et al.,
1987,
1998; Heth et al.,
1987,
1991). From a geophysical
perspective, soil in general is a good conductor for such low frequency
seismic waves and for propagating them for a long distance with relatively
little attenuation (depending on the physical properties of the soil;
Liu et al., 1979;
Steeples et al., 1997;
Bachrach et al., 1998;
Bachrach and Nur, 1998).
Insects, frogs, snakes and lizards, and even some species of mammals, use
seismic signals for communication, food detection and to avoid hazards
(reviewed in Narins, 2001;
Mason and Narins, 2001;
Hill, 2001;
Randall, 2001). Previous
studies have shown that the mole-rat produces vibrational signals for
long-distance communication by rapidly striking the flattened anterodorsal
surface of its head against the tunnel roof. It was also shown that the
mole-rat can perceive and respond both behaviourally and neurologically to
neighbouring mole-rats' `head drumming' (Heth et al.,
1987,
1991; Rado et al.,
1987,
1998).
Consequently, we hypothesized that one of the mechanisms employed by the mole-rat to orient in its underground habitat might be the use of low frequency seismic waves reflected back to it, in a type of echolocation system. We applied a multidisciplinary approach to test whether such a mechanism could be used by the mole-rat to assess the relative distance, dimensions and density of underground obstacles. In a field study we examined whether the mole-rat indeed generates seismic waves while burrowing a bypass tunnel to detour an obstacle. We then used a computer simulation to determine the physical characteristics of seismic waves reflected by subterranean obstacles in order to determine the feasibility of their perception by the mole-rat. Finally, we used both behavioural tests and histology to determine whether the mole-rat can perceive seismic waves through its feet using the somatosensory system.
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). The study was carried out during the wet season (October to
April) in 2001 and 2002.
Procedure
Two conditions were examined. In the first condition, in seven separate
mole-rat territories (at least 50 m apart), identified above ground through
the mounds of excavated soil forming a straight line, we dug a small
rectangular ditch (50 cmx60 cm) across a tunnel, bisecting it into two
disconnected parts, as previously described (Kimchi and Terkel
2003a,b).
For each ditch, six vertical geophones (Geo space GSC-20D, Houston, TX, USA;
vibration detection above 20 Hz) were inserted in the ground at 30-40 cm
intervals, at a distance of 15-20 cm from the boundaries of the ditch
(Fig. 1A), and connected to a
multi-channel tape-recorder (6 channels analog tape, TASCAM, Montebello, CA,
USA) (Fig. 1A). Using this
geophone array we recorded the seismic waves generated by each mole-rat in its
respective territory throughout the entire process of burrowing the bypass
tunnel to detour the obstacle and reconnect the two disconnected tunnel
parts.
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In the second condition, in five separate mole-rat territories with no obstacle obstructing the mole-rat's path, using the same equipment as for the first condition, we recorded the seismic waves that the animal generated while digging a tunnel of about 200 cm length (estimated by observing the above-ground mounds of earth excavated by the mole-rat).
The seismic waves recorded in the field were transferred to a computer, viewed with Sound Forage software (Sonic Foundry, Inc., Madison, WI, USA), and analyzed by standard seismic data processing software (ProMAX, Englewood, CO, USA).
Computer seismic simulator modeling: general considerations
The computer simulations were used to determine the physical
characteristics of seismic waves being reflected by different types of
underground obstacles in order to determine the feasibility that those
reflected waves can be used by the mole rat to assess the location, size and
density of the obstacle.
Our simulated model was carried out under the assumption that the seismic
energy travels as acoustic waves (P waves) in the subsurface, where the
mole-rat dwells (Zuri and Terkel,
1996; Heth, 1989).
In all simulations, the mole-rat was replaced by a basic seismic recording
system in which the source and the receiver were located in the same spatial
position.
In a purely acoustic medium, where both source and receiver are located in
the same place, the shape and strength of the reflected signal are governed by
two variables: distance from the source to reflecting object; and the
reflection coefficient at the reflection point. The acoustic reflection
coefficient (C) at the boundary separating two materials (1 and 2) is
defined by:
 | (1) |
where V is the acoustic velocity (P-wave velocity) and 
is
the density of the material. The material characteristic V is
known as the acoustic impedance (Sheriff,
2002). In the case where the second material is air, for which the
density is practically zero, the reflection coefficient is equal to -1.
The wavelength 
is determined by:
 | (2) |
where V is the velocity and f is the dominant frequency.
To simulate the seismic source generated by the mole-rat's head drumming,
using seismic data-processing software we built a synthetic zero-phase wavelet
pulse with a dominant frequency of 300 Hz that matched the amplitude spectrum
of a typical seismic wave generated by a mole-rat detouring an obstacle (see
Fig. 1B,C; recorded head-drum
vs synthesized pulse). To simulate the mole-rat's underground habitat
(non-packed soil; density of about 1.1 g cm-3) we used a velocity
of 85 m s-1 (based on the field records of
Rado, 1993) and a velocity of
330 m s-1 with zero density for air space. The software used for
the computer simulation was a standard finite-difference modeling of the
acoustic wave equation (Kelly et al.,
1976). This software allows for a variety of source functions,
generation of synthetic seismograms and snapshots of wave propagation at
specified times.
Laboratory studies: perception of seismic waves
For intraspecific long-distance communication it has been demonstrated that
the mole-rat is able to perceive low frequency seismic signals via
bone conduction, by pressing its lower jaw against the tunnel wall (Rado et
al., 1989,
1998).
In spatial orientation based on an echolocation mechanism, in contrast to intraspecific communication, the transmitter and receiver source are the same individual. As such, a mole-rat which produces seismic waves by head-drumming on the tunnel roof, is unlikely could change its head position and press its lower jaw against the tunnel wall within less than the 10 ms required to perceive the reflected signal from close by obstacles (about 50 cm away). This led us to hypothesize that for spatial orientation the mole-rat might perceive the seismic waves through those other body parts that are always tightly pressing the tunnel floor, such as its paws.
The aim of the following experiment was to test whether the mole-rat can both perceive and locate the source of seismic waves (similar to those generated by the mole-rat in nature) only through its paws.
(a) Behavioural experiment
Animals
Adult mole-rats of both sexes were trapped in the Tel Aviv area and
maintained in individual plastic cages (33 cmx38 cmx14 cm) with
wood shavings for bedding, at Tel Aviv University, for 1-2 months before the
beginning of the experiment. The animals were kept under a constant light
regime (14 h:10 h L:D) and room temperature (24-26°C), and received rodent
chow, carrots and apples ad libitum, from which they obtained
sufficient water.
Apparatus
The set-up described below was specially designed to ensure that the
seismic signals would be transferred only to the mole-rats' paws, via
the maze floor, and could not be perceived through the animal's lower jaw,
which has been previously found to be used for long-distance intraspecific
communication (referred to as `jaw-listening'; Rado et al.,
1989,
1998).
Set-up
The experimental set-up was as follows (see
Fig. 2A,B): a wooden board (140
cmx80 cmx2 cm) was placed on a layer of sponge (4 cm thick) on a
table in the centre of the room. Two transparent Perspex tubes (6 cm in
diameter) were joined to form a T-maze comprising a 60 cm long entrance tube
(with two movable doors, one near the entrance and the second half way along)
intersecting another perpendicular tube (50 cm) in the middle. A 3.5 cm width
slit was cut out along the entire length of both tubes. The entire T-maze was
then suspended 1 cm above the wooden board with the slit facing downwards
(Fig. 2B). It was supported by
three clip clamps connected by arms to two peripheral tables placed about 30
cm fromthe wooden board (Fig.
2A). This design enabled the experimental animals to locomote in
the suspended tubes with only their feet protruding from the slit and in
contact with the board surface (Fig.
2B). There was no contact between the tubes and the wooden floor,
and any vibratory signals produced on the board could thus be perceived only
through the animal's paws.
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Vibratory source
Two sources of vibratory signals were used.
To monitor and adjust the mechanical shaker so that the characteristics of the vibratory signals generated would resemble those produced by a mole-rat, we attached one geophone firmly to the wooden board and another one to the maze tubes. The vibrations detected by the geophones were recorded and viewed using Sound Forage software. Spectral analysis was used to ensure that the frequency content and phase of the mechanical signal were similar to those generated by the mole-rat in the field, and that indeed no vibrations produced by the vibratory source (on the wooden floor) were transmitted to the maze tubes.
Procedure
Pre-testing (acclimation). In order to acclimatize the animals
(N=14) to the apparatus, they were allowed to move freely in the maze
for 4 days, 15 min a day each. For three additional days (10 trials a day) the
animals were trained to move from the maze arm entrance to the T-junction,
passing the two doors that were opened by the researcher. At the T-junction
each animal was given the choice to turn either right or left, into one of the
two maze arms. To increase the animals' motivation to explore the apparatus,
we placed a food reward (small piece of apple) at the far end of both maze
arms. Animals that reached the far end of the maze arm received the food
reward. After consuming the reward the animal was removed from the maze tube
and returned to its nest box, using a Perspex transfer tube.
Experimental tests. Mole-rats are solitary and highly aggressive
territorial animals. Two mole-rats being introduced into the same tube quickly
move toward each other and generate frequent head-drumming against the tunnel
roof, which elicits extreme mutual aggression
(Shanas and Terkel, 1997;
Rado et al., 1987). This
natural spontaneous aggressive behaviour was exploited in the design of the
present experiment. We tested the mole-rats' ability to locate the direction
of the seismic (vibratory) source and to turn in that direction. The 14
trained animals were divided randomly into two equal groups. One group was
exposed to seismic stimuli produced by a stimulus mole-rat, and the second
group to those produced by a mechanical mini-shaker.
(1) Mole-rat stimulus. First, the experimental mole-rat was transferred from its nest box into the entrance tube using a connecting tube. The first door was then closed behind the mole-rat and the nest box was removed. The mole-rat now faced the T-junction with the doors in front and behind it closed. At this stage the stimulus mole-rat was inserted using a connecting tube into one of the two Perspex tubes (either right or left) attached to the wooden board. Within a few seconds the stimulus animal started to head-drum, generating intense seismic waves that were transferred to the wooden board. If such behavior did not occur spontaneously we triggered the stimulus animal to start drumming by gently touching its fur with a small brush. After a few seconds of head-drumming we opened the door adjoining the T-junction, allowing the experimental animal to freely select right or left turn.
The animals were tested individually for two days, 20 trials per day. For each trial the laterality of the vibratory source was selected using a random table.
(2) Mechanical shaker stimulus. The experimental mole-rats in this group were tested individually for their ability to identify the direction of the seismic stimulus produced by the mechanical shaker. The test procedure was the same as in the previous (mole-rat stimulus) group.
Control tests
In order to verify that the mole-rats were relying on seismic waves and not
on airborne sound or olfactory cues to determine the position of the vibratory
source, we performed the following control test using the same animals and
procedure of the experimental tests but with the vibratory source (the
stimulus mole-rat or the mechanical shaker) positioned on a narrow wooden
board to the right or left of the perpendicular tube ends, at a distance of 10
cm from the edges of the central table. In this way airborne sound waves and
possibly olfactory cues could pass to the experimental mole-rats, but seismic
waves could not.
Data recording and analysis
The performances of the two groups of animals (one exposed to vibratory
stimuli produced by a stimulus mole-rat and the second to a mechanical
mini-shaker) were recorded in the same way. We recorded the directional choice
as correct when the mole-rat turned into the maze arm leading to the vibratory
source, from a total of 20 trials a day, on the two test days.
We initially used Wilcoxon matched pairs tests for each of the animal groups separately, in order to compare between the mole-rats' performances on days 1 and 2. Since we found no significant difference between the performances over the two days we pooled the data for each group. We then used the pooled data to compare between the performances of the two separate animal groups using Mann-Whitney U-test. Further, for each of the two groups we used Wilcoxon matched pairs test to compare between the animals' performance in the experimental vs control; and between the experimental vs random directional choice (50%). A Bonferroni correction was applied to set alpha level to 0.025 due to the multiple comparisons.
(b) Histological examination
Animals
Two adult mole-rats and two adult Levant voles (Microtus guentheri
L.), all trapped in the Tel Aviv area, were used. We chose the vole to serve
as a comparison to the mole-rat for the following reasons: (1) it is a rodent
systematically close to the mole-rat; (2) it inhabits niches similar to those
inhabited by the mole-rat; (3) it spends a substantial amount of time in an
underground tunnel system; and (4) as far as we know, there has not been a
single report that this species, in contrast to the mole-rat, produces and/or
uses seismic vibrations for communication, spatial orientation or any other
task.
Procedure
All animals were sacrificed with an overdose (80 mg/100 g) of a combination
of Ketamine (Ketalar; Parke-Davis, Ann Arbor, MI, USA) and Xylazine (Rompun;
Bayer, Leverkusen, Germany). The toes and toe-pads from both forefeet and
hindfeet were removed, kept in 10% formaldehyde solution for 3 days,
decalcified with EDTA, dehydrated, embedded in paraffin and sectioned at 5-7
µm either perpendicular or parallel to the skin surface. The serial
sections were mounted on gelatin-coated microscope slides and stained with
Hemotoxylin and Eosin. The slides were examined using a light microscope for
the presence and number of rapidly adapting mechanoreceptors (e.g. Pacinian
corpuscles receptors) in each foot.
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Clear seismic waves were recorded from all seven monitored mole-rats throughout the process of burrowing a tunnel to bypass an obstacle. The seismic waves consisted of a sharp single head drum with frequency band between 250-300 Hz (Fig. 1B), with maximum energy concentrated around 300 Hz. The mean (± S.E.M.) amplitude of the waves was 49.5±12.0 dB (range: 36-70 dB). The mole-rats generated on average 198±15 seismic waves per meter of bypass tunnel burrowed. We observed no significant difference in this variable between the different stages of the bypass construction or between animals. Analysis of 40 sequential vibrations produced by a mole-rat during the bypass tunneling revealed that the average time interval between the head-drums was 8±5 s (range: 1-13 s).
The control (N=5) mole-rats, digging a tunnel with no obstacle in front, burrowed 1 m of tunnel at the same speed as the mole-rats burrowing a bypass tunnel (128±12 vs 126±10 min m-1, accordingly). The low frequency seismic waves (around 300 Hz) produced while burrowing were similar for both sets of mole-rats. However, the control animals produced significantly fewer seismic waves/meter than those burrowing a bypass tunnel (95±12 taps min-1 vs 198±15 taps min-1, accordingly; t-test for independent samples, t10=5.1, P<0.001).
Computer simulator model
In the first simulation we attempted to evaluate the mole-rat's ability to
estimate its distance from a reflected air-soil interface while burrowing a
new tunnel. The simulation model consisted of a single-source/single-receiver
(the mole-rat's body) located at 30 or 50 cm from the soil-air interface. The
simulation demonstrated that the amplitude of the reflected seismic signal is
inversely proportional to the distance of the mole-rat from the reflecting
interface, i.e. the greater the distance, the weaker the reflection that
reaches the mole-rat (Fig.
3).The arrival time of the reflected energy is also proportional
to the distance from the interface: each 10 cm from the obstacle boundary
results in a time delay of about 2.5 ms.
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In the second simulation we evaluated the mole-rat's ability to distinguish between reflected interfaces of air-soil and soil-solid material (an open ditch compared to a solid obstacle). As in the previous simulation, this model consisted of a single-source/single-receiver located at 30 or 50 cm from the reflected interface with the same geometry, except that we replaced the air with a solid material (typical stone), which has an acoustic velocity of 2000 m s-1 and a density of 1.8 g cm-3. The simulation demonstrated that both amplitude and time delay of the reflected wave decrease as a function of the distance from the reflected interface, as in the previous example. However, since solid materials (stone, wood, etc) are denser (i.e. their velocity is greater) than non-packed soil, the reflected energy from the soil-solid material interface has a smaller reflection coefficient and therefore smaller amplitude than that reflected from the soil-air interface. Further, the polarity of the reflected pulse is now positive in contrast to the negative polarity of the reflection from the soil-air interface (Fig. 3).
The third simulation evaluated the mole-rat's ability to estimate the size
and position of obstacles using reflected seismic waves. In the field the
mole-rat has been shown to distinguish between a small and a large ditch and
its relative position from the obstacle in the case of an asymmetrical ditch.
To simulate this situation a two-dimensional model was digitized
(Fig. 4). The rectangular
obstacle was an open ditch (soil-air interface) and the source/receiver (the
mole-rat) was located inside the simulated soil (acoustic velocity of 85 m
s-1). A zero-phase wavelet with a dominant frequency of 300 Hz was
used as the source function. The wave-front simulation was calculated by
solving the two-dimensional acoustic wave equation using a finite-difference
scheme to determine the spatial and temporal numerical derivations
(Kelly et al., 1976). The
simulation revealed that three major reflected waves eventually reached the
source location (Fig. 4). The
first and strongest one was the reflection wave from the soil-air boundary.
Next were two weaker waves, constituting the secondary diffractions from the
ditch corners (see Fig. 4,
T3 and T4). Since the source is located closer to the
left corner, the diffraction from this corner reaches the source first (see
diffraction wave I).
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This simple simulation shows that the `information' about the location of the obstacle corners is contained in the diffracted energy. If the diffractions can be perceived by the mole-rat, then the question remains as to how it identifies them as diffractions (and not reflections) and how it determines their laterality.
In the third simulation we assumed that the mole-rat can detect reflected/diffracted energy through at least two of its paws (we used left forepaw and left hindpaw). We also assumed that the mole-rat generates at least two single head-taps at different distances from the obstacle's closest boundary (in this simulation at 30 and 35 cm) (Fig. 5A). If the animal is able to assess the difference between the return time of the reflection and diffraction waves detected by the forepaw and hindpaw (whether left or right), there would be no difference between the first and second tap reflected wave, while for the diffraction wave there would be a substantial difference between the two taps (Fig. 5B). This would enable the mole-rat to differentiate between the reflected waves and the diffracted waves. Following identification of the diffraction wave, its laterality must be determined. From the mole-rat's perspective, the closer diffracting corner will be the side from which the first diffraction wave reaches its paws (in this simulation from the left corner). Further, similar to the reflection waves, the amplitude and time delay of the diffraction waves are proportional to the distance of the mole-rat from the obstacle corners, and this information could be used by the mole-rat to estimate the size of the obstacle.
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Perception of seismic waves
Behavioural experiment
Experiment test: All mole-rats (from both groups) succeeded in locating and
selecting the correct maze arm leading toward the stimulus mole-rat or
mechanical shaker vibratory source in most of the trials (>80%;
Table 1).
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No significant difference was found in the performance between the first and the second day of the experiment for both types of (animal groups) vibratory source (mechanical shaker: Z=1.2, P=0.2; stimulus mole-rat: Z=0.3, P=0.7; Table 1).
The performance of the animals exposed to vibration generated by the stimulus mole-rat was significantly better than that of those exposed to vibration generated by the mechanical shaker (U=3.5, P<0.01).
Control test: The animals failed to correctly localize the side of the vibratory stimulus when the vibratory waves could not reach their feet (only air-borne waves and possibly some olfactory cues were available). The performance of all animals in the control test was significantly lower than that in the experimental test (mechanical shaker: Z=2.4, P<0.025; stimulus mole-rat: Z=2.4, P<0.025); and not different from random directional choice (mechanical shaker: Z=0.9, P=0.3; stimulus mole-rat: Z=0.8, P=0.4) (Table 1; Fig. 6).
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Histological examination
Defined lamellate corpuscle mechanoreceptors resembling Pacinian corpuscle
receptor morphology were found in both the forepaws and hindpaws of the
mole-rats but not of the voles. These structures were usually oval or elliptic
in shape, with a diameter of 30-60 µm and in clusters of up to three
corpuscles (Fig. 7). The
corpuscular structures were distributed mainly in the dermis and subcutaneous
tissue of the glabrous skin. Most (
80%) of them were found in the toe
region and the remainder in the distal part of the paws. There were 15-20
corpuscles per foot, with no substantial difference in shape, size or number
between the forefeet and hindfeet.
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,b).
As far as we know, none of the sensory channels that are used to detect and
assess obstacles in short-distance orientation by surface-dwelling mammals are
accessible for subterranean mammals like the mole-rat
(Kimchi and Terkel, 2002).
Nonetheless, the mole-rat demonstrates an amazing ability for efficient
spatial orientation (see Introduction). We thus hypothesized that it might be
using a light-independent sensory mechanism adapted to the unique conditions
of its underground habitat: a type of echolocation mechanism based on seismic
waves.
A number of terrestrial invertebrate and vertebrate species are known to
use seismic waves (vibration) for intraspecific communication (e.g.
white-lipped frog, Lewis and Narins,
1985; Narins,
1990; kangaroo rats, Randall
and Lewis, 1997; blind mole-rat,
Rado et al., 1987;
Heth et al., 1987; Cape
mole-rat, Bennet and Jarvis,
1988; Narins et al.,
1992). Some predators use the seismic waves produced by their prey
for directional localization (e.g. sand scorpions,
Brownell and Farley, 1979;
Brownell and Hemman, 2001;
sandfish lizard, Hetherington,
1989; Namib desert golden mole,
Narins et al., 1997; for more
detail, see Narins, 2001;
Hill, 2001).
Common to all the above processes in which information is obtained seismically is that the source of the signal is one individual while the recipient is another. In contrast, we present here evidence supporting a novel application of seismic waves by a subterranean animal: the use of self-generated seismic waves reflected from an obstacle interface in order to estimate the obstacle's size, shape, density and distance; and the use of self-generated seismic waves reflected from the surface interface to estimate the tunnel digging depth.
Seismic waves generated by the mole-rat
The characteristics of the seismic waves produced during excavation of a
detour tunnel in this study differed markedly from those waves shown
previously to be used in social intraspecific long-distance communication. The
latter seismic waves produced by a series of rapid head drums (average 4 taps
s-1 at a frequency range of 150-250 Hz;
Rado et al., 1987;
Heth et al., 1987). In
contrast, during bypass tunnel excavation the mole-rats produced single
low-frequency seismic waves with an average time interval between waves of
8±5 s (range 1-13 s interval) at a frequency range of 250-300 Hz.
The finding that mole-rats burrowing a bypass tunnel around an obstacle produce significantly more seismic waves per meter of tunnel digging than those digging a straight tunnel with no obstructions, provides additional support for the possibility that the mole-rat uses seismic waves for spatial orientation. It further implies that during performance of a more complex spatial orientation task, such as estimating the type and position of underground obstacles, production of frequent seismic waves (per burrowing length) assists in better spatial discrimination.
Together, these two findings suggest the use of seismic waves as a type of `echolocation' mechanism during burrowing, differing in quality and function from the seismic waves (head-drums) produced in social communication.
Computer modeling
Using computational modeling, we examined the reflection wave
characteristics of seismic waves such as those generated by the mole-rat and
reflected from the obstacle boundaries. The resulting data indicated the
feasibility of using seismic echoes for short-distance spatial
orientation.
The computer simulation reveals that the seismic waves generated by a mole-rat can be reflected back to the animal from both the soil-air interface and the soil-solid material interface. We suggest that these reflected seismic waves may be used by the mole-rat to assess the size, shape and density of an obstacle and possibly also to assess its digging depth, in the following way. Differentiation between obstacle densities (i.e. reflected interfaces of soil-air vs reflected interfaces of soil-solid material) can be performed by analyzing the polarity of the reflected signal. Solid obstacles (stone, wood, etc.) reflect seismic waves with the same polarity as the transmitted waves, whereas an open ditch reflects waves with the opposite polarity. The relative distance from the obstacle boundary can be estimated both from the amplitude and the time delay of the reflected signal.
The simulation also showed that generation of a single seismic signal and perception of the reflected wave by a single detector might be sufficient for the mole-rat to maintain a constant distance from a reflected interface (obstacle boundary and ground surface). However, the animal's ability to determine the closest corner of an asymmetrical obstacle, by detecting the diffraction waves from the obstacle's corners, can be explained only if the mole-rat has generated at least two seismic waves and that the reflected waves are perceived by at least two detectors on its body (e.g. on two different paws). This is necessary because in this task the mole-rat must first identify the diffraction waves and then distinguish them from the reflection waves.
Although these acoustic modeling tests allow a theoretical explanation for
the field observation (Kimchi and Terkel,
2003a,b),
we would like to emphasize that some practical difficulties remain unsolved in
this study.
In standard seismic work it is commonly assumed that the maximum observable
resolution in the recorded data is /4
(Sheriff, 2002). Thus, if we
assume that the mole-rat produces seismic waves with a dominant frequency of
300 Hz (present study) and that the soil velocity is 85 m s-1 in
the subsurface (Rado et al., 1993), the mole-rat can possibly detect and
distinguish between objects with a minimal spatial resolution of 7 cm (i.e.
the mole-rat probably cannot detect items smaller than about 7 cm). Relative
to the size of the mole-rat (length 15-20 cm) and its surrounding habitat,
this is a very low resolution for spatial orientation (in comparison, in some
insectivorous bats echolocation resolution can reach less than 0.5 mm using
ultrasound waves of up to 120 kHz;
Nachtigall and Moore, 1988;
Schnitzler et al., 2003). This
limited frequency band, which initially appears to be disadvantageous, may
have been adopted by the mole-rat to serve as a filter to screen out
irrelevant seismic waves. The reflections from small objects (e.g. stones and
roots) and/or any other type of irrelevant high frequency noise in the
mole-rat's underground surrounding can thereby be avoided.
Finally, we would like to emphasize that the computational modeling presented in this study only provides a theoretical model for the lab/field observations. However, although the simulations were based on very simplistic models compared to the variables faced by the mole-rat in its natural habitat (i.e. obstacles with rough surfaces, non-homogeneous soil and obstacle composition), the concept remains the same. It is most likely that in nature the main reflected waves are masked by stronger noise (secondary seismic waves) and thus the mole-rat's sensory system must perform in a poor signal-to-noise ratio. This would require the mole-rat to possess an effective amplifying capability as well as some kind of frequency filter.
Perception and localization of seismic waves through the animals' paws
We suspect that the mole-rat uses more than one sensory channel for
perception of seismic waves. In intraspecific long-distance communication it
was demonstrated both behaviourally and electrophysiologically that the
mole-rat is able to perceive low frequency seismic waves via bone
conduction, by pressing its lower jaw against the tunnel wall. The vibrations
are thought to be processed mainly by the auditory system
(Rado et al., 1998).
Nevertheless, the authors do not rule out partial involvement of the
somatosensory system in this process (Rado
et al., 1998). Indeed, other studies have implicated somatosensory
system perception through body mechanoreceptors of the animals
(Nevo et al., 1991;
Heth et al., 1991).
In contrast to intraspecific communication, where the transmitter and receiver are separate entities, in detection and estimation of underground obstacles the transmitter and receiver are the same (the individual mole-rat). The physical properties of seismic echoes would require the mole-rat to perceive the reflecting echo within about 7 ms if the obstacle is 30 cm away. Since it would not be possible to move from head-drumming to jaw-listening within such a short time, somotosensory detection of the reflected seismic waves through the animal's feet, which are in constant contact with the ground, might be a more feasible solution.
The laboratory behavioural experiment supports this idea, having shown that the mole-rat can efficiently perceive seismic waves through its paws and accurately localize the position of the vibratory source (mole-rat head-drumming or seismic waves generated by a mechanical shaker).
In a complementary histological study we found that the glabrous skin
(mainly in the dermis and subcutaneous tissue) in the paws of both the
forefeet and hindfeet of the mole-rat contain (lamellate corpuscle)
mechanoreceptors that morphologically resemble Pacinian corpuscles. These
alike structures, found to be concentrated in the toe region and the distal
part of the paws of various mammals (cats, macropod marsupials and primates),
are known to be very sensitive to vibrations, in particular at frequencies
ranging from 10 to 400 Hz, with maximum sensitivity between 100 and 300 Hz
(reviewed in McIntyre, 1980).
Thus, it is highly possible that these somatosensory receptors found in the
mole-rat paws are responsible, at least in part, for the detection of seismic
waves, and thus constitute part of the animal's spatial orientation mechanism.
Such a possibility was also suggested for another subterranean mammal. Catania
and Kaas (1995,
1996) found that the large
forepaws of the star-mole, Condylura cristata, have a huge
representation in the somatosensory cortex, suggesting that the forepaws
provide an important sensory surface, possibly used in detecting ground
vibrations
We suggest that the rationale for the mole-rat possibly using two signal-detection systems (i.e. jaw and feet) might be related to differences in the amplitudes of the seismic waves perceived and analyzed by the animals in the two tasks (i.e. social communication vs spatial orientation).
In spatial orientation (seismic `echolocation'), as presented in this
study, the waves travel in the soil for short distances (tens of centimetres),
while in social seismic communication
(Rado et al., 1987; Randall et
al., 1997; Heth et al., 1987;
Narins et al., 1992) the waves
travel a distance of several to tens of meters, suggesting that different
amplification systems might be required for the different tasks.
To examine this suggestion we first determined whether there is a
substantial difference between the amplitude of the seismic waves generated
for communication and those possibly generated for seismic echolocation. We
found no significant difference between the strength (amplitude) of seismic
waves generated by the mole-rat while burrowing a bypass (present study:
49.5±12.0 dB) to that produced for social communication
(Rado, 1993). We also found
that the overall variations in the strength of the waves were no more than a
factor of two. This is not surprising if we consider that it is the
restrictions imposed on the animal by its habitat (narrow tunnels), its manner
of generating vibration (head-drumming), and its small body dimensions, that
impose this acoustic limitation (the frequency and amplitude of the seismic
waves produced by the mole-rat).
A detailed field study of the amplitude decay of the seismic signal
generated by the mole-rat, as a function of the distance, was demonstrated by
Rado (1993). Rado found that
the mole-rats' seismic vibrations decay exponentially (expressed by the
formula y=3847.6x10(-0.65537x), where
y=acceleration, x=distance). Using Rado's decay formula to
compare the strength of vibrations traveling a distance of 0.6-1.0 m (typical
seismic wave travel distance in echolocation), to their strength after
traveling a distance of a few (3-4) meters (typical travel distance used in
communication), revealed that in communication the waves will reach the
mole-rat 30-90-fold weaker than in echolocation. If we double the travel
distance of the waves used for communication the difference can even reach 3-4
orders of magnitude.
Thus it seems that although the amplitude of the seismic waves produced by the mole-rat for social communication and spatial orientation (seismic `echolocation') are probably alike in both frequency content and amplitude, the amplitude of the waves perceived by the mole-rat should be substantially different in the two tasks, due to the difference in the travel distance of the waves.
It is thus theoretically possible that the two detection systems are optimized for different amplitude ranges of seismic waves and thus for different functions. Confirmation of this hypothesis requires further comprehensive field observations and computer simulations.
Conclusions and evolutionary aspects
Any spatial orientation using self-generated substrate-borne reflecting
vibrations (seismic `echolocation') must incorporate the following
requirements: (1) the animal must have the morphological structures and
behavioural repertoire to generate a seismic signal with suitable geophysical
transmission properties (e.g. wave amplitude and frequency); (2) the medium in
which the animal dwells must be able to conduct such seismic waves; (3) the
animal must possess sensory structures capable of detecting reflection and
diffraction waves from the ground, and a neural network that transmits the
signal to the appropriate brain regions; and (4) the animal must have a neural
system capable of extracting the reverberating waves from the ambient noise,
and of quantifying them, in order to respond with the appropriate
behaviour.
The means of generating seismic signals used by the blind mole-rat was
first discovered by Rado et al.
(1987) and Heth et al.
(1987). The two research
groups found that the mole-rat produces low frequency (150-250 Hz) seismic
signals by rapidly striking the flattened anterodorsal surface of its head
against the tunnel roof. It was further found that the mole-rat responds both
behaviourally and neurologically to such low-frequency seismic signals (Heth
et al., 1987,
1991; Rado et al.,
1987,
1998).
To date, the use of seismic signals by the blind mole-rat has only been
demonstrated with relation to long-distance intraspecific communication
(Heth et al., 1987;
Rado et al., 1987). Other
fossorial mammals also seem to be able to use the seismic channel for
communication as well as for prey detection (reviewed by
Mason and Narins, 2001;
Narins, 2001;
Randall, 2001).
The present study is the first to demonstrate that fossorial mammals might also use seismic signals in some kind of seismic `echolocation' mechanism, when orienting underground.
We have shown that low frequency seismic waves generated by the blind mole-rat while digging its burrow can be reflected back to the animal from the surface of underground obstacles and are probably perceived through the specialized lamellate corpuscle mechanoreceptors in its paws. The computer modeling also demonstrated that those reflected seismic waves could carry with them information on the spatial position, size and density of underground obstacles.
This type of low frequency seismic waves could thus serve the mole-rat as a
reliable spatial orientation tool to accurately dig the optimum
energy-conserving bypass tunnel while detouring an obstacle, as shown recently
(Kimchi and Terkel,
2003a,b).
Further, it is possible that such a mechanism might also be used by the animal
to determine and continuously monitor its digging depth, ensuring that its
tunnel will be dug parallel to the surface at a depth of 15-20 cm, which is
correlated with the depth of its underground food sources (geophytes) and the
optimal abiotic conditions (e.g. temperature, atmospheric conditions)
(Heth, 1989;
Zuri and Terkel, 1996).
We suggest that the unique characteristics of the underground habitat, which impose extreme sensory restrictions and survival costs (e.g. extremely energy-costly digging, exposure to high CO2 and low O2 pressure), exerted strong evolutionary pressure on subterranean mammals, such as the blind mole-rat, to develop and utilize such a complex specialized short-distance mechanism of orientation. This would enable them to avoid unnecessary, energy-costly digging, as well as reducing other risks to survival (e.g. exposure to the surface and consequent high predation risk).
Future studies combining neuroethological and physiological approaches will also contribute to clarifying the mechanism of this specialized spatial orientation system. Particularly interesting problems are how the mole-rat manages to extract the reflected waves from the ambient noise and to quantify and rapidly process this information, in order to respond with the appropriate behaviour.
Finally, further research is needed to examine whether this mechanism is also used by other subterranean mammals that have convergently evolved in this fascinating underground habitat.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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