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First published online February 12, 2007
Journal of Experimental Biology 210, 781-787 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02708
Tracking of biogenic hydrodynamic trails in harbour seals (Phoca vitulina)
Ruhr-Universität Bochum, Allgemeine Zoologie and Neurobiologie, ND 6/33, D-44780 Bochum, Germany
Author for correspondence (e-mail:
Bjoern.Mauck{at}rub.de)
Accepted 4 January 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: natural hydrodynamic trails, trail-following, harbour seal, vibrissae
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Coombs et al., 1989) and
diverse hydrodynamic receptor systems in many invertebrate phyla
(Heinisch and Wiese, 1987;
Laverack, 1962;
Tautz and Sandemann, 1980;
Wiese, 1976). In mammals, the
vibrissae of harbour seals were demonstrated to respond to vibrations mediated
by a rod contacting the hair in earlier studies
(Dykes, 1975;
Mills and Renouf, 1986;
Renouf, 1979), but their
function as a hydrodynamic receptor system was demonstrated only a few years
ago using a technique commonly used to study the fish lateral line
(Dehnhardt et al., 1998). The
tuning curve of detection thresholds for dipole water movements (10–100
Hz) determined in a psychophysical experiment characterized the vibrissae of
harbour seals as a highly sensitive hydrodynamic receptor system.
Concerning the ecological significance of seal vibrissae as a hydrodynamic
receptor system, however, it was pointed out that even the deep-diving
pinnipeds are adequately adapted for visual functioning under dark conditions
in the depth and thus there might be no need for compensatory non-visual
explanations of their underwater sensory orientation
(Levenson and Schusterman,
1999). Furthermore, probably because the initial characterization
of the pinniped hydrodynamic receptor system was done using an oscillating
dipole (Dehnhardt et al.,
1998) and water velocities attenuate rapidly with distance from a
flow-field generating dipole source, it was assumed for underwater orientation
of hunting seals that prey is detected mainly visually, and hydrodynamic
information may be used only during the last stage of prey pursuit
(Davis et al., 1999).
Concerning the first argument our recent results show that in pinnipeds, even
though darkness might not impair underwater vision, it clearly is impaired by
even moderate levels of turbidity (Weiffen
et al., 2006). Thus, there is good reason to assume that
underwater orientation cannot rely on vision alone but is in fact a multimodal
sensory process. Furthermore, the assumption that hydrodynamic events might be
important only in the vicinity of potential prey seems obsolete, since it has
been demonstrated that water movements in the wake of fishes show a complex
vortex structure (Blickhan et al.,
1992) with water velocities persisting for up to several minutes
above the threshold of most hydrodynamic receptor systems
(Hanke et al., 2000). Thus,
the wakes of fishes constitute hydrodynamic trails that could be tracked by a
piscivorous predator equipped with a suitable receptor system.
In a pilot study presenting the first evidence for hydrodynamic
trail-following in seals, a miniature submarine was used to generate
reproducible hydrodynamic trails
(Dehnhardt et al., 2001). By
visualizing and measuring the submarine's trail using Particle Image
Velocimetry (PIV), a narrow jet flow of turbulent water was found containing
velocities in the same order of magnitude as those calculated for the wake of
a fish of 30 cm body length. Blindfolded harbour seals were perfectly able to
follow the submarine's course exclusively by using their mystacial vibrissae.
The seals also detected the swimming direction of the submarine when
perpendicularly encountering its trail and were able to follow distinct
changes in the course of a trail. Control tests with a stocking mask covering
the seal's muzzle, thereby impeding whisker movements, showed that the seal
failed even to detect the hydrodynamic trail without vibrissae.
However, although these experiments showed that seals in principle can
detect and follow hydrodynamic trails, the artificial hydrodynamic trail left
by a miniature submarine certainly differs from biogenic trails, concerning
both the three-dimensional structure and the ageing of available information.
The submarine used by Dehnhardt et al. generated a trail of turbulent
structure with a jet flow mainly in the opposite direction of the submarine's
motion (Dehnhardt et al.,
2001). This trail decayed within approximately 30 s. In contrast,
hydrodynamic trails generated by fish consist of vortices arranged in a highly
complex, ladder-like three-dimensional pattern
(Bleckmann et al., 1991;
Blickhan et al., 1992). The
trail of a goldfish of 10 cm body length has been shown to last for more than
3 min under laboratory conditions (Hanke
et al., 2000).
Given these differences, the objective of the present study was to
investigate if a harbour seal is also able to follow natural hydrodynamic
trails. The subcarangiform or thunniform swimming style of seals
(Fish et al., 1988;
Williams and Kooyman, 1985)
generates a hydrodynamic trail similar in structure to that left by respective
fishes and thus can serve as an easy-to-perceive adequate stimulus for
predators hunting by hydrodynamic cues. We therefore trained a harbour seal to
swim predefined courses and measured its hydrodynamic trail by Particle Image
Velocimetry. The test seal was trained to follow the predefined hydrodynamic
trails of its conspecific.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) mentioned in the Introduction. The trail-generating
animal was a 3-year-old experimentally naive male harbour seal named Malte
which, however, was already accustomed to basic training tasks. Both seals
were born in captivity and were housed with seven other harbour seals in a
spacious enclosure consisting of two interconnected outdoor pools with a total
volume of about 1000 m3 of freshwater and adjacent land parts at
our `Marine Science Center' at Cologne Zoo, Germany. The seals were fed
2–5 kg of freshly thawed cut herring supplemented with vitamins; about
half of the seals' daily diet was fed during the experiments. Typically
experiments were conducted over 5 days per week. There was a routine food
deprivation of 12–18 h between the last feeding in the late afternoon
and the experiments on the next day. During experiments the two subjects were
separated from the other seals.
Experimental setup
The experiments were conducted in a kidney-shaped pool
(Fig. 1). We used half of this
pool for conducting the actual trail-following experiments in an almost
semi-circular area; the other half was used to station the trail generator
outside the water on a platform after a hydrodynamic trail had been generated.
The test seal's start position was a stationing hoop attached just above the
water surface next to the experimenter's platform at the edge of the pool's
experimental area. At the opposite side of the pool nine positions near the
pool edge were defined as end points for the trail-following. The position
directly facing the seal's start position was defined as 0°; to the left
and right of this position, respectively, another four end points were defined
in terms of the angle with the 0° position in steps of 10° (i.e.
–10° to –40° and 10° to 40°). Due to the shape of
the pool the distances between the start position and the end points varied
between 10.5 m and 15 m.
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). Now the trail generator was sent to this position to pick
up the ring floating in mid-water and to make a sharp turn towards the
platform in the other half of the pool. The trail generator, still carrying
the ring, jumped onto the platform and remained silently in this position
until the end of the trial. After the trail generator had left the water, the
headphones were removed from the test seal's head, which was the signal to
start the search for the hydrodynamic trail. The trial was considered
successful when the test seal followed the trail to the end point where the
trail generator had picked up the plastic ring, or when it reached an area of
one body length radius (1.5 m) around this point. Successful trials were
rewarded with pieces of herring; the trail generator was rewarded for
retrieving the plastic ring to the experimenter.
The probability that the test seal reached the correct end point by mere
chance can be calculated as follows. The area in which the end points were
defined spanned a distance of 21 m. Since all trials in which the seal reached
an area of one body length radius (
1.5 m) around the actual end point of
the trail were evaluated as hits, the probability that the animal reached this
area by chance was P=(2x1.5)/21=0.14.
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Data recording and analysis
The experiments were filmed with a digital video camera (Canon XL1s,
Krefeld, Germany) mounted on a mast above the pool. The recordings were
digitally cut into single pictures at a frequency of 5 frames
s–1. The swimming paths of both animals were then marked on
subsequent pictures and fitted into a diagram for evaluation.
Flow measurements
To investigate the flow in the seal's wake, we set up a PIV (Particle Image
Velocimetry) system (cf. Adrian,
1991; Westerweel,
1997) that we specially designed for this application. A wooden
box (125 cmx245 cmx125 cm, LxWxH) with sliding doors
in its broad sides was installed in the water
(Fig. 2). A horizontal plane of
laser light was fanned out in the box using an optical fibre and a cylinder
lens (light source: 500 mW-DPSS-Laser, Entertainer 500, Quantum Physics,
Newcastle, UK; optical fibre: Laserlight Showdesign, Berlin, Germany). The
energy density of the fanned-out laser light was in the order of magnitude of
a commercial laser pointer. A CCD Camera (DMK 2001, The Imaging Source,
Bremen, Germany) above the box filmed a section of 48 cmx36 cm of the
illuminated layer. Another CCD camera (DMK 803, The Imaging Source) was used
to film the movements of the seal. An 11 W lamp illuminated the scene as long
as the seal was in the field of view.
Tracer particles (Vestosint 1101, Degussa-Hüls AG, Marl, Germany) were
seeded into the water within the box with the sliding doors shut. After the
water had calmed down, the sliding doors were opened, and after another delay
of 5 min the measurements started. Each measurement started with recording the
background flow in the box for 15 s with the seal waiting outside the box.
With the laser switched off, the seal was then gestured to swim through the
box; as soon as the first half of its body had passed the box, the laser was
switched on. Video images of the flowing illuminated tracer particles were
recorded for 1–3 min on digital tape (Canon XL1s used as recording
device) with 50 fields s–1. Analysis of the recorded images
was done in MatLab 6.5 (The Mathworks, Natick, MA, USA) following the
principles of digital Particle Image Velocimetry
(Hart, 2000;
Willert and Gharib, 1991).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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The test animal performed successful trail-following in 90% of the trials
(444 out of 495 trials). With respect to the nine courses of the hydrodynamic
trails the seal's performance was never less than 80% successful
trail-following (hit-rates: –40°: 87.2%; –30°: 83.7%;
–20°: 90.9%; –10°: 94.5%; 0°: 92.7%; 10°: 94.5%;
20°: 85.5%; 30°: 90.9%; 40°: 87.2%) A 
2-test did
not reveal a correlation between the nine courses and hit- and miss-rates
(2=7.48, d.f.=8, P=0.49)
(Fig. 4).
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In the control experiments with the vibrissae covered, no successful trail-following was observed. In fact, the test animal refused to start its search for the trail at all, not leaving its hoop station even though the start signal had been given. When manually pulled out of the hoop station and pushed in the direction where the hydrodynamic trail could be found, the seal was clearly irritated, never moved further away than approximately 1 m from the experimenter and tried to shake off the stocking mask from its muzzle.
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;
Hanke and Bleckmann, 2004). It
spreads laterally in two branches (one of which was measured here,
Fig. 7). During the first 5 s
the trail contained water velocities that could exceed 200 mm
s–1 and spread laterally mainly to about 80 cm to each side.
While the lateral spread of the trail increased further during the next 5 s,
water velocities decreased to about 45–60 mm s–1. After
30 s water velocities of about 30 mm s –1 were measured in
the outer areas of the box while the areas between the two branches of the
trail consisted of comparatively calm water. The wake was then at least 2 m
wide. The wake's vertical extent was probably much smaller as our harbour seal
swam at a depth of approximately 0.5–1 m and there was no indication of
the wake disturbing the water surface. |
Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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The seal's overall performance in locating the biological trail's end point
was not affected by the direction in which the trail led and was even slightly
higher (ranging from 83.7% to 94.5%) than the performance of our two seals
tested with the miniature submarine's trail (Henry: 78.5%; Nick: 82.2%)
(Dehnhardt et al., 2001).
The reasons for the slightly better overall performance can be speculated
on. One aspect might be variable motivation of a test animal, resulting in
differing performance both within a study and between studies using the same
task. In addition, as Nick took part in both studies but was experimentally
naive in the first study, he might have learned to follow hydrodynamic trails
more effectively. Nevertheless, it might be also possible that the
hydrodynamic trail to be followed in the present study represented a stimulus
very easy to detect and to track, at least in comparison with the hydrodynamic
trail of the miniature submarine we used earlier
(Dehnhardt et al., 2001).
In contrast to biological trails such as those left by swimming fishes, the
submarine's trail does not consist of several branches, but mainly of a
rapidly decaying backward streaming jet of rather round cross-sectional shape.
Although the earlier results with the submarine stimuli unequivocally
demonstrated the capability of harbour seals to track hydrodynamic trails in
general, these stimuli are only a rather rough approach to trails encountered
in the natural habitat. The use of a harbour seal as a trail generator in the
present study combined the advantage of being able to generate highly
reproducible trails due to the reliable training of the seal with generating
easy-to-detect, high-intensity hydrodynamic trails assumed to resemble those
left by a carangiform or thunniform swimming fish
(Fish et al., 1988;
Lighthill, 1969), concerning
both the complex three-dimensional structure and the slow ageing of the
hydrodynamic information. It seems plausible that this kind of trail
represents a more adequate hydrodynamic stimulus for the vibrissal system.
Therefore, the present results open the door towards a more
sensory–ecologically oriented research using natural hydrodynamic
stimuli.
Some ecological implications of the results
Underwater orientation in marine mammals is certainly a multimodal process
that may involve vision (e.g. Davis et
al., 1999; Levenson and
Schusterman, 1999) (but see
Weiffen et al., 2006),
echolocation and/or passive audition (Au,
1993; Bodson et al.,
2006), taste (e.g. Sticken and
Dehnhardt, 2000) and active touch (e.g.
Dehnhardt and Dücker,
1996; Dehnhardt and Kaminski,
1995), as well as hydrodynamic perception, to compose a complex
representation of the environment. Which of the various senses of a seal
predominates in a given situation, however, probably depends on the
information available at a certain time and place. In the case of hydrodynamic
information, this means that trails of water movements could supplement or
even temporarily substitute other types of information if these are currently
not available.
In addition to hydrodynamic trails generated by swimming prey fish, trails
left by conspecifics can gain significance for harbour seals in certain
situations. For example, lactating harbour seals and their pups equipped with
time-depth-recorders at Sable Island, Nova Scotia, spent about 40% of their
time together at sea and tended to dive together
(Bowen et al., 1999). Pups
appeared to descend with their mother at the beginning of a dive, returned to
the surface to load oxygen if the dive exceeded about 1.5 min, and then dived
again, presumably to rejoin their mother
(Bowen et al., 1999). The
authors hypothesize that on these dives, in addition to maintaining contact to
the mother, the pups may also learn where and on what the mother is feeding.
Furthermore, a young harbour seal could benefit from following a more
experienced conspecific while exploring safe routes and feeding grounds.
Harbour seal pups have to cope with an abrupt transition from milk to food
they obtain themselves (cf. Frost et al.,
2006). They increase their vertical operating range continuously
(Bekkby and Bjorge, 2000;
Frost et al., 2006) and can
undertake excursions of more than 75 km from their natal area in their first
summer (Small et al., 2005).
Even older harbour seals may encounter situations when it pays to follow a
conspecific with deeper knowledge of the respective area. Following another
seal by its hydrodynamic trail could be of great importance in these cases if
water or light conditions limit vision.
While hunting, seals may use hydrodynamic information not just during the
last stage of prey pursuit after having detected prey visually, as assumed by
Davis et al. (Davis et al.,
1999). We suppose that it might be rather the other way round:
seals may detect and possibly even identify prey when encountering a
hydrodynamic trail, and trail-following might bring the seal close to its prey
where it can be hunted down visually. In the light of this hypothesis our
results also provide a first important step to our understanding of how
hydrodynamic events are used by seals in terms of search strategies for prey.
Our seal employed at least two different search patterns, probably depending
on the way it encountered the hydrodynamic trail. When the seal encountered
the trail at an acute angle it mostly stayed in the main channel of water
turbulences (compare Fig. 5A),
between the two branches of the trail or touching these on both sides while
following the trail. Although the structure of the harbour seal trails used in
the present study was different, this linear pattern of trail-following
corresponds well to the way our seals tracked hydrodynamic trails generated by
the miniature submarine used in earlier work
(Dehnhardt et al., 2001). As
it accounted for 63% of the successful trials of the present study, the linear
pattern is a fairly reliable way of trail-following and thus can be assumed to
be preferably used in the wild whenever possible, e.g. to stalk travelling
prey fish. However, our present results also reveal that when the seal
encountered the trail generator's hydrodynamic trail at a more obtuse angle
– the probability of which was higher the further the trail's end point
deviated from the 0° direction – it was obviously often moving so
fast that on missing it seemed to overshoot the trail (or at least the first
lateral branch of the trail) and subsequently corrected its course. This
resulted in the undulatory pattern of trail-following consisting of a course
that repetitively crossed the trail (or one of its branches), and only by
gradually narrowing led the seal to the end point. In the wild, this
trail-following pattern might be used to track prey fish the trail of which
has been newly encountered and subsequently missed for some reason, or to
track down fleeing prey fish trying to escape by repetitive protean manoeuvres
(rapidly turning away from the predator's attack path at unpredictable times
and turning angles).
The question of how hydrodynamic information could support or even
substitute vision remains, however. In contrast to terrestrial habitats where
some of the large predator species are frequently observed to attack their
prey over rather large distances [e.g. 50–200 m for cheetah
(Eaton, 1970)], most fish
predator pursuits and corresponding prey escapes examined up to now are
obviously rather brief and occur over relatively short distances
[(Godin, 1997) and references
therein]. This might be related to the fact that many fish predator attacks
seem to be guided visually and thus terminated as soon as the fleeing prey
gets out of sight. Given that visibility is often drastically reduced in the
marine environment (Aarup,
2002), a fleeing prey fish might simply vanish in the haze after a
short fast start or some protean manoeuvres and then stop fleeing to save the
costs associated with continued flight (e.g. energy expenditure, lost
opportunities). In contrast to fish predators, which have not been shown yet
to be capable of hydrodynamic trial-following bridging a large distance
between predator and prey (but see
Pohlmann et al., 2001;
Pohlmann et al., 2004),
harbour seals and probably some other pinnipeds capable of tracking the trail
left by a prey fish would be able to bridge this distance using hydrodynamic
information until vision is of some use again. This multimodal use of
available information while hunting could represent a fitness advantage and
might have favoured the evolution of vibrissae as a hydrodynamic receptor
system.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Aarup, T. (2002). Transparency of the North Sea and Baltic Sea – a Secchi depth data mining study. Oceanologia 44,323 -337.
Adrian, R. J. (1991). Particle imaging techniques for experimental fluid mechanics. Annu. Rev. Fluid Mech. 23,261 -304.
Au, W. W. L. (1993). The Sonar of Dolphins. New York: Springer.
Bekkby, T. and Bjorge, A. (2000). Diving behaviour of harbour seal Phoca vitulina pups from nursing to independent feeding. J. Sea Res. 44,267 -275.[CrossRef]
Bleckmann, H. (1994). Reception of Hydrodynamic Stimuli in Aquatic and Semiaquatic Animals. Stuttgart, Jena, New York: Fischer Verlag.
Bleckmann, H., Breithaupt, T., Blickhahn, R. and Tautz, J. (1991). The time course and frequency content of hydrodynamic events caused by moving fish, frogs and crustaceans. J. Comp. Physiol. A 168,749 -757.[Medline]
Blickhan, R., Krick, C., Zehren, D. and Nachtigall, W. (1992). Generation of a vortex chain in the wake of a subundulatory swimmer. Naturwissenschaften 79,220 -221.[CrossRef]
Bodson, A., Miersch, L., Mauck, B. and Dehnhardt, G. (2006). Underwater auditory localization by a swimming harbor seal (Phoca vitulina). J. Acoust. Soc. Am. 120,1550 -1557.[CrossRef][Medline]
Bowen, W. D., Boness, D. J. and Iverson, S. J. (1999). Diving behaviour of lactating harbour seals and their pups during maternal foraging trips. Can. J. Zool. 77,978 -988.[CrossRef]
Coombs, S., Görner, P. and Münz, H. (1989). The Mechanosensory Lateral Line. Neurobiology and Evolution. New York: Springer.
Davis, R. W., Fuiman, L. A., Williams, T. M., Collier, S. O.,
Hagey, W. P., Kanatous, S. B., Kohin, S. and Horning, M.
(1999). Hunting behavior of a marine mammal beneath the Antarctic
fast ice. Science 283,993
-996.
Dehnhardt, G. and Dücker, G. (1996). Tactual discrimination of size and shape by a California sea lion (Zalophus californianus). Anim. Learn. Behav. 24,366 -374.
Dehnhardt, G. and Kaminski, A. (1995). Sensitivity of the mystacial vibrissae of harbour seals (Phoca vitulina) for size differences of actively touched objects. J. Exp. Biol. 198,2317 -2323.[Medline]
Dehnhardt, G., Mauck, B. and Bleckmann, H. (1998). Seal whiskers detect water movements. Nature 394,235 -236.[CrossRef]
Dehnhardt, G., Mauck, B., Hanke, W. and Bleckmann, H. (2001). Hydrodynamic trail-following in Harbor seals (Phoca vitulina). Science 193,102 -104.
Dykes, R. W. (1975). Afferent fibers from
mystacial vibrissae of cats and seals. J.
Neurophysiol. 38,650
-662.
Eaton, R. L. (1970). Hunting behavior of the cheetah. J. Wildl. Manag. 34, 56-67.
Fish, F. E., Innes, S. and Ronald, K. (1988).
Kinematics and estimated thrust production of swimming harp and ringed seals.
J. Exp. Biol. 137,157
-173.
Frost, K. J., Simpkins, M. A., Small, R. J. and Lowry, L. F. (2006). Development of diving by harbor seal pups in two regions of Alaska: use of the water column. Mar. Mamm. Sci. 22,617 -643.[CrossRef]
Gellermann, L. W. (1933). Chance orders of alternating stimuli in visual discrimination experiments. J. Genet. Psychol. 42,206 -208.
Godin, J.-G. J. (1997). Evading predators. In Behavioural Ecology of Teleost Fishes (ed. J.-G. J. Godin), pp. 191-236. Oxford: Oxford University Press.
Hanke, W. and Bleckmann, H. (2004). The
hydrodynamic trails of Lepomis gibbosus (Centrarchidae),
Colomesus psittacus (Tetraodontidae) and Thysochromis
ansorgii (Cichlidae) investigated with scanning particle image
velocimetry. J. Exp. Biol.
207,1585
-1596.
Hanke, W., Brücker, C. and Bleckmann, H. (2000). The ageing of the low-frequency water disturbances caused by swimming goldfish and its possible relevance to prey detection. J. Exp. Biol. 203,1193 -1200.[Abstract]
Hart, D. P. (2000). PIV error correction. Exp. Fluids 29,13 -22.[CrossRef]
Heinisch, P. and Wiese, K. (1987). Sensitivity to movement and vibration of water in the North Sea shrimp Crangon crangon L. J. Crust. Biol. 7, 401-413.[CrossRef]
Laverack, M. S. (1962). Responses of cuticular sense organs of the lobster Homarus vulgaris (Crustacea). I. Hair-peg organs as water current receptors. Comp. Biochem. Physiol. 5,319 -325.[CrossRef]
Levenson, D. H. and Schusterman, R. J. (1999). Dark adaptation and visual sensitivity in shallow and deep-diving pinnipeds. Mar. Mamm. Sci. 15,1303 -1313.[CrossRef]
Lighthill, J. M. (1969). Hydromechanics of aquatic animal propulsion. Annu. Rev. Fluid Mech. 1, 413-446.[CrossRef]
Mills, F. H. J. and Renouf, D. (1986). Determination of the vibration sensitivity of harbour seals (Phoca vitulina) vibrissae. J. Exp. Mar. Biol. Ecol. 100, 3-9.[CrossRef]
Pohlmann, K., Atema, J. and Breithaupt, T.
(2004). The importance of the lateral line in nocturnal predation
of piscivorous catfish. J. Exp. Biol.
207,2971
-2978.
Pohlmann, K., Grasso, F. W. and Breithaupt, T.
(2001). Tacking wakes: the nocturnal predatory strategy of
piscivorous catfish. Proc. Natl. Acad. Sci. USA
98,7371
-7374.
Renouf, D. (1979). Preliminary measurements of the sensitivity of the vibrissae of Harbour seals (Phoca vitulina) to low frequency vibrations. J. Zool. 188,443 -450.
Small, R. J., Lowry, L. F., Hoef, J. M. V., Frost, K. J., DeLong, R. A. and Rehberg, M. J. (2005). Differential movements by harbor seal pups in contrasting Alaska environments. Mar. Mamm. Sci. 21,671 -694.[CrossRef]
Sticken, J. and Dehnhardt, G. (2000). Salinity discrimination in harbour seals: a sensory basis for spatial orientation in the marine environment? Naturwissenschaften 87,499 -502.[CrossRef][Medline]
Tautz, J. and Sandemann, D. C. (1980). The
detection of waterborne vibration by sensory hairs on the chelae of the
crayfish. J. Exp. Biol.
88,351
-356.
Weiffen, M., Möller, B., Mauck, B. and Dehnhardt, G. (2006). Effect of water turbidity on the visual acuity of Harbour seals (Phoca vitulina). Vis. Res. 46,1777 -1783.[CrossRef][Medline]
Westerweel, J. (1997). Fundamentals of digital particle image velocimetry. Meas. Sci. Technol. 8,1379 -1392.[CrossRef]
Wiese, K. (1976). Mechanoreceptors for
near-field water displacements in crayfish. J.
Neurophysiol. 39,816
-833.
Willert, C. E. and Gharib, M. (1991). Digital particle image velocimetry. Exp. Fluids 10,181 -193.
Williams, T. M. and Kooyman, G. L. (1985). Swimming performance and hydrodynamic characteristics of harbor seals Phoca vitulina. Physiol. Zool. 58,576 -589.
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