Vibrissae provide pinnipeds with tactile information primarily in the aquatic environment, which is characterized by its high thermal conductivity and large potential cooling power. Since studies of thermal effects on human tactile sensitivity have revealed that cooling below normal skin temperature impairs sensitivity, the present study investigates the tactile sensitivity of the vibrissal system of harbour seals at varying ambient temperatures. Using plates bearing gratings of alternating grooves and ridges, the texture difference thresholds of two adult seals were determined under water. We took advantage of the natural difference in ambient temperature between summer and winter. Mean water temperature was 1.2 °C during the winter and 22 °C during the summer. During the cold season, the thermal status of both seals was examined using an infrared-sensitive camera system. The texture difference threshold of both seals remained the same (0.18 mm groove width difference) under both test conditions. The thermographic examination revealed that the skin areas of the head where the mystacial and supraorbital vibrissae are located show a substantially higher degree of thermal emission than do adjacent skin areas. This suggests that, in the vibrissal follicles of harbour seals, no vasoconstriction occurs during cold acclimation, so that the appropriate operating temperature for the mechanoreceptors is maintained.

In cold-acclimated mammals, vasoconstriction in the periphery results in a reduced blood flow to the skin, followed by a decrease in skin temperature and a reduction in heat loss (Randall et al. 1997). While a substantial decrease in skin temperature is favourable from a thermoregulatory point of view, we know from the common experience of finger numbness in humans (Mackworth, 1953; Mills, 1956) as well as from studies on human touch that it is extremely unfavourable with respect to touch. Although the extent of the effects of cooling varies with the mode of tactile stimulation (passive stimulation, active touch), with the quality of the stimulus (punctate pressure, frequency of vibration, texture) and with the type of threshold determined (detection threshold, difference threshold), the results can be summarized by stating that in humans a substantial decrease in skin temperature leads to severe deterioration of tactile sensitivity (Green, 1977; Stevens et al. 1977; Green et al. 1979; Bolanowski and Verrillo, 1982; Verrillo and Bolanowski, 1986; Bolanowski et al. 1988; Gescheider et al. 1997).

In pinnipeds, the highly innervated facial vibrissae or whiskers are the prime organs of the tactile sense. Phocid seals, such as the harbour seal Phoca vitulina, possess three distinct groups of these sensory hairs: the conspicuous mystacial vibrissae, two small vertical rhinal vibrissae on the top of the muzzle and five vibrissae above each eye, the so-called supraorbital vibrissae (for a description of the distribution of mystacial and supraorbital vibrissae, see Fig. 1A). Each hair is embedded in a large and intricately structured follicle in the skin, which is characterized by a complex blood-filled sinus system (Stephens et al. 1973; Hyvärinen, 1989; Fig. 1B). Despite the different morphological organization of vibrissal follicles in comparison with the glabrous skin of the human hand, the provision of mechanoreceptors (Merkel cells, lanceolate and lamellated endings, free nerve endings) is quite similar for both tactile systems (Stephens et al. 1973; Johansson and Vallbo, 1979; Hyvärinen, 1989). Accordingly, recent psychophysical studies have demonstrated that the active touch performance of mystacial vibrissae in pinnipeds is comparable with that of the hands of primates, not only with regard to tactile sensitivity but also with regard to functional aspects of the sense of touch (Lederman and Klatzky, 1987; Dehnhardt, 1990, 1994; Dehnhardt and Kaminski, 1995; Dehnhardt and Dücker, 1996; Dehnhardt et al. 1997).

Fig. 1.

(A) Distribution of supraorbital and mystacial vibrissal follicles in a harbour seal. (B) Schematic view of a longitudinal section of a vibrissal follicle (overall length 1–2 cm). Shaded areas belong to the tripartite, blood-filled sinus system. M, mouth of follicle at the skin surface; H, vibrissal hair shaft; UCS, upper cavernous sinus; RS, ring sinus; LCS, lower cavernous sinus; N, nerve bundle penetrating the capsule of the follicle.

Fig. 1.

(A) Distribution of supraorbital and mystacial vibrissal follicles in a harbour seal. (B) Schematic view of a longitudinal section of a vibrissal follicle (overall length 1–2 cm). Shaded areas belong to the tripartite, blood-filled sinus system. M, mouth of follicle at the skin surface; H, vibrissal hair shaft; UCS, upper cavernous sinus; RS, ring sinus; LCS, lower cavernous sinus; N, nerve bundle penetrating the capsule of the follicle.

Vibrissae provide seals with tactile information primarily in the aquatic environment, where the animals (during the winter, with increasing water depth or in polar regions) often face temperatures of approximately 0 °C. In principle, seals reduce the dissipation of heat at low environmental temperatures in the same way as has been described for humans. However, in addition to a reduced blood flow to the skin, seals possess an extra layer of fat (blubber) that provides effective insulation and, unlike most terrestrial mammals, they have been shown to allow their outermost tissue layers to cool to close to the ambient temperature (Irving, 1969; Ryg et al. 1988, 1993; Folkow and Blix, 1989; Hokkanen, 1990; Worthy, 1991; Watts et al. 1993; Kvadsheim et al. 1997). How do seals maintain vibrissal tactile sensitivity in their thermally hostile environment? Since it has been suggested that the vibrissal system provides a seal with important sensory input during underwater orientation and foraging (Oliver, 1978; Dehnhardt and Kaminski, 1995), appropriate adaptations are to be expected to counteract the loss of tactile sensitivity that has been demonstrated in humans under cold conditions. In the present study, we first show using a psychophysical technique that, in contrast to the human hand, the tactile sensitivity of the mystacial vibrissae of harbour seals (Phoca vitulina, L.) is not affected by ambient temperature. We provide an explanation of this phenomenon in seals based on infrared thermographic examination, a technique that has been successfully employed for measuring surface temperatures in both arctic (Ursus maritimus, Øritsland et al. 1974) and tropical (Loxodonta africana, Phillips and Heath, 1992) mammals.

Subjects

The study was conducted at ‘Tierpark Rheine’, Germany. Two adult harbour seals (Phoca vitulina, L.) took part in the psychophysical experiments: a 6-year-old female (Rosi) and a 19-year-old male (Robbi). Testing was conducted in a concrete pool (9.0 m×5.0 m×1.5 m) with an adjacent dry platform. From an earlier study, both seals were experienced in making tactile discriminations by means of their mystacial vibrissae (Dehnhardt and Kaminski, 1995). During the psychophysical experiments, the seals were blindfolded with removable eye caps, usually used for human medical purposes. In this way, the test animal was prevented from receiving any visual information during trials. Both these seals and one additional female seal (Susi, 20 years of age) served as subjects for the infrared thermographic examination.

Stimuli and test apparatus

To investigate whether the vibrissal system of the seals shares the deficiencies described for human tactile sense functions in response to cold, a texture discrimination task adapted from that employed for testing thermal effects on the tactile sensitivity of the human hand was used (Green et al. 1979). However, instead of a magnitude estimation method we used a two-alternative forced-choice procedure, requiring the animals to discriminate between Perspex plates (10 cm×10 cm×2 cm) bearing gratings of alternating grooves and ridges (Fig. 2). The only distinct stimulus parameter that varied among the plates was the width of the vertical grooves, which were 2.0, 2.1, 2.2, 2.3, 2.4, 2.5, 3.0, 3.5, 4.0, 4.5 and 5.0 mm wide. The grooves were cut by a computer-controlled milling machine with a permissible deviation in width of less than 0.01 mm. The ridge between two grooves was held constant at 2 mm, while the groove depth was 5.0 mm. The plate with a 2 mm groove width served as a standard stimulus which was presented in each discrimination task with one of 10 comparison stimuli.

Fig. 2.

The experimental arrangement for the discrimination of grooved surfaces by a seal and a detail of the stimulus presentation area.

Fig. 2.

The experimental arrangement for the discrimination of grooved surfaces by a seal and a detail of the stimulus presentation area.

The test apparatus (Fig. 2) consisted of a white plastic board with two windows (25 cm×25 cm) cut out beside each other. The back of each window was covered by a Perspex shutter (Fig. 2) which could be folded back from its vertical position. Stop blocks ensured that the shutters could only fall back to an angle of 40 °. When the windows were closed, springs held the shutters in the vertical position. The stimuli were mounted on small T-bars (Fig. 2), which could be inserted into frames (resembling the counterpart of a T-bar) fixed to the centre of the front of each shutter. This allowed the stimuli to be mounted rapidly and to be held securely on the apparatus. A shutter could be pushed out of its vertical position by the test animal pressing its snout gently against the grooved surface. A rubber disc (10 cm in diameter) between the two windows at the front of the apparatus served as a stationing point for the test animal. From this position, a blindfolded seal could easily reach the stimuli. The apparatus was positioned in a guideway mounted on the edge of the pool (Fig. 2). The board could be moved up and down in this guideway and fastened in different positions. Stimuli were presented approximately 50 cm below the water surface.

Test conditions and psychophysical procedure

The pool water was neither cooled nor heated so that advantage could be taken of the natural difference in water temperature between summer and winter. Mean water temperature was 1.2±0.3 °C (mean ± S.E.M) during the winter and 22±2 °C during the summer. During the winter, the pool was covered by thick ice (Fig. 3). The ice was broken into small pieces in the area around the test apparatus before testing so that the animals were not hindered during trials.

Fig. 3.

The test conditions during the winter, when the water temperature was approximately 1 °C.

Fig. 3.

The test conditions during the winter, when the water temperature was approximately 1 °C.

A trial started with the apparatus fastened in the guideway so that the stationing point for the test animal was immediately above the water surface. The seal placed its snout on the stationing point and was blindfolded with the eye caps. The standard stimulus and one comparison stimulus were mounted on the shutters, and the apparatus was then lowered in the guideway until the stimuli were 50 cm below the water surface. The test animal followed this vertical movement by simply remaining in the stationing position. The test animal left the stationing position immediately after hearing a short blast on a whistle, given by the experimenter as a starting signal, and examined both surfaces alternately. It indicated its decision by pushing the shutter of the respective stimulus out of its vertical position. The choice of the standard stimulus was rewarded with a piece of herring.

Two test sessions were carried out every day, each consisting of 20 trials. During a session, one discrimination task consisting of a single pair of stimuli (the standard stimulus and one comparison stimulus) was used. Each stimulus was presented at both positions on the apparatus according to pseudorandom schedules (Gellerman, 1933). The same discrimination task was presented until the performance differed by less than 5 % correct choices between at least two consecutive sessions. The percentage of correct choices calculated from these corresponding sessions (at least 40 trials) resulted in the psychometric function. Difference thresholds (ΔS), defined as the difference in groove width between the standard and comparison stimuli at which the test animal made 75 % correct choices (30 correct choices in 40 trials; binomial test, P<0.001), were determined using a modified method of limits, with the comparison stimuli presented only in descending order (from 5.0 mm to 2.1 mm groove width). The exact value of ΔS was obtained by linear interpolation of the two data points on either side of 75 % correct choices. The test series started with a task in which the test animal showed reliable discrimination between the standard and a comparison stimulus (2 mm versus 5 mm groove width). The difference in groove width between the standard and comparison stimuli was then reduced from task to task until the seal failed to make the discrimination. Testing was terminated when a seal did not achieve 75 % correct choices and did not improve its performance during at least ten additional sessions.

Comparison with human subjects

To examine whether the tactile discrimination task used for the seals is appropriate for demonstrating the typical decrease in tactile sensitivity in humans during cold exposure, we roughly estimated the performance of four human subjects on the same texture discrimination task using their hands immersed in the water. At a water temperature of approximately 20 °C, all four human subjects were able to discriminate the standard stimulus from the stimulus with the smallest grooves (2.1 mm) at a level of 70–75 % correct choices, indicating a threshold of approximately 5 % groove width difference. This result corresponds well with the texture difference thresholds measured by Lamb (1983) and Morley et al. (1983) for human subjects. However, at a water temperature of approximately 1.5 °C, the three subjects tested (one subject decided not to take part in the cold condition tests), could only detect a difference in groove width of 0.4 or 0.5 mm, indicating a decline in performance by a factor of at least four. Thermographic examinations of the subjects’ index fingers revealed skin temperatures of 8–10 °C after 15 s of exposure to the cold water. These results are consistent with those of the study of Green et al. (1979), in which grooves of 0.38 mm or less in width were estimated as ‘nearly smooth’ at skin temperatures below 15 °C. Thus, the texture discrimination task used in this study should be an appropriate test for the effects of temperature on the tactile sensitivity of seals.

Thermography

At low air temperatures during the winter, the seals usually did not leave the water, so that they were permanently exposed to a temperature of approximately 1 °C. Even when the seals were swimming on the surface, the mystacial vibrissal pads were submerged most of the time or were washed by cold surface water. For infrared recordings, the animals were trained to bring the upper part of their body out of the water and to press their lower jaw onto a target held by a trainer (see inset to Fig. 5). In this way, only a few seconds passed between an animal leaving the water and the onset of the thermographic recording. During the course of a recording session (approximately 20 min), several thermograms were recorded from each animal to check for variability in temperature distributions. Thermal radiation was recorded twice (with a 2-week interval) from the faces of the three seals.

An AGEMA-Thermovision THV 450 D thermoscanner was used to measure infrared radiation with a temperature resolution of 0.1 °C (internal calibration). Object distance was approximately 0.8 m, and the temperature measuring range was set from −2.2 to +18.9 °C. Thermograms were stored digitally and analyzed using specially designed software (IR-win 5.0, AGEMA) that allowed exact measurements of surface temperatures, e.g. in spots (SP) and areas (AR) as well as by isotherms. A ‘rainbow’ colour scheme was chosen for the thermogram.

Difference thresholds

Throughout the study, tactile discrimination behaviour was similar for both seals and did not change with water temperature. When touching a grooved surface, a seal protracted its vibrissae to the most forward position, where they were no longer actively moved. Once a stimulus had been located, the animal moved its head in a single horizontal sweep so that the vibrissae stroked across the surface perpendicular to the orientation of the grooves. A detailed analysis of the seals’ tactile behaviour and performance in making texture discriminations will be provided in a subsequent paper (G. Dehnhardt, in preparation).

The response behaviour of both seals was extremely reliable, yielding in typical psychometric functions (Fig. 4). These functions show that the ability of both seals to discriminate grooved surfaces by means of their mystacial vibrissae remained essentially unaltered under both test conditions. At mean water temperatures of 22 °C and 1.2 °C, the difference threshold of both seals was a groove width difference of 0.18 mm (9 % stimulus difference).

Fig. 4.

Psychometric functions of performance of two harbour seals discriminating between grooved surfaces. The percentage of correct choices is plotted versus the groove width of the stimuli to be compared. The seals were required to choose the standard stimulus (vertical arrow; the 2 mm groove width) in each stimulus combination. The horizontal dashed line at 75 % correct choices marks the defined difference threshold; the vertical dashed line indicates the size of the interpolated comparison stimulus at threshold. Each data point represents the result of at least 40 trials.

Fig. 4.

Psychometric functions of performance of two harbour seals discriminating between grooved surfaces. The percentage of correct choices is plotted versus the groove width of the stimuli to be compared. The seals were required to choose the standard stimulus (vertical arrow; the 2 mm groove width) in each stimulus combination. The horizontal dashed line at 75 % correct choices marks the defined difference threshold; the vertical dashed line indicates the size of the interpolated comparison stimulus at threshold. Each data point represents the result of at least 40 trials.

Thermograms

Thermograms obtained from individual seals showed no difference, nor were any differences found between the two measuring dates. Thermograms did not change with time; from the onset of recording, the temperature distribution remained stable for the duration of a session. The thermogram shown in Fig. 5 is representative of the results of the infrared measurements.

Fig. 5.

Infrared thermogram showing the typical distribution of temperatures measured on the surface of a seal’s face immediately after the animal had left water of approximately +1 °C (air temperature −7 °C). The grey area on the colour scale indicates the temperature of the isotherm (grey regions in the thermogram) at 15.7 °C. In the lower left-hand corner of the thermogram, the black colour indicates the temperature of ice (SP 5=−2 °C) adjacent to the pool. The inset in the upper right-hand corner shows a seal stationing on a target during infrared recording. Temperatures of greater than 18 °C, which appear pink in the thermogram, are where the majority of vibrissal follicles are oriented almost vertically from their mouth to the focal plane of the camera. Because of the domed shape of the muzzle, follicles outside this high-temperature area are increasingly inclined to the focal plane so that the camera misses direct radiation (dark red areas). The same is true for the surface temperatures of the supraorbital vibrissal pads (SP 3). SP 1, the top of the muzzle; SP 2, the nose; SP 4, vibrissal hair shafts; AR 1, the mystacial vibrissal pad.

Fig. 5.

Infrared thermogram showing the typical distribution of temperatures measured on the surface of a seal’s face immediately after the animal had left water of approximately +1 °C (air temperature −7 °C). The grey area on the colour scale indicates the temperature of the isotherm (grey regions in the thermogram) at 15.7 °C. In the lower left-hand corner of the thermogram, the black colour indicates the temperature of ice (SP 5=−2 °C) adjacent to the pool. The inset in the upper right-hand corner shows a seal stationing on a target during infrared recording. Temperatures of greater than 18 °C, which appear pink in the thermogram, are where the majority of vibrissal follicles are oriented almost vertically from their mouth to the focal plane of the camera. Because of the domed shape of the muzzle, follicles outside this high-temperature area are increasingly inclined to the focal plane so that the camera misses direct radiation (dark red areas). The same is true for the surface temperatures of the supraorbital vibrissal pads (SP 3). SP 1, the top of the muzzle; SP 2, the nose; SP 4, vibrissal hair shafts; AR 1, the mystacial vibrissal pad.

As expected from heat-loss models (Hokkanen, 1990; Watts et al. 1993; Kvadsheim et al. 1997), most of a seal’s head showed rather low levels of thermal radiation. The turquoise and grass-green colour of the top of the muzzle (SP 1, see Fig. 5), the nose (closed nostrils, SP 2), the cheeks and the skull indicated surface temperatures of 2.7–6.0 °C. Well defined against these cold skin regions were narrow areas (yellow) with temperatures of 8.0–10.0 °C surrounding the eyes and supraorbital vibrissal pads, as well as the mystacial vibrissal pads. Eyeball temperature was outside the range of measurement (>18.9 °C, white). An isotherm tool (grey regions) revealed the temperature of the adjacent skin to be 15.7 °C (isotherm width 0.3 °C). The same isotherm encircled all the areas of highest thermal radiation on the seal’s face, the central areas of the mystacial vibrissal pads. The red colour outside the isotherm indicated the mean surface temperature of the mystacial (measured in AR 1) and supraorbital (SP 3) vibrissal pads to be approximately 15 °C, and the mystacial areas inside the isotherm appeared as hot spots on the muzzle of a seal. These areas showed a skin temperature of 18.1 °C, which was more than 25 °C above the air temperature, 17 °C above the water temperature and more than 12 °C above the highest temperature measured at the periphery of the head. In contrast, the surface temperature of 0.9 °C measured for the vibrissal hair shafts (SP 4) was equal to that of the water.

Since it has been suggested that the vibrissal system of pinnipeds plays a major role in underwater orientation and foraging (Oliver, 1978; Hyvärinen, 1989; Dehnhardt and Kaminski, 1995), it was to be expected that seals possess adaptations to prevent the loss of tactile sensitivity under thermally hostile conditions. However, with respect to their thermoregulatory needs, the way in which they have solved the problem is somewhat surprising. Because of their unfavourable surface area to body mass ratio (compared with baleen whales, for example) and the high conductivity and specific heat of water, seals are in danger of hypothermia when exposed to low water temperatures and should therefore avoid heat dissipation (Hokkanen, 1990; Kvadsheim et al. 1997). As a corollary, during seasonal temperature changes, the blubber layer of most phocid seals, which also serves as an energy reserve, is depleted in a way that always maximizes insulative effectiveness (Ryg et al. 1988; Slip et al. 1992; Rosen and Renouf, 1997). However, our infrared thermographic examination revealed that, contrary to the dictate of thermal economy, the mystacial and supraorbital vibrissal pads are areas of excessive heat loss. While the drastic reduction of superficial blood circulation in seals is a major way of counteracting heat loss, the high temperatures measured at the surfaces of the vibrissal pads vividly demonstrate that no vasoconstriction occurs in these sensory areas during cold acclimation. Thermally clearly defined against the rest of the head, the blood supply to these areas must be highly localized, suggesting the existence of a separate vibrissal blood circulation. A recent anatomical study demonstrated that such specialized vascular systems do exist in seals. The intra-abdominal testes of male seals are at hyperthermic risk and need to be cooled to maintain the production of viable sperm. The animals solve this problem with a localized blood supply, but in this case bringing cold superficial venous blood via the inguinal venous plexus to the testes (Rommel et al. 1995). Temporary abdominal cooling has also been demonstrated in foraging king penguins and is thought to be a physiological adaptation to extended breath-holding during diving (Handrich et al. 1997). The present finding of regional heating in a cold peripheral region once more demonstrates that thermoregulation in marine endotherms must be considered as an active process selectively adjusted to the particular needs of certain body regions.

Selective heating of cranial neural structures has also been demonstrated in several oceanic fish (e.g. tuna and billfish; Block and Franzini-Armstrong, 1988; Block et al. 1993; Block, 1994). However, unlike the absence of cold-induced vasoconstriction demonstrated for the vibrissal system of seals, these heterothermic vertebrates possess local heat generators, modified from eye muscles, that warm their brain and eyes. Since this cranial endothermy evolved independently in different lineages, always in association with a movement into colder waters, Block et al. (1993) suggested that it was an adaptation permitting thermal niche expansion, a hypothesis that may also explain vibrissal heating not only in seals but probably also in other mammals.

Although the vascular architecture making it possible for seals to provide their vibrissae with warm blood remains obscure, the permanent filling of the follicle sinus system (Fig. 1B) guarantees an appropriate operating temperature for the mechanoreceptors located there. For example, in axons terminating at rapidly adapting Pacinian corpuscles, the amplitude of the action potential decreases sharply below 20 °C, while at temperatures below 15 °C the action potential often disappears (Inman and Peruzzi, 1961; Ishiko and Loewenstein, 1961; Necker, 1983). However, a temperature of approximately 18 °C at the surface of the mystacial pads indicates a substantially higher temperature at deeper levels inside the follicle; most receptors occur in the area of the ring sinus, approximately 1 cm away from the mouth of the follicle. In this respect, the present results provide for the first time an explanation for the function of the upper cavernous sinus (see Fig. 1B), which is unique to the vibrissal follicles of pinnipeds (for comparison with other mammals, see Rice et al. 1986). This sinus, which extends for approximately 60 % of the total length of the follicle (Hyvärinen and Katajisto, 1984), is free of any innervation and thus may serve primarily as a thermal insulator for the receptor area below it. However, the absence of cold-induced vasoconstriction in the vibrissal pads may serve not only to maintain the appropriate operating temperature for mechanoreceptors but also to ensure that the follicles are continuously provided with the oxygen and metabolites that are essential for these sensory units.

An adequate heat supply is important not only for the functioning of mechanoreceptors but also for the mechanical properties of the surrounding tissue. Cooling of the vibrissal pads would increase tissue stiffness which, in turn, should have a negative effect on the mobility of vibrissae and thus on the transduction of mechanical stimulation via the hairshaft to the receptor (Lederman, 1976; Green et al. 1979). With regard to such effects of tissue cooling, the unusual fatty acid composition of the adipose tissue around the mystacial and supraorbital vibrissal follicles of phocids may represent an additional adaptation to low ambient temperatures. The excess low-melting-point monoenoic fatty acids found in the adipose tissue near the vibrissae is thought to maintain adequate fat fluidity and thus the mobility of the vibrissae (Käkelä and Hyvärinen, 1993, 1996).

The fact that seals do not allow cooling of their vibrissae may demonstrate that, without this adaptation, this tactile system would be subject to the same deficiencies known for the human hand in response to cooling. Heat loss from these comparatively small skin regions is the energetic price a seal must pay to keep its vibrissal system working. This indicates that permanent access to tactile information is of biological importance for these marine mammals.

We are indepted to J. Thiesbrummel (AGEMA) for providing the Thermoscanner. Thanks are also due to H. Bleckmann for his support during this study. Together with F. Trillmich, S. Oetting and I. Röbbecke, he also provided valuable comments on the manuscript. The Deutsche Forschungsgemeinschaft (DFG) supported this study with a grant to G.D.

Block
,
B. A.
(
1994
).
Thermogenesis in muscle
.
A. Rev. Physiol.
56
,
535
577
.
Block
,
B. A.
,
Finnerty
,
J. R.
,
Stewart
,
A. F.
and
Kidd
,
J.
(
1993
).
Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny
.
Science
260
,
210
214
.
Block
,
B. A.
and
Franzini-Armstrong
,
C.
(
1988
).
The structure of the membrane system in a novel muscle cell modified for heat production
.
J. Cell Biol.
107
,
1099
1112
.
Bolanowski
,
S. J.
, Jr
,
Gescheider
,
G. A.
,
Verillo
,
R. T.
and
Checkosky
,
C. M.
(
1988
).
Four channels mediate the mechanical aspect of touch
.
J. acoust. Soc. Am
.
84
,
1680
1694
.
Bolanowski
,
S. J.
, Jr
and
Verrillo
,
R. T.
(
1982
).
Temperature and criterion effects in a somatosensory subsystem: a neurophysiological and psychophysical study
.
J. Neurophysiol.
48
,
836
855
.
Dehnhardt
,
G.
(
1990
).
Preliminary results from psychophysical studies on the tactile sensitivity in marine mammals
. In
Sensory Abilities of Cetaceans
(ed.
J. A.
Thomas
and
R. A.
Kastelein
), pp.
435
446
.
New York
:
Plenum Press
.
Dehnhardt
,
G.
(
1994
).
Tactile size discrimination by a California sea lion (Zalophus californianus) using its mystacial vibrissae
.
J. comp. Physiol.
175
,
791
800
.
Dehnhardt
,
G.
and
Dücker
,
G.
(
1996
).
Tactual discrimination of size and shape by a California sea lion (Zalophus californianus)
.
Anim. Learning 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
.
Dehnhardt
,
G.
,
Sinder
,
M.
and
Sachser
,
N.
(
1997
).
Tactual discrimination of size by means of mystacial vibrissae in Harbour seals: in air versusunderwater
.
Z. Säugetierkd
.
62
(
Suppl. II
),
40
43
.
Folkow
,
L. P.
and
Blix
,
A. S.
(
1989
).
Thermoregulatory control of expired air temperature in diving harp seals
.
Am. J. Physiol.
257
,
R306
R310
.
Gellerman
,
L. W.
(
1933
).
Chance orders of alternating stimuli in visual discrimination experiments
.
J. Genet. Psychol.
42
,
206
208
.
Gescheider
,
G. A.
,
Thorpe
,
J. M.
,
Goodarz
,
J.
and
Bolanowski
,
S. J.
, Jr
(
1997
).
The effects of skin temperature on the detection and discrimination of tactile stimulation
.
Somatosens Mot. Res.
14
,
181
188
.
Green
,
B. G.
(
1977
).
The effect of skin temperature on vibrotactile sensitivity
.
Percept. Psychophys.
21
,
243
248
.
Green
,
B. G.
,
Lederman
,
S. J.
and
Stevens
,
J. C.
(
1979
).
The effect of skin temperature on the perception of roughness
.
Sensory Proc.
3
,
327
333
.
Handrich
,
Y.
,
Bevan
,
R. M.
,
Charrassin
,
J.-B.
,
Butler
,
P. J.
,
Pütz
,
K.
,
Woakes
,
A. J.
,
Lage
,
J.
and
Le Maho
,
Y.
(
1997
).
Hypothermia in foraging king penguins
.
Nature
388
,
64
67
.
Hokkanen
,
J. E. I.
(
1990
).
Temperature regulation of marine mammals
.
J. theor. Biol.
145
,
465
485
.
Hyvärinen
,
H.
(
1989
).
Diving in darkness: whiskers as sense organs of the ringed seal (Phoca hispida)
.
J. Zool., Lond.
218
,
663
678
.
Hyvärinen
,
H.
and
Katajisto
,
H.
(
1984
).
Functional structure of the vibrissae of the ringed seal (Phoca hispida, Schr
.).
Acta zool. Fenn
.
171
,
27
30
.
Inman
,
D. R.
and
Peruzzi
,
P.
(
1961
).
The effects of temperature on the response of Pacinian corpuscles
.
J. Physiol., Lond.
155
,
280
301
.
Irving
,
L.
(
1969
).
Temperature regulation in marine mammals
. In
The Biology of Marine Mammals
(ed.
H. T.
Andersen
), pp.
147
174
.
London
:
Academic Press
.
Ishiko
,
N.
and
Loewenstein
,
W. R.
(
1961
).
Effects of temperature on the generator and action potentials of a sense organ
.
J. gen. Physiol.
45
,
105
124
.
Johansson
,
R. S.
and
Vallbo
,
A. B.
(
1979
).
Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin
.
J. Physiol., Lond.
286
,
283
300
.
Käkelä
,
R.
and
Hyvärinen
,
H.
(
1993
).
Fatty acid composition of fats around the mystacial and superciliary vibrissae differs from that of blubber in the Saimaa ringed seal (Phoca hispida saimensis)
.
Comp. Biochem. Physiol
.
105B
,
547
552
.
Käkelä
,
R.
and
Hyvärinen
,
H.
(
1996
).
Site-specific fatty acid composition in adipose tissues of several northern aquatic and terrestrial mammals
.
Comp. Biochem. Physiol
.
115B
,
501
514
.
Kvadsheim
,
P. H.
,
Gotaas
,
A. R. L.
,
Folkow
,
L. P.
and
Blix
,
A. S.
(
1997
).
An experimental validation of heat loss models for marine mammals
.
J. theor. Biol.
184
,
15
23
.
Lamb
,
G. D.
(
1983
).
Tactile discrimination of textured surfaces: Psychophysical performance measurements in humans
.
J. Physiol., Lond.
338
,
551
565
.
Lederman
,
S. J.
(
1976
).
The ‘callus-thenics’ of touching
.
Can. J. Psychol.
30
,
82
89
.
Lederman
,
S. J.
and
Klatzky
,
R. L.
(
1987
).
Hand movements: a window into haptic object recognition
.
Cognitive Psychol.
19
,
342
368
.
Mackworth
,
N. H.
(
1953
).
Finger numbness in very cold winds
.
J. Appl. Physiol.
5
,
533
543
.
Mills
,
A. W.
(
1956
).
Finger numbness and skin temperature
.
J. Appl. Physiol.
9
,
447
450
.
Morley
,
J. W.
,
Goodwin
,
A. W.
and
Darian-Smith
,
I.
(
1983
).
Tactile discrimination of gratings
.
Exp. Brain Res.
49
,
291
299
.
Necker
,
R.
(
1983
).
The problem of bimodal receptors: responses to thermal stimuli
. In
Multimodal Convergences in Sensory Systems
(ed.
E.
Horn
), pp.
1
16
. Stuttgart: Gustav Fischer Verlag.
Oliver
,
G. W.
(
1978
).
Navigation in mazes by a grey seal, Halichoerus grypus(Fabricius)
.
Behaviour
67
,
97
114
.
øritsland
,
N. A.
,
Lentfer
,
J. W.
and
Ronald
,
K.
(
1974
).
Radiative surface temperatures of the polar bear
.
J. Mammal.
55
,
459
461
.
Phillips
,
P. K.
and
Heath
,
J. E.
(
1992
).
Heat exchange by the pinna of the African elephant (Loxodonta africana)
.
Comp. Biochem. Physiol.
101A
,
693
699
.
Randall
,
D.
,
Burggren
,
W.
and
Frensch
,
K.
(
1997
).
Eckert Animal Physiology: Mechanisms and Adaptations
.
New York
:
Freeman
.
Rice
,
F. L.
,
Mance
,
A.
and
Munger
,
B. L.
(
1986
).
A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle–sinus complexes
.
J. comp. Neurol.
252
,
154
174
.
Rommel
,
S. A.
,
Early
,
G. A.
,
Matassa
,
K. A.
,
Pabst
,
D. A.
and
Mclellan
,
W. A.
(
1995
).
Venous structures associated with thermoregulation of phocid seal reproductive organs
.
Anat. Rec.
243
,
390
402
.
Rosen
,
D. A. S.
and
Renouf
,
D.
(
1997
).
Seasonal changes in blubber distribution in Atlantic harbor seals: Indications of thermodynamic considerations
.
Mar. Mammal Sci.
13
,
229
240
.
Ryg
,
M.
,
Lydersen
,
N.
Knutsen
,
L. ø.
,
bjørge
,
A.
,
Smith
,
T. G.
and
Øritsland
,
N. A.
(
1993
).
Scaling of insulation in seals and whales
.
J. Zool., Lond.
230
,
193
206
.
Ryg
,
M.
,
Smith
,
T. G.
and
Øritsland
,
N. A.
(
1988
).
Thermal significance of the topographical distribution of blubber in ringed seals (Phoca hispida)
.
Can. J. Fish aquat. Sci.
45
,
985
992
.
Slip
,
D. J.
,
Gales
,
N. J.
and
Burton
,
H. R.
(
1992
).
Body mass loss, utilisation of blubber and fat and energetic requirements of male southern elephant seals, Mirounga leonina, during the moulting fast
.
Aust. J. Zool.
40
,
235
243
.
Stephens
,
R. J.
,
Beebe
,
I. J.
and
Poulter
,
T. C.
(
1973
).
Innervation of the vibrissae of the California sea lion, Zalophus californianus
.
Anat. Rec.
176
,
421
442
.
Stevens
,
J. C.
,
Green
,
B. G.
and
Krimsley
,
A. S.
(
1977
).
Punctate pressure sensitivity: effects of skin temperature
.
Sensory Processes
1
,
238
243
.
Verrillo
,
R. T.
and
Bolanowski
,
S. J.
, Jr
(
1986
).
The effects of temperature on the psychophysical responses of vibration on glabrous and hairy skin
.
J. Acoust. Soc. Am.
80
,
528
532
.
Watts
,
P.
,
Hansen
,
S.
and
Lavigne
,
D. M.
(
1993
).
Models of heat loss by marine mammals: Thermoregulation below the zone of irrelevance
.
J. theor. Biol.
163
,
505
525
.
Worthy
,
G. A. J.
(
1991
).
Insulation and thermal balance of fasting harp and grey seal pups
.
Comp. Biochem. Physiol.
100A
,
845
851
.