Journal of Experimental Marine Biology and Ecology 452 (2014) 111–118

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Journal of Experimental Marine Biology and Ecology

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Thermoregulation of the vibrissal system in harbor seals (Phoca vitulina)and Cape fur seals (Arctocephalus pusillus pusillus)

Nicola Erdsack, Guido Dehnhardt, Wolf Hanke ⁎University of Rostock, Institute for Biosciences, Sensory & Cognitive Ecology, Albert-Einstein-Strasse 3, D-18059 Rostock, Germany

Abbreviations: CS, Cavernous sinus; F–SC, Follicle–siAmbient air temperature; Tdiff, Temperature difference;vibrissal follicles; Tmax, Maximum temperature; Tmea

Minimum temperature; Trange, Temperature range; TsFur surface temperature; Twater, Ambient water tempe⁎ Corresponding author. Tel.: +49 381 498 6010; fax: +

E-mail addresses: nicola.erdsack@uni-rostock.de (N. Eguido.dehnhardt@uni-rostock.de (G. Dehnhardt), wolf.han

0022-0981/$ – see front matter © 2013 Elsevier B.V. All rhttp://dx.doi.org/10.1016/j.jembe.2013.12.011

a b s t r a c t

a r t i c l e i n f o

Article history:Received 9 October 2013Received in revised form 16 December 2013Accepted 17 December 2013Available online 11 January 2014

Keywords:Cape fur sealFollicle–sinus complexHarbor sealPinnipedsThermoregulationVibrissae

The vibrissal system is a very important sensory system in pinnipeds. Therefore it is essential for the animalsto maintain its functionality under all environmental conditions. Particularly low ambient temperatures pose agreat demand to tactile sensitivity, which seals solve by selective heating of the vibrissal pads. This means,adversely, a source of heat loss for the animal. Depending on foraging habits, climate of the habitat and degreeof adaptation to the aquatic lifestyle we proposed that there are differences in the level of heating of vibrissalfollicles between seal species. Since tactile sensitivity in harbor seals (Phoca vitulina) is not affected by ambienttemperature, we hypothesized that also the temperature within their vibrissal follicles is not influenced by am-bient temperature. For the first time we measured temperature inside the vibrissal follicles of a mammal, here,the harbor seal.Measurementswere taken under different environmental conditions in summer andwinter. Fur-thermore we conducted comparative measurements of skin and fur surface temperature on the vibrissal pads inharbor seals and a Cape fur seal (Arctocephalus pusillus pusillus) over a period of one year. In harbor seals follicletemperature was constant and independent of ambient temperature, while skin temperature on the vibrissalpads was weakly correlated to water temperature. Contrarily, vibrissal pad skin temperature of the fur sealwas strongly correlated to water temperature, though it was significantly higher than in the harbor seals. Inboth species fur surface temperature was strongly correlated to water temperature. We presume that, due totheir different lifestyles, foraging habits and thermal insulation, these species have developed different heatingmechanisms for their tactile sense. While the more aquatic harbor seals keep vibrissal follicle temperature at aconstant level, the more terrestrial Cape fur seals appear to heat their vibrissal follicles with a more constantpower, which results in a dependency on ambient temperature.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

The vibrissal system is an important tactile sensory system which ispresent in all mammals, except for primates and humans. In particularfor aquatic mammals, often confronted with limited visibility in darkor murky waters, the reception of mechanosensory information isoften essential, including information from direct touch of objects andthe reception of water movements. Pinnipeds obtain hydrodynamicinformation by detecting water movements with their vibrissae(Dehnhardt et al., 1998a). They can use this information to follow thetrails of prey (Dehnhardt et al., 2001; Wieskotten et al., 2010, 2011) orconspecifics (Schulte-Pelkum et al., 2007). Furthermore pinnipeds areable to detect, recognize and discriminate objects of different sizes and

nus complex; IR, Infrared; Tair,Tfollicle, Temperature inside then, Mean temperature; Tmin,kin, Skin temperature; Tsurface,rature.49 381 498 6302.

rdsack),ke@uni-rostock.de (W. Hanke).

ights reserved.

shapes (Dehnhardt, 1994; Dehnhardt and Dücker, 1996; Dehnhardtand Kaminski, 1995; Dehnhardt et al., 1997; Kastelein and van Gaalen,1988) by active touch. Vibrissae also play an important role in socialcontacts between conspecifics, particularly in themother–pup relation-ship (Evans and Bastian, 1969).

In contrast to other mammals, such as the sirenia with vibrissae onthe entire body surface (Reep et al., 2011), in pinnipeds the vibrissaeare located exclusively in the face region: the mystacial vibrissaevary in number between species, from 15 up to 350 per body side(Hyvärinen et al., 2009; Ling, 1977; Yablokov and Klevezal, 1962) andare arranged in rows on the vibrissal pads on each side of the muzzle.Two to nine supraorbital vibrissae (Ling, 1966) are located above eacheye. Phocids additionally possess one rhinal vibrissa above each nare.Vibrissae emanate from follicle-sinus complexes (F-SCs), which com-prise large blood-filled sinuses, are highly innervated, and show inter-specific anatomical variations (Ebara et al., 2002). Pinniped vibrissalF–SCs are especially strongly innervated (about ten times more thanin other mammals) (Hyvärinen and Katajisto, 1984; Marshall et al.,2006), highly endowed with mechanoreceptors (Hyvärinen, 1989) andamply supplied via blood sinuses (Hyvärinen, 1989; Hyvärinen andKatajisto, 1984; Ling, 1977). Pinniped vibrissal F–SCs can reach 2 cm in

112 N. Erdsack et al. / Journal of Experimental Marine Biology and Ecology 452 (2014) 111–118

length (Hyvärinen, 1989; Hyvärinen and Katajisto, 1984; Marshall et al.,2006). Due to the requirements of the habitat and the degree of adap-tation to the aquatic environment, development and structure of thevibrissal system as well as the single vibrissae differs highly betweenpinniped species. In phocids the vibrissal pads consist of blubberwith a specific fatty acid composition and density that differs fromthe blubber on other body parts (Käkelä and Hyvärinen, 1993), andare covered with short hairs (Erdsack et al., in prep.). In otariidvibrissal pads blubber abundance and composition have not beendescribed so far, but the pads are covered with dense fur of similardensity as the fur on the trunk and, like on the trunk, consisting ofguard hairs and underfur (pers. obs.). Phocid vibrissae have a flattenedundulated structure (Hanke et al., 2010; Hyvärinen and Katajisto,1984), except for the bearded seal (Erignathus barbatus (Erxleben,1777)) and the monk seals (Monachus spp.), and are renewed annuallyduringmolt (Hirons et al., 2001; pers. obs.). Contrarily, otariid vibrissaehave an oval diameter with a smooth outline, are not molted annually,and grow very slowly (Hirons et al., 2001), but up to more than 45 cmlength (Bonner, 1981). Like the structural differences in the vibrissalsystems, the capabilities of the vibrissal systems vary between species.Harbor seals (Phoca vitulina Linnaeus, 1758), for example, have betterabilities in trail following in the water (Dehnhardt et al., 2001) thanCalifornia sea lions (Zalophus californianus Lesson, 1828) (Gläser et al.,2011).

An important factor for the functionality of tactile sensory systemsis the temperature of the receptors, which often depends strongly onambient temperature. Tactile sensitivity in humans decreases severelywith decreasing skin temperature (Gescheider et al., 1997; Green,1977; Green et al., 1979; Mackworth, 1953, 1955; Mills, 1956; Stevensand Hooper, 1982; Stevens et al., 1977). Particularly in pinnipeds,which are distributed even in polar regions, low air and water temper-atures pose a great challenge to the functionality of the tactile sense.Käkelä and Hyvärinen (1993, 1996) found fatty acid compositions inthe blubber of the vibrissal pads of ringed seals (Phoca hispida Schreber,1775) differing from the blubber in all other parts of the body, and pre-sumed a possible adaptation to the functioning of the vibrissal sense incold temperatures. Dehnhardt et al. (1998b) found in a psychophysicalstudy that the tactile sensitivity of harbor seal vibrissae is not affectedby low water temperatures down to 1.2 °C. Harbor seals achieve thisby selective heating of the vibrissal follicles, as Mauck et al. (2000)found by using infrared thermography. It was not known so far if a sim-ilar mechanism is also present in otariids.

Since few comparative data are available for otariid seals, we setout to answer the following related questions: Do harbor seals, asrepresentatives of phocids, maintain a constant temperature withintheir F-SCs, independent of ambient temperature, and to whatdegree? Do fur seals, as representatives of otariids, heat their F-SCsas well?

We hypothesized that in harbor seals, given their high degree of ad-aptation to the aquatic environment and their good tactile performanceat lowwater temperatures, the temperaturewithin the vibrissal folliclesis constant and independent of ambient temperatures. To test thishypothesis we measured the temperature within vibrissal follicles oftwo adult harbor seals in summer andwinter bymeans of a thermocou-ple, which was inserted into empty vibrissal follicles. Empty follicleslacking hair shafts are often found duringmolt, and occasionally outsidemolt. Our second hypothesis was that fur seals heat their vibrissal folli-cles aswell, but not to the same extent as harbor seals, given their lowerdegree of adaptation to the aquatic environment compared to harborseals. Otariids do not molt their vibrissae regularly like phocids(Hirons et al., 2001), therefore no follicles without hair shafts wereavailable for temperature measurements inside and we had to restrictour measurements to the skin temperature close to the vibrissal folli-cles. We measured skin temperature in a Cape (South African) fur seal(Arctocephalus pusillus pusillus Schreber, 1776) and conducted compar-ative measurements in four harbor seals.

2. Materials and methods

2.1. Experimental animals

The study was carried out in four adult male harbor seals (Nick, Sam,Henry and Luca) aged nine to eighteen years, as well as one subadultmale Cape fur seal (Fin), aged three to four years during the study period.All animals were kept in an open water enclosure (30 m ∗ 60 m ∗ 2 to6 m depth) within the Baltic Sea, exposed to the environmental condi-tions of a natural habitat.

2.2. Temperature measurements

Temperature within the follicles (follicle temperature, Tfollicle) as wellas skin temperature of the vibrissal pads (Tskin) were measured witha mantle thermocouple (TKAL 05030, mawi-therm GmbH, Monheim,Germany; mantle diameter: 0.5 mm, nominal length: 30 mm) attachedto a digital quick response thermometer (GTH 1170, Greisinger electron-ic GmbH, Regenstauf, Germany). For measurements of Tfollicle, the ther-mocouple was inserted 5 to 6 mm into follicles lacking hair shafts(Fig. 1A). Most empty follicles were present during molt throughoutJuly and August to beginning of September. Tfollicle was measured intwo animals while all other measurements were conducted in all fourharbor seals and the fur seal. For measurements of Tskin, in harbor sealsthe tip of the thermocouplewas placed perpendicularly onto the skin ap-proximately 1 mm from the vibrissal shaft (Fig. 1C). For measurementsof Tskin in the fur seal, the tip of the thermocouple was inserted into thefur next to and parallel to a vibrissa (vibrissae protrude in an obliqueangle in resting position, see Fig. 1B) and placed onto the skin directlyadjacently below the vibrissal shaft Fig. 1D.

For the measurements of follicle and vibrissal pad surface tempera-ture (Tsurface), i. e. the temperature at the opening of an empty follicle,and for the fur surface at the vibrissal follicle, an infrared (IR) laser ther-mometer (Fluke 561, Eindhoven, The Netherlands, temperature range:−40 °C to 550 °C, emissivity: 0.95) was used to collect pinpoint tem-perature measurements. An IR thermocamera (Fluke Ti25, Eindhoven,The Netherlands) was used to visualize and measure the temperaturedistribution of the entire vibrissal pad.

Air and water temperature (Tair, Twater) weremeasured with a man-tle thermocouple (Greisinger Electronic GmbH, Regenstauf, Germany)attached to the digital quick response thermometer described above.

2.3. Experimental procedure

Measurements were carried out continuously from May 2011to March 2012. A range of water temperatures of 19.4 K (0.8 °C to20.2 °C) was covered, including the annual temperature minimumand maximum. All measurements took place in the shade or underovercast skies.

Animals had to stay in the water for at least 30 min prior to thebeginning of themeasurement. Immediately before eachmeasurementthe animal had to station in a hoop station 1 m below thewater surfacefor 30 s. After that the animal was called onto land and stationed withits chin on a target. Measurement of Tfollicle or Tskin started at oncewith a maximum delay of 5 s after the seal left the water. Immediatelyafterwards Tsurface was measured. After the measurement the seal wasrewarded with fish and sent back into the water. Twater was measuredat the hoop station and Tair was measured close to the ground, wherethe animal was to station. Additional measurements of Tskin and Tsurfaceof the vibrissal padswere carried out in hauled out sealswith completelydry fur.

The experiments were carried out in accordance with the EuropeanCommunities Council Directive of 24November 1986 (86/609/EEC). Ac-cording to § 8 of the German AnimalWelfare Act of 18May 2006 (BGB l.I S. 1206, 1313), experiments conducted in this study were neither

C D

F-SC F-SC

skin skinfur

A B

Fig. 1.Details of seals' vibrissal padswithwet fur, andmethod of skin temperaturemeasurement. A)Harbor seal duringmolt. B) Cape fur seal. A) The yellow arrowmarks an empty folliclewhere the old vibrissa had been shed but the new vibrissa had not yet emerged. The follicle mouth is clearly protruded. Follicles in this state were used for measurements of temperatureinside the follicle (Tfollicle). Above and on the left side new vibrissae already emerged but had not reached final length. The vibrissae's undulated outline is clearly visible. B) Red arrowsmark the areas where the vibrissa shafts emerge from the fur, the guard hair splits and the light beige underfur is visible. Follicle mouths and basal parts of the vibrissa shafts are coveredby the fur and are not visible. The smooth outline of the vibrissae is visible. C) In harbor seals, the thermocouple (blue) was placed perpendicularly onto the skin within approximately1 mm from the vibrissa (gray). D) In the fur seal, the thermocouple (blue) was inserted into the dense fur parallel to a vibrissa and placed onto the skin directly adjacently below thevibrissal shaft (gray).

113N. Erdsack et al. / Journal of Experimental Marine Biology and Ecology 452 (2014) 111–118

notifiable nor subject to approval, since they did not cause pain, suffer-ing or injuries to the animals.

2.4. Data analysis

Statistical analyses were carried out with SPSS 20.0 and MicrosoftExcel 2003. Data were tested for normal distribution by means of achi2-test and for equality of variances by means of an f-test. Statisticaldependence between values was calculated using Spearman's rankcorrelation coefficient (rs) and its probability of deviating from zeroby chance (p). Statistical significance of differences of mean valueswas tested for normally distributed data using one-tailed or two-tailedt-tests, and for not normally distributed data using a Mann–WhitneyU-test or a Wilcoxon-Test for paired samples (surface temperatureof the fur seal's vibrissal pads). Significance level in all cases wasα = 0.05. Thermograms from the IR thermocamera were analyzedwith Smartview 3.2 software (Fluke, Eindhoven, The Netherlands).

3. Results

Water temperature ranged from 0.8 °C to 20.2 °C and air tempera-ture from−6.0 °C to 27.9 °C during the study period. Minimum, maxi-mum and mean values of Tfollicle, Tskin and Tsurface of the vibrissal pads

are given in Table 1. Also presented in Table 1 are temperature ranges,standard deviation and temperature difference between skin and sur-face for the harbor seals and the fur seal. Fig. 2 shows exemplary ther-mograms of the face region of a harbor seal (A) and the fur seal (B),immediately after leaving the water.

3.1. Impact of water temperature

3.1.1. Harbor sealsA total of 39measurements of Tfollicle aswell as 308measurements of

Tskin and 306 measurements of Tsurface were conducted on the vibrissalpads of the harbor seals. Fig. 3 shows Tfollicle, Tskin and Tsurface after 30 sof diving at 1 m depth as functions of Twater along with linear regres-sions. Tfollicle was constant with a mean value of 31.7 ± 2.7 °C(N = 39) and was not correlated to Twater (rs = 0.06; p = 0.71; slopeof regression:−0.0001). Tskin was highly significantly lower than Tfollicle(p b b0.0001) with a mean value of 27.3 ± 2.6 °C (N = 308) and arelatively weak correlation to Twater (rs = 0.31; p b 0.001; slope ofregression: 0.12). Tsurface was highly significantly lower than Tskin(p b b0.0001) with a mean temperature of 13.9 ± 5.6 °C (N = 306)and a strong positive correlation to Twater (rs = 0.81; p b 0.001; slopeof regression: 0.82). Tskin and Tsurface were weakly correlated witheach other (rs = 0.26; p b 0.001).

Table 1Vibrissal pad temperatures inharbor seals and a Cape fur seal.Minimum(Tmin),maximum(Tmax) and mean (Tmean) temperature measured within the vibrissal follicles (Tfollicle), onthe skin (Tskin) and on the surface (Tsurface) of the vibrissal pads of four harbor seals and aCape fur seal along with temperature range (Trange), standard deviation (sd), number ofmeasurements (N) and temperature difference between skin and surface (Tdiff). Data aresorted by seal species and measurement situation: after diving (wet) and while haulingout with completely dry fur (dry).

Temperature Tmin [°C] Tmax [°C] Trange [K] Tmean ± sd [°C] N

Harbor sealsWet Tfollicle 27.8 37.2 9.4 31.7 ± 2.7 39

Tskin 19.0 32.9 13.9 27.3 ± 2.6 308Tsurface 2.0 26.2 24.2 13.9 ± 5.6 306Tdiff 0.6 26.9 26.3 14.2 ± 5.2 269

Dry Tskin 25.8 37.6 11.8 32.0 ± 2.8 26Tsurface 14.4 34.6 20.2 22.6 ± 5.4 29Tdiff 4.6 18.0 13.4 10.4 ± 3.2 26

Fur sealWet Tskin 23.3 36.0 12.7 31.7 ± 3.0 181

Tsurface 6.5 30.3 23.8 16.7 ± 6.0 181Tdiff 4.3 25.5 21.2 15.1 ± 4.6 178

Dry Tskin 24.2 38.0 13.8 33.3 ± 2.7 35Tsurface 6.5 34.4 27.9 20.0 ± 7.2 33Tdiff 1.6 22.0 20.4 13.2 ± 5.6 33

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Fig. 3. Harbor seals after diving. Tfollicle (triangles, continuous regression line, N = 39) aswell as Tskin (circles, long dashed regression line, N = 308) and Tsurface (crosses, shortdashed regression line, N = 306) of the vibrissal pads of harbor seals after diving as func-tions of Twater, alongwith linear regressions. Tfolliclewas constant with a slope of regressionclose to zero (−0.0001) and not correlated to Twater (rs = 0.06, p = 0.71). Tskin was rela-tively weakly correlated to Twater (rs = 0.31, p b 0.001; slope of regression line 0.12)while Tsurface had a strong correlation to Twater (rs = 0.81; p b 0.001) with a steep slopeof regression (0.82). Tfollicle was significantly higher than Tskin (p b b0.0001).

114 N. Erdsack et al. / Journal of Experimental Marine Biology and Ecology 452 (2014) 111–118

Tskin of left and right vibrissal pads did not differ significantly, neitherin all four animals pooled nor within one individual. Tskin furthermoredid not differ between the vibrissal pads of three animals, but one indi-vidual, Luca, had a significantly lower mean Tskin than the others(p b 0.0005).

The temperature difference between skin and surface of the harborseals' vibrissal pads ranged from 0.6 to 26.9 K (14.2 ± 5.2 K) and corre-lated negatively to Twater (rs = −0.60; p b 0.001; slope of regression:−0.69). Skin-surface temperature differences in the harbor seals incomparison to the fur seal after diving are shown in Fig. 4 as functionsof Twater along with linear regressions. Mean temperature differencedid not differ between harbor seals and fur seal (p = 0.09).

3.1.2. Cape fur sealThe measurements on the vibrissal pads of the fur seal resulted in

181 recordings each of Tskin and Tsurface. Due to the fact that fur sealsdo not molt their vibrissae regularly and the vibrissae grow very slowly(pers. obs.; similar to other otariid species (Hirons et al., 2001)), noempty vibrissal follicles were found and no measurements of Tfolliclecould be performed. In contrast to the harbor seals, the fur seal featureda difference in Tskin between the right and the left vibrissal pad. MeanTskin of the right vibrissal pad (32.5 ± 2.7 °C, N = 87)was significantlyhigher (p b 0.001) than on the left side (30.9 ± 3.1 °C, N = 94). AlsoTsurface was significantly higher (p = 0.001) on the right vibrissalpad (17.1 ± 5.8, N = 87) than on the left vibrissal pad (16.3 ± 6.2,N = 94). In Fig. 5 Tskin and Tsurface of both vibrissal pads of the fur seal

Fig. 2. Typical infrared thermograms of the faces of seals. A) A harbor seal and B) a Cape fur sevibrissal pads, the inside of the nostrils (in the fur seal the nostrils are closed) as well as the ar

are plotted against Twater, alongwith linear regressions. Correlations be-tween Tskin and Twater were found on each side as well as in the pooleddata from both sides (Tskin right side: rs = 0.57; Tskin left side:rs = 0.67; Tskin both sides: rs = 0.59; p b 0.001 for all) with similarslopes of regression (left side: 0.33; right side: 0.27). Also Tsurface wasstrongly correlated to Twater (rs = 0.86; p b 0.001; slope of regression:0.89).

Tskin and Tsurface were highly significantly higher in the fur seal thanin the harbor seals (p b 0.0001). Furthermore Tskin and Tsurface werestronger correlated with each other in the fur seal than in the harborseals (left vibrissal pad: rs = 0.70, right vibrissal pad: rs = 0.67 bothvibrissal pads: rs = 0.67; p b 0.001 for all). Similar to the harbor seals,the difference between Tskin and Tsurface of the vibrissal padswas strong-ly negatively correlated to Twater (rs = −0.73; p b 0.001; slope of re-gression: −0.58), as shown in Fig. 4. The skin-surface temperaturedifference in the fur seal did not differ from that in the harbor seals(p = 0.09).

3.2. Impact of air temperature while hauling out

3.2.1. Harbor sealsIn addition to the temperature measurements in the vibrissal pads

after the animals had been submerged in the water, a total of 26 mea-surements of Tskin and 29 measurements of Tsurface were conducted inthe vibrissal pads of hauled out harbor seals with completely dry fur.

al, immediately after diving (Twater = 0 °C). Warmest areas were the eyes, the mystacialea at the supraorbital vibrissae.

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Fig. 4. Harbor seals and fur seal after diving. Difference between Tskin and Tsurface of thevibrissal pads of the harbor seals (empty diamonds, dashed regression line, N = 269)and the fur seal (dots, continuous regression line, N = 178) as functions of Twater, alongwith linear regressions. The skin-surface temperature difference did not differ significantlybetween harbor seals and fur seal (p = 0.09). In both species temperature differenceswere strongly negatively correlated to Twater (Phoca vitulina: rs = −0.60, p b 0.001; slopeof regression: −0.69; Arctocephalus pusillus: rs = −0.73; p b 0.001; slope of regression:−0.58).

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Ap

Pv

Ap

Fig. 6.Harbor seals and fur seal with dry fur. Tskin of the harbor seals (circles, short dashedregression line Pv, N = 26) and the fur seal (dots, continuous regression line Ap, N = 35)as well as Tsurface of the harbor seals (empty triangles, dashed dotted regression linePv, N = 29) and the fur seal (filled triangles, long dashed regression line Ap, N = 33)with completely dry vibrissal padswhile hauling out, as functions of Tair, alongwith linearregressions. While Tskin of the harbor seals was not significantly correlated to Tair(rs = 0.31; p = 0.12), Tskin of the fur seal was strongly correlated to Tair (rs = 0.77;p b 0.001). Tsurface of the dry vibrissal pads of both species were correlated to Tair (Phocavitulina: rs = 0.55, p = 0.004; Arctocephalus pusillus: rs = 0.88; p b 0.001), in the furseal stronger than in the harbor seals. Slopes of regression lines of Tskin were similar inboth species (P. vitulina: 0.34; A. pusillus: 0.29), whereas for Tsurface, the regression linewas much steeper in the fur seal (0.91) than in the harbor seals (0.61).

115N. Erdsack et al. / Journal of Experimental Marine Biology and Ecology 452 (2014) 111–118

Fig. 6 shows Tskin and Tsurface of the dry vibrissal pads of the hauledout harbor seals in comparison to the hauled out fur seal, plotted againstTair along with linear regressions. Tskin of the harbor seals' dry vibrissalpads had a mean value of 32.0 ± 2.8 °C (N = 26) without correlationto Tair (rs = 0.31; p = 0.12), while Tsurface (22.6 ± 5.4 °C, N = 29)was correlated to Tair (rs = 0.55; p = 0.004; slope of regression:0.61). Tskin of the dry vibrissal pads was significantly higher than ofthe wet vibrissal pads after being submerged (p b 0.0001). The meantemperature difference between skin and surface was 10.4 ± 3.2 Kwith a negative correlation to Tair (rs = −0.45; p = 0.02; slope ofregression:−0.27; not shown).

3.2.2. Cape fur sealA total of 35 measurements of Tskin and 33 measurements of Tsurface

were conducted in the vibrissal pads of the hauled out fur seal withcompletely dry fur.

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Fig. 5. Fur seal after diving. Tskin of the right (dots, continuous regression line, N = 87)and the left (diamonds, long dashed regression line, N = 94) vibrissal pad as well asTsurface of the right (triangles, short dashed regression line, N = 87) and the left vibrissalpad (circles, dashed dotted regression line, N = 94) of the fur seal after diving as functionsof Twater, along with linear regressions. Tskin and Tsurface were significantly higher on theright vibrissal pad than on the left side (Tskin: p b 0.001; Tsurface: p = 0.001). Both Tskinand Tsurface were strongly correlated to Twater (Tskin right side: rs = 0.57; Tskin left side:rs = 0.67; Tskin both sides: rs = 0.59; Tsurface right side: rs = 0.86; Tsurface left side:rs = 0.87; Tsurface both sides: rs = 0.86; p b 0.001 for all). Slopes of the regression lineswere Tskin right side: 0.27, Tskin left side: 0.33, Tsurface right side: 0.85 and Tsurface leftside: 0.94.

In dry state Tskin did not differ significantly between the right andthe left vibrissal pad and had a mean value of 33.3 ± 2.7 °C (N = 35)at Tair between −1.2 °C and 21.5 °C. In Fig. 6 Tskin and Tsurface of thedry vibrissal pads of the hauled out fur seal are plotted against Tairalong with linear regressions, in comparison to the harbor seals. Tskinwas significantly higher on the dry than on the wet vibrissal padsreported above (p = 0.003). Also Tsurface was higher on the dry vibrissalpads than after being submerged with a mean value of 20.0 ± 7.2 °C(N = 33; p = 0.01). Tskin of the fur seal's dry vibrissal pads was sig-nificantly higher than in the harbor seals (p = 0.02) while Tsurfaceon the dry vibrissal pads did not differ from that in the harbor seals(p = 0.12). But, in contrast to the harbor seals Tskin of the dry vibrissalpads of the fur seal was strongly positively correlated to Tair (rs = 0.77,p b 0.001; slope of regression: 0.29) and Tsurface showed a stronger corre-lation to Tair (rs = 0.88, p b 0.001; slope of regression: 0.91) than inthe harbor seals. Also the difference between Tskin and Tsurface had astronger negative correlation to Tair (r = −0.80, p b 0.001; slope of re-gression:−0.62; not shown) in the fur seal than in the harbor seals.

4. Discussion

The results of themeasurements within the vibrissal follicles of har-bor seals confirm our hypothesis that Tfollicle is independent of ambientwater temperature. Although there was a variability of about 9 K, meanvalues during summer with water temperatures between 15.9 °C and19.6 °C and during winter with 1.8 °C to 4.1 °C were equal to themean value of all measurements pooled (31.7 °C). A possible reasonfor the variability could be differences in physical activity before themeasurements. Tskin of the harbor seals' vibrissal pads was about 14%lower than Tfollicle, but was also relatively constant with a weak correla-tion to Twater and a standard deviation b 10%. These results show thatnot only the vibrissal follicles are heated, probably in order to maintaintactile sensitivity (Dehnhardt et al., 1998b), but also the entire vibrissalpads, presumably by heat conduction from the follicles.

One characteristic of pinniped vibrissal follicle–sinus complexes(F–SCs) is the presence of an upper cavernous sinus (CS) (Hyvärinen,1989; Hyvärinen and Katajisto, 1984; Marshall et al., 2006; Stephenset al., 1973), as shown in Fig. 7. The upper CS is lacking not only in the

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F–SCs of terrestrial mammals (Ebara et al., 2002; Hyvärinen et al., 2009;Kim et al., 2011; Ling, 1977; Rice et al., 1986), but also in other semi-aquatic and aquatic mammalian species such as the European otter(Lutra lutra) (Hyvärinen et al., 2009) and the Sirenia (Sarko et al.,2007). Since this upper CS is not, or at the utmostmarginally, innervated(Ling, 1966), Hyvärinen (1989) speculated about an indirect insulatingfunction of the upper CS. The insulating value would in his view lie inthe increased distance of the ring sinus from the skin surface by thelarge upper CS. The ring sinus is the most important sensory area,while the lower CS contains nervous end organs as well (HyvärinenandKatajisto, 1984). Dehnhardt et al. (1998b) assumed a direct functionof the upper CS as thermal insulator by heating the subjacent receptors.In ringed seals (Phoca hispida saimensis Nordquist, 1899), which areclose relatives of the harbor seals investigated here, as well as in beard-ed seals the upper CS comprises up to 60% of the total follicle length(Hyvärinen and Katajisto, 1984; Marshall et al., 2006) and is separatedfrom the ring sinus by a collagenous membrane (Hyvärinen, 1989).Regarding the size of vibrissal follicles in the ringed seal, the upper CScovers the upper 6 to 12 mm of the follicle (Hyvärinen, 1989). Sinceour measurements were conducted at a depth of 4 to 5 mm inside thefollicle, we can act on the assumption that the values were obtaineddirectly at the “heater” of the tactile organ, and, according to this,where highest temperatures should appear. The short time span be-tween shedding and growth of the vibrissa of approximately twoweeks (pers. obs.) gives reason to assume that all structures otherthan the hair shafts are maintained more or less unchanged.

The description by Stephens et al. of the vibrissal F–SC of a Californiasea lion (Zalophus californianus) (Stephens et al., 1973) is similar to that

Fig. 7. Schematic drawing of a vibrissal follicle–sinus complex of a phocid seal (adaptedfrom Dehnhardt et al., 1998b). Total length is 1–2 cm. Ring sinus and lower cavernoussinus (lower CS) are the sensory area of the F–SC and cover about 40% of the F–SC length.The upper cavernous sinus (upper CS) contains no sensory elements and comprises about60% of total F–SC length.

of ringed seals (Hyvärinen, 1989; Hyvärinen and Katajisto, 1984) andbearded seals (Marshall et al., 2006), but differs in total size as well asthe relative size of the upper CS. Sea lion vibrissal F–SCs are approxi-mately half the length of those of ringed seals, with the upper CS shorterthan the lower CS (Stephens et al., 1973), covering only about 40%of the entire follicle length of about 1 cm (Ling, 1977) (comparedto 60% in the ringed seal (Fig. 7) and the bearded seal). Assumingthat the upper CS functions as thermal insulator for the subjacentsensory area of the follicle, this would imply that thermal insulationin the otariid is lower than in phocids for two reasons: the smallersize of the “heater” as well as the smaller distance between sensoryarea and skin surface. Together with the fur insulation of the vibrissalpads, which is in water less effective than in air due to the compres-sion of the air layer in the water, this could be an explanation for thedependency on water temperature of vibrissal pad temperature in thefur seal. Measurements within the vibrissal follicles of a fur seal wouldbe useful to clarify this question, but are difficult to implement, sinceotariids do not molt their vibrissae annually and therefore usually noempty follicles are available formeasurements. Therefore investigationsof vibrissal follicle structure as well as vibrissal pad temperature inother otariid species would be revealing, such as the Antarctic fur seal(Arctocephalus gazella (Peters, 1866)) that lives in polar regions withwater temperatures below 0 °C.

The findings in the hauled out seals with dry fur are consistent withthe values obtained in the diving seals. Mean Tskin in the hauled out har-bor seals as well as in the fur seal were significantly higher than afterdiving, but only in the fur seal a distinct correlation to Tair was found.This corresponds to the strong correlation between Tskin and Twater inthe fur seal after diving as well as the weak correlation between Tskinand Twater in the harbor seals after diving. Heat loss from dry vibrissalpads in air is reduced, even at low air temperatures, due to the muchlower specific heat capacity and thermal conductivity of air than ofwater as well as the lack of evaporative cooling, which explains thehigher Tskin in a dry state in air.

Tskin on the vibrissal pads of the fur sealwas significantly higher thanin the harbor seals, inwet aswell as in dry state. This results presumablyfrom the effective thermal insulation of the fur seal's dense pelage, cov-ering the entire vibrissal pads, including the vibrissal folliclemouths andthe basal parts of the vibrissae (Fig. 1B). The dense fur was presumablyalso responsible for the larger skin-surface temperature differences indry and wet state than in the harbor seals. However, the skin-surfacetemperature differences on the harbor seals' vibrissal pads indicate astrong insulating effect of the fur on the harbor seals' vibrissal pads aswell. Since the insulating value of harbor seal fur was regarded as neg-ligible (Irving and Krog, 1955) or if at all existent in dry state whilehauling out (Kvadsheim and Aarseth, 2002; Tarasoff and Fisher, 1970),this finding is somewhat surprising. Since none of these previous stud-ies included the fur at the seals' snouts, this is worth a closer look andtherefore object of a forthcoming paper (Erdsack et al., in prep.). Asseen in Fig. 1A, harbor seal vibrissal pads are covered with short and,compared to the fur seal, sparse pelage. A higher hair density on thevibrissal pads than on other body parts could be a useful adaptation toreduce heat loss. The remaining heat loss is tolerated by the seals infavor of keeping their tactile sense functional.

The lateral difference in Tskin and Tsurface found on the vibrissal padsof the fur seal after divingmay be an individual phenomenon. For a gen-eralized statement, more individuals have to be investigated. The sameapplies to the lower Tskin in harbor seal “Luca” than in the other harborseals after diving. The entire blubber of this animal, including thevibrissal pads, seemed to be of a softer, more flexible consistency thanin the other eight harbor seals at the facility. According to Käkelä andHyvärinen (1993, 1996) who found differences in blubber compositionin ringed seals not only between body regions but also between individ-uals from different habitats, “Luca's” blubber has potentially a differentfatty acid composition with different thermal properties than that ofthe other seals.

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The comparison of the different findings about temperature andtemperature constancy in the vibrissal pads of the two investigated spe-cies leads to the consideration of their natural habitats and foragingbehaviors. Phocid seals, except for the monk seals (Monachus sp.), aredistributed in the moderate to polar regions of the northern hemi-sphere. In coastal areas they feed mainly on benthic prey, such as flat-fish, but they undertake foraging trips of more than 100 km to theopen ocean as well, where they hunt for pelagic fish in depths downto several hundred meters (King, 1983). In both cases vision is oftenlimited: in coastal regions, such as the Wadden Sea, by murky water,and by light limitation at depth. Therefore harbor seals, as well asother phocids, are highly reliant on their vibrissal system for feedingand orientation. Our results show that harbor seal vibrissal follicles areconstantly heated up to a certain temperature by a “thermostat”,despite of heat loss. A constant temperature could be maintained eitherby changes of insulation or by regulating the heating intensity via theblood supply. Short term changes of insulation seem unlikely, particu-larly since pinnipeds lack arrector pili muscles (Ling, 1965, 1970;Scheffer, 1962) and therefore are unable to erect their hairs in order toincrease an insulating air layer. By contrast, short term changes ofblood supply seem likely, as the F–SCs are richly endowed with arterio-venous anastomoses (AVAs): Low ambient temperatures may provokean increase of circulation within the F–SCs while at high ambient tem-perature heating intensity, circulation, respectively, may be reduced.

Otariids however are distributed in all climates in both hemispheres,mostly at the western coasts of the continents with clear upwellingwaters (King, 1983). Cape fur seals are abundant in the moderateclimate of the south tip of South Africa up to the tropical climate ofNamibia and will seldom experience water temperatures close to thefreezing point, contrarily to harbor seals. They forage in the upwellingwaters of the Benguela current with minimal turbidity, mostly at day-time (Rand, 1959) and at low depth, 45–50 m on average (Gentry,1986; Rand, 1959). Thus hunting by vision is generally possible. Conse-quently their dependency on the vibrissal sense, at least in foraging, ispotentially lower than in phocid seals and maintaining a constant hightemperature in the F–SCs therefore might not be necessary. Besides,fur seals, like all otariids, spend much more time on shore than phocidseals (Erdsack et al., 2013; Gentry, 1998, 2009). In air heat loss ismuch lower than in water, and the dense fur on the vibrissal pads insu-lates more effectively than in water. Hence vibrissal pads can be heatedup to high temperatures, as our results showed, with less expense thanin water. Beside tactile sensing otariid vibrissae play an important rolein social interactions (Ahl, 1986; Miller, 1975), e. g. highly erectedvibrissae indicate aggression in fur seal bulls (Caudron, 1995; Miller,1975). For this purpose intensive heating of the vibrissal follicles is pre-sumably not essential, but the active motion of the vibrissae increasesheat production, like any muscle activity does, and therefore may actas heat source. Harbor seals are able to inhibit the development of ther-mal windows depending on the situation (Erdsack et al., 2012), thus itmay be conceivable that the fur seal is able to regulate heating of thevibrissal follicles situationally aswell, according to necessity, e. g. duringhaptic investigations of objects. Therefore further temperature mea-surements while the fur seal is performing a haptic task using its vibris-sae would be of great interest.

Though both species are adapted to the aquatic environment andfor both species the vibrissal system is important, there are differencesin lifestyle and foraging habits that are reflected in morphological andphysiological adaptations, such as the different types of insulation. Themorphological differences of the vibrissal systems may display such aspecific adaptation to lifestyle, involving different heating mechanismsfor the tactile sense. While harbor seals (large vibrissal follicles, largeupper CS, fat insulation) maintain their vibrissal follicles at a certaintemperature, despite high, varying energy expenses, fur seals (smallervibrissal follicles, smaller upper CS, fur insulation) appear to heat thevibrissal pads with a more constant power, relying on the insulatingpower of the dense fur that covers the vibrissal pads. These two

different heating mechanisms would be consistent with adaptations totwo different environments and feeding habits.

5. Conclusion

The temperature inside the vibrissal follicles of harbor sealswas con-stant, without influence of the ambient water temperature. In fur sealsthe temperature inside the vibrissal follicles could not yet bemeasured.In harbor seals, the skin temperature on the vibrissal pads was onlyweakly correlated to water temperature, and not correlated to air tem-perature while hauling out, while in the Cape fur seal vibrissal pad skintemperature was actually higher than in the harbor seals, but distinctlycorrelated to ambient temperature (water or air). Sources for these dif-ferences between the species could be (1) the different F-SC sizes; inphocids approximately two times that in otariids; (2) the differentsizes of the upper CS within the F-SCs, about 50% longer in phocidsthan in otariids; (3) the different types of thermal insulation of thevibrissal pads: fat in the harbor seals and dense fur in the fur seal. Wepresume that, due to the differences in foraging habits and degree of ad-aptation to aquatic living, the species have developed different heatingmechanisms to maintain functionality of the tactile sense. Large tem-perature differences between skin and surface of the vibrissal pads indi-cate insulating properties of the fur on the vibrissal pads not only in thefur seal but also in the harbor seals.

Acknowledgements

This study was funded by a grant from the VolkswagenStiftung toGD and the Landesgraduiertenförderung Mecklenburg-Vorpommernto NE. [SS]

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