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The Effects of Submergence on the Thermal Function of Pinniped Fur

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The Effects of Submergence on the Thermal Function of Pinniped Fur Notes MARINE MAMMAL SCIENCE, 33(2): 611–620 (April 2017) © 2016 Society for Marine Mammalogy DOI: 10.1111/mms.12372 The effects of submergence on the thermal function of pinniped fur NEHA SHARMA Department of Biology, Adelphi University, 1 South Avenue, Garden 1 City, New York 11530-0701, U.S.A. AND HEATHER E. M. LIWANAG, Department of Biology, Adelphi University, 1 South Avenue, Garden City, New York 11530-0701, U.S.A. and Department of Biological Sciences, California Polytechnic State University, 1 Grand Ave- nue, San Luis Obispo, California, 93407-0401, U.S.A. As endothermic homeotherms, mammals derive their body temperature from internal metabolism and achieve balance by regulating core temperature around a set point that is independent from the environment (Scholander et al. 1950). Ther- moregulation is especially challenging for endotherms in marine environments, because heat loss in water occurs 25 times faster than in air at the same temperature (Dejours et al. 1987). As a result, most marine mammals have evolved physiological and morphological mechanisms for reducing heat loss to the environment (Pabst et al. 1999). Across marine mammal lineages, species have developed specialized insulation in the form of modified fur and/or blubber (Scholander et al. 1950, Pabst et al. 1999, Liwanag et al. 2012a, b). The most recent lineages to reinvade the marine environment, sea otters and polar bears, still rely on fur for their primary insulation (Pabst et al. 1999, Berta et al. 2006). The more derived lineages, cetaceans and sireni- ans, have secondarily lost the characteristic mammalian fur and instead rely on blub- ber as their primary insulator (Hart and Fisher 1964, Ling 1970, Berta et al. 2006). Pinnipedia is the only extant marine mammal lineage that has retained both forms of insulation. Among the pinnipeds, phocids (true seals) and odobenids (walrus) rely on blubber for their thermal insulation. Otariids (eared seals), however, retain body heat through two distinct mechanisms: fur seals have dense, waterproof fur along with a moderate blubber layer, whereas sea lions have nonwaterproof fur and primarily rely on their thicker blubber to keep warm (Liwanag et al.2012a, b). Pinnipeds are unique among marine mammals because they forage and migrate in the water but breed and rest on land. Heat loss on land can take place through con- duction, convection, radiation, and evaporation, whereas in an aquatic medium the more likely avenues of heat loss are conduction and convection (Perrin et al. 2009). 1Corresponding author (e-mail: [email protected]). 611 612 MARINE MAMMAL SCIENCE, VOL. 33, NO. 2, 2017 The amphibious lifestyle of pinnipeds could result in trade-offs with regard to how well their insulation performs in each medium. The insulating properties of fur are dependent on its ability to sustain a layer of air trapped between the hairs (Kvad- sheim and Aarseth 2002). There are two primary types of hairs that characterize mammalian fur: short, fine underhairs, which act to trap air against the animal’s skin, and longer, coarse guard hairs, which cover and protect the underhairs (Ling 1970). Fur has been described as the superior insulator over blubber, as long as the air layer is maintained (Kvadsheim and Aarseth 2002, Liwanag et al.2012b). When the ani- mal is submerged, however, the air layer can become compromised and the fur may no longer serve as effective insulation. Because blubber is a subcutaneous tissue, its effectiveness as insulation is not compromised by submergence (Schmidt-Nielsen 1997, Liwanag et al. 2012b). Change in fur function during submergence is likely variable among pinniped groups; fur seals have the densest fur and can maintain a layer of air between the underhairs while submerged, whereas sea lion and phocid pelts become saturated with water upon submergence (Liwanag et al. 2012a). Though several previous stud- ies have measured the thermal properties of marine mammal integument and/or blubber (Kvadsheim and Aarseth 2002; Dunkin et al. 2005; Bagge et al. 2012; Liwa- nag et al. 2012b;Pearsonet al.2014a, b;Horganet al. 2014), very few have directly measured the effects of submergence on those properties, particularly across groups (Scholander et al. 1950, Frisch et al. 1974, Kvadsheim and Aarseth 2002). The objec- tive of this study was to quantify the extent to which submergence in water reduces the effectiveness of pinniped fur as an insulator. This was achieved by comparing the thermal conductivity (k;WÁm–1Á°C–1) and thermal resistance (R;m2Á°CÁW–1)ofpin- niped pelts in air and in water. We hypothesized that fur seal pelts would undergo a minimal loss of thermal function in water compared to those of sea lions and phocids, based on differences in fur density and ability to maintain a layer of air within the fur. Sculp (fur, skin, and blubber) samples were collected postmortem, from the dor- sum of five fur seal species (n = 17), one sea lion species (n = 20), and three phocid species (n = 9; Table S1). Fresh tissue samples were collected only from good condi- tion carcasses, as determined by tissue color. Because samples were acquired oppor- tunistically from stranded or harvested animals, age classes were variable and included pups, yearlings, subadults, and adults. Young mammals typically exhibit similar fur characteristics to adult conspecifics (Meyer et al. 2002), and this is particu- larly true for pinnipeds that have shed the initial lanugo coat (Pearson et al. 2014a, Gmuca et al. 2015); thus, pup pelts were only included if they did not have lanugo. Samples included in this study did not show any signs of molt. All samples were stored in plastic food wrap and heavy-duty freezer bags to prevent desiccation, and kept frozen (–20°C) until use. Samples were cut into squares (approximately 10 9 10 cm), rinsed under cold, distilled water, and then dried using a hairdryer on the cool setting to restore the naturally existing air layer between the hairs (Williams et al. 1988, Kvadsheim and Aarseth 2002, Liwanag et al. 2012a). Conductivity measure- ments in air were made on these samples in a previous study, with pelt and blubber conductivity determined simultaneously but distinctly for each layer (Liwanag et al. 2012a, b). For the present study, the blubber layer was carefully cut away from each sample, leaving the pelt (fur and skin). Skin, dry fur (before trial), and wet fur (after trial) thicknesses were measured to the nearest 0.001 mm using digital calipers (Absolute Digimatic caliper 500 series, Mitutoyo, Aurora, IL) three times on each side, and the mean values were used for calculations. NOTES 613 Thermal conductivity (k) was measured in a heat flux chamber (162 quart Igloo Marine ice chest, Igloo Commercial) using the standard material method (Kvadsheim et al. 1994; Kvadsheim and Aarseth 2002; Dunkin et al. 2005; Liwanag et al. 2012a, b). The chamber consisted of an insulated lower compartment heated to 37°C with a circulating water bath (Lauda RM20, Brinkmann Instruments or Isotemp 6200, Fisher Scientific) and a chilled upper compartment filled with ice packs (Liwa- nag et al. 2012a, b;Pearsonet al.2014b). The entire setup was surrounded by foam insulation to maintain a stable thermal gradient and to ensure unidirectional heat flow. An elastomer (Plastisol vinyl, Carolina Biological Supply, Burlington, NC) was used as the standard material (k = 0.119 Æ 0.017 WÁm–1Á°C–1). The standard mate- rial was placed directly against the heat source. On top of the standard material, the pelt sample was placed skin-side down with the edges carefully adjusted into a cup-like formation to prevent water from leaking below the sample. Cold water (5.88°C Æ 3.49°C, approximately 1 cm height) was evenly poured on top of the fur to simulate submergence. Three copper-constantin (Type T) thermocouples (Physitemp Instruments, Inc., Clifton, NJ) were placed between each layer: between the heat source and standard material, between the standard material and pelt, and on top of the pelt. Each thermocouple was connected to a Fluke Hydra data logger (Model 2625A, Fluke Inc., Everett, WA), which recorded outputs every 6 s onto a desktop computer. Trials were conducted for a minimum of 2 h to ensure a steady thermal gradient, such that the water reached a slightly warmer, but steady, tem- perature. Data collected during the final 30 min of each trial were used for analysis. Thermal conductivity was calculated across the pelt using the Fourier equa- tion (Kreith 1958): H ¼ k Á A Á DT Á LÀ1 ð1Þ where H is heat transfer (J/s), k is thermal conductivity (WÁm–1Á°C–1), A is the area (m2) through which the heat is moving, DT is the temperature differential (°C) across the material, and L is the thickness of the material (m). Assuming equal rates of heat transfer across the standard material and pelt sample, the equations for both materials can be set equal and solved for thermal conductivity of the pelt sample. Note that thermal conductivity is a material property, and describes the quality of the insula- tion independent of thickness (Kvadsheim et al. 1994). To take thickness of the insu- lation into account, thermal resistance (R;m2Á°CÁW–1) was calculated as: R ¼ L=k ð2Þ To determine thickness (L) during submergence, the height of the wet pelt was measured with digital calipers upon completion of each conductivity trial. Within-group comparisons between measurements in air and in water were ana- lyzed using paired t-tests, and comparisons among groups (fur seal, sea lion, phocid) were analyzed using 1-way ANOVA followed by the Tukey honestly significant dif- ference test (JMP Pro 11.2.1, SAS, Cary, NC). Upon analysis, we observed that the northern elephant seals (subfamily Monachinae) showed a different pattern from the other phocid species (subfamily Phocinae); therefore, we also conducted 1-way ANOVA to compare subgroups (fur seal, sea lion, phocine, monachine).
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