Effects of ontogeny and oiling on the thermal function of southern sea otter (Enhydra lutris nereis) fur.

During the evolution of most marine mammals, fur as an insulator has been replaced with more buoyant, energy storing and streamlining blubber. By contrast, the sea otter (Enhydra lutris) relies on insulation from its dense, air-trapping pelage, which differs morphologically between natal and adult stages. In this study, we investigated the ontogenetic changes in thermal function of southern sea otter (Enhydra lutris nereis) pelts in air, in water, and when saturated with crude oil. Pelt thermal conductivity, thickness, and thermal resistance were measured for six age classes: neonate (<1 month), small pup (1-2 months), large pup (3-5 months), juvenile (6 months-1 year), subadult (1-3 years), and adult (4-9 years). Thermal conductivity was significantly higher for pelts in air than in water, with oiled pelts exhibiting the highest values (P < 0.001). Oiled pelts had the lowest thermal resistance, which suggests that regardless of age, all sea otters are vulnerable to the effects of oiling (P < 0.001). To scale up our laboratory findings, we used a volume-specific geometric model of conductive heat transfer for a simplified sea otter body, representing all tested age classes and treatments. Neonates, small pups, and large pups are more vulnerable to the effects of oiling compared with older age classes (P < 0.0001) due to a higher surface area-to-volume ratio. These results are consistent with the known thermal conductance values for adult sea otter pelts, yet this is the first time such thermal differences have been demonstrated in young otters. Overall, body size and age play a more important role in the thermal abilities of sea otters than previously thought.

Rapid Physiological Plasticity in Response to Cold Acclimation for Nonnative Italian Wall Lizards (Podarcis siculus) from New York.

AbstractThermal physiology helps us understand how ectotherms respond to novel environments and how they persist when introduced to new locations. Researchers generally measure thermal physiology traits immediately after animal collection or after a short acclimation period. Because many of these traits are plastic, the conclusions drawn from such research can vary depending on the duration of the acclimation period. In this study, we measured the rate of change and extent to which cold tolerance (critical thermal minimum [CTmin]) of nonnative Italian wall lizards (Podarcis siculus) from Hempstead, New York, changed during a cold acclimation treatment. We also examined how cold acclimation affected heat tolerance (critical thermal maximum [CTmax]), thermal preference (Tpref), evaporative water loss (EWL), resting metabolic rate (RMR), and respiratory exchange ratio (RER). We predicted that CTmin, CTmax, and Tpref would decrease with cold acclimation but that EWL and RMR would increase with cold acclimation. We found that CTmin decreased within 2 wk and that it remained low during the cold acclimation treatment; we suspect that this cold tolerance plasticity reduces risk of exposure to lethal temperatures during winter for lizards that have not yet found suitable refugia. CTmax and Tpref also decreased after cold acclimation, while EWL, RMR, and RER increased after cold acclimation, suggesting trade-offs with cold acclimation in the form of decreased heat tolerance and increased energy demands. Taken together, our findings suggest that cold tolerance plasticity aids the persistence of an established population of invasive lizards. More generally, our findings highlight the importance of accounting for the plasticity of physiological traits when investigating how invasive species respond to novel environments.

Ontogenetic changes in southern sea otter (Enhydra lutris nereis) fur morphology.

Many animals exhibit morphological changes across ontogeny associated with adaptations to their environment. Sea otters (Enhydra lutris) have the densest fur of any animal, which is composed of guard hairs, intermediate hairs, and underhairs. Sea otters live in cold water environments, and their fur traps a layer of air to remain properly insulated, due to morphological adaptations that allow the hairs to trap air when submerged. When a sea otter is born, it has a natal pelage which it will eventually molt and replace with a pelt resembling the adult pelage. Past studies have investigated the morphology and hair density of adult sea otter fur, but these characteristics have not been measured for other age classes, including for the natal pelage. This study quantified ontogenetic changes in hair morphology of southern sea otter (E. lutris nereis) pelts. We measured guard hair length and circularity, shape of cuticular scales on guard hairs and underhairs, and overall hair density for sea otter pelts across six age classes: neonate (<1 month), small pup (1-2 months), large pup (3-5 months), juvenile (6 months-1 year), subadult (1-3 years), and adult (4-9 years). Neonate and small pup pelts had significantly longer guard hairs than older age classes. Natal pelage guard hairs were similarly shaped but smaller in diameter than adult guard hairs. Hairs of the natal pelage had similar cuticular scale patterns as adult hairs, indicating the importance of this structure for the function of the fur. Natal pelage had a lower hair density than the pelage of older age classes, with the adult pelage exhibiting the highest hair density. Overall, the morphological differences between natal and adult pelage in sea otters suggest functional differences that may make sea otter pups more vulnerable to heat loss.

Osmotic and metabolic responses to cold acclimation and acute cold challenge in a freeze avoidant lizard, Podarcis siculus.

Ectotherms survive exposure to subzero temperatures through freeze tolerance or freeze avoidance. Among vertebrate ectotherms, glucose is commonly used as a cryoprotectant in freeze tolerant strategies and as an osmolyte in freeze avoidant strategies, while also functioning as a metabolic substrate. Whereas some lizard species are capable of both freeze tolerance and freeze avoidance, Podarcis siculus is limited to freeze avoidance through supercooling. We hypothesized that, even in a freeze-avoidant species such as P. siculus, plasma glucose would accumulate with cold acclimation and would increase in response to acute exposure to subzero temperatures. To investigate this, we tested whether plasma glucose concentration and osmolality would increase in response to a subzero cold challenge before and after cold acclimation. In addition, we examined the relationship between metabolic rate, cold acclimation, and glucose by measuring metabolic rate during the cold challenge trials. We found that plasma glucose increased during the cold challenge trials, and that the increase was more pronounced after cold acclimation. However, baseline plasma glucose decreased throughout cold acclimation. Interestingly, total plasma osmolality did not change, and the increase in glucose only slightly altered freezing point depression. Metabolic rate during the cold challenge decreased after cold acclimation, and changes in respiratory exchange ratio suggest an increased relative use of carbohydrates. Overall, our findings demonstrate an important role for glucose in the response of P. siculus to an acute cold challenge, thus adding evidence for glucose as an important molecule for overwintering ectotherms that use freeze avoidant strategies.

Some like it hotter: Differential thermal preferences among lizard color morphs.

Temperature rules the lives of ectotherms. To perform basic biological functions, ectotherms must make behavioral adjustments to keep their body temperatures near a preferred temperature (Tpref). Many color polymorphic lizards are active thermoregulators and exhibit morph differences in traits related to thermoregulation, such as color, body size, and microhabitat use. The Aegean wall lizard, Podarcis erhardii, is a heliothermic lizard with orange, white, and yellow color morphs that differ in size, behavior, and microhabitat use. Here, we tested whether P. erhardii color morphs from the same population from Naxos island, Greece, differ in Tpref. We hypothesized that orange morphs would prefer lower temperatures than white and yellow morphs because orange morphs are often found on cooler substrates and in microhabitats with more vegetation cover. We obtained Tpref for 95 individuals using laboratory thermal gradient experiments of wild-caught lizards and found that orange morphs do, indeed, prefer cooler temperatures. Average orange morph Tpref was 2.85 °C lower than average white and yellow morph Tpref. Our results add support to the idea that P. erhardii color morphs have multivariate alternative phenotypes and present the possibility that thermally heterogeneous environments play a role in the maintenance of color polymorphism in this species.

Using a combination of midazolam and butorphanol is a safe and effective reversible field sedation protocol for Weddell seal (Leptonychotes weddellii) pups.

BACKGROUND: Weddell seals (Leptonychotes weddellii) are a well-studied species of phocid with an apparent sensitivity to immobilising agents. Mortality as high as 31% has been reported during field immobilisation. This study investigated the use of a benzodiazepine in combination with an opioid agonist/antagonist for sedation in Weddell seal pups as part of a physiological study. METHODS: During the 2017 and 2019 Antarctic pupping seasons, 18 Weddell seal pups were sedated by intramuscular administration of a combination of midazolam and butorphanol or intravenous midazolam alone. Individuals were sedated at 1, 3, 5 and 7 weeks of age. Naltrexone and flumazenil were used to reverse sedation. The combination was 100% effective in providing appropriate sedation for the intended procedures. RESULTS: Analyses were performed to investigate relationships between dose administered, age, individual reactions, adverse effects and changes in dive physiology. Transient apnoea (10-60 seconds) was the most frequently observed adverse effect. No sedation-associated morbidity or mortality occurred. LIMITATIONS: The sample size is small and there is no pharmacokinetic information for either sedative or reversal in phocid species. CONCLUSIONS: The combination of midazolam (0.2-0.3 mg/kg) and butorphanol (0.1-0.2 mg/kg) provided safe and effective sedation, with reversible effects, in Weddell seal pups.

Metabolic cost of thermoregulation decreases after the molt in developing Weddell seal pups.

Allocation of energy to thermoregulation greatly contributes to the metabolic cost of endothermy, especially in extreme ambient conditions. Weddell seal (Leptonychotes weddellii) pups born in Antarctica must survive both on ice and in water, two environments with very different thermal conductivities. This disparity likely requires pups to allocate additional energy toward thermoregulation rather than growth or development of swimming capabilities required for independent foraging. We measured longitudinal changes in resting metabolic rate (RMR) for Weddell seal pups (n=8) in air and water from one to seven weeks of age, using open-flow respirometry. Concurrently, we collected molt, morphometric and dive behavior data. Absolute metabolic rate (MR) in air followed the expected allometric relationship with mass. Absolute MR in water was not allometric with mass, despite a 3-fold increase in mass between one and seven weeks of age. Developmental stage (or molting stage), rather than calendar age, determined when pups were thermally capable of being in the water. We consistently observed post-molt pups had lower RMR in air and water (6.67±1.4 and 7.90±2.38 ml O2 min-1 kg-1, respectively) than pre-molt (air: 9.37±2.42 ml O2 min-1 kg-1, water: 13.40±3.46 ml O2 min-1 kg-1) and molting pups (air: 8.45±2.05 ml O2 min-1 kg-1, water: 10.4±1.63 ml O2 min-1 kg-1). RMR in air and water were equivalent only for post-molt pups. Despite the increased energy cost, molting pups spent three times longer in the water than other pups. These results support the idea of an energetic trade-off during early development; pups expend more energy for thermoregulation in water, yet gain experience needed for independence.

From ice to ocean: changes in the thermal function of harp seal pelt with ontogeny.

Many animals exhibit ontogenetic changes associated with adaptations for survival. Harp seals (Pagophilus groenlandicus) live in the Arctic and rely on thick insulation to maintain thermal homeostasis. Adult harp seals primarily use blubber for insulation, but newborn harp seals rely on a lanugo pelt while nursing, as their blubber layer develops and their first-year pelage grows. This study compared ontogenetic changes in the thermal properties of harp seal pelts in water and in air. Thermal conductivity, pelt thickness, and thermal resistance were measured in water for pelts of harp seal neonates (1 day old), thin whitecoats (4 day old), fat whitecoats (9 day old), ragged jackets (2 week old), beaters (3 week old), and adults and compared to previously published measurements made on the same pelts in air. Pelt conductivity was significantly higher in water than air for pre-molt and molting pups (P ≤ 0.031). Unlike adult pelage, which flattened underwater, lanugo hairs lifted underwater, a phenomenon that has not been reported previously. Thermal resistance of the pelt was significantly reduced in water compared to air for neonates and thin whitecoats (P ≤ 0.0001). A mathematical model of conductive heat transfer for an ellipsoid body showed volume-specific heat loss in water decreased and then stabilized as harp seals aged (P = 0.0321) and was significantly higher for neonates, thin whitecoats, and ragged jackets in water than in air (P ≤ 0.0089). Overall, pelt function is reduced in water for harp seal pups with lanugo, and this renders neonates and thin whitecoats particularly vulnerable to heat loss if submerged.

Thermal tolerance varies with age and sex for the nonnative Italian Wall Lizard (Podarcis siculus) in Southern California.

Temperature has a substantial effect on both the physiology and behavior of ectothermic animals such as lizards. Physiology and behavior can also be influenced by ontogenetic and sex differences, but these effects are largely understudied in lizards. We examined ontogenetic and sex-based differences in thermal tolerances, preferred temperature, and temperature-dependent evaporative water loss rates in Italian Wall Lizards, Podarcis siculus, collected from an introduced population near Los Angeles, California, USA that were acclimated to laboratory conditions. Podarcis siculus has been introduced to multiple localities in the USA and the Mediterranean region and has demonstrated remarkable ability to adapt to novel climatic conditions. In the California population, adults of both sexes had a higher critical thermal maximum (CTmax) than juveniles, and adult females had a lower critical thermal minimum (CTmin) than juveniles and adult males. Thus, adult females had a significantly wider thermal breadth (CTmax - CTmin) compared to adult males and juveniles. Mass-specific evaporative water loss was higher in juveniles compared to adult males at intermediate temperatures. There was no significant difference among groups for preferred temperature. This implies that thermal tolerance, a physiological characteristic, varies with age and sex for this population, whereas thermal preference, a behavioral characteristic, does not. Interestingly, CTmin for all age and sex classes was above temperatures likely experienced by some nonnative populations in winter, suggesting individuals need to find urban thermal retreats. These results add to the growing literature demonstrating that thermal tolerances and breadths can vary between sexes and across age classes in squamate species.

The fat and the furriest: morphological changes in harp seal fur with ontogeny.

Ontogenetic changes in physiological performance often exemplify the development of adaptations to environmental challenges. For mammals in polar regions, the extreme cold of the environment presents a constant challenge to thermal homeostasis. The harp seal (Pagophilus groenlandicus) is an Arctic species that shifts its thermoregulatory strategy with ontogeny. Adult harp seals primarily use blubber for insulation, but newborn harp seals instead rely on their fur coat while their blubber layer develops. Harp seal pups are weaned abruptly, less than 2 wk after birth, and must subsequently learn to swim and dive in frigid waters on their own. This study examined how the morphological characteristics of harp seal fur change with ontogeny. We compared hair length, hair circularity, and hair density for neonates (1 d old; n = 7), early-nursing pups (4 d old; n = 3), late-nursing pups (9 d old; n = 4), newly weaned (molting) pups (2 wk old; n = 5), late-weaned (molted) pups (3 wk old; n = 4), and adult harp seals (n = 4). Hairs were shorter (P < 0.001) and flatter (P < 0.001) in older animals. Additionally, hair density decreased with age (P < 0.001), in terms of both the average number of hair bundles per unit area and the average number of underhairs present in any given bundle. These morphological changes were associated with a reduced thermal resistance of the pelt in late-weaned (molted) pups and adults (P < 0.001). Results are consistent with known evolutionary patterns of fur morphology associated with the transition from fur to blubber in aquatic species, yet this is the first time such morphological differences have been demonstrated across age classes within a single species. Thus, the ontogenetic patterns described here for harp seals recapitulate the convergent phylogenetic patterns observed across secondarily aquatic species. Overall, the timing of these ontogenetic changes may limit the ability of harp seals to adapt to the deterioration of sea ice in the Arctic, as predicted with continued climate change.

Shifts in thermoregulatory strategy during ontogeny in harp seals (Pagophilus groenlandicus).

Heat balance can be difficult for young and/or small animals in polar regions because environmental conditions in combination with small body size or physiological immaturity can increase heat loss. We investigated how thermoregulatory patterns change with ontogeny in 5 age classes of harp seal (Pagophilus groenlandicus) from birth to post-molt to further understand the timing of thermoregulatory development in relation to their potential vulnerability to ongoing fluctuations in the extent and stability of Arctic pack ice. We measured changes in the amount, conductivity, and resistance of the seal pups׳ insulative layers (blubber and fur), the potential for endogenous heat-generation by shivering (muscle enzyme activity), and nonshivering thermogenesis (NST; brown adipose tissue (BAT) uncoupling protein 1 (UCP1) expression and mitochondrial density). There was no significant difference in blubber conductivity among age classes, though the amount of blubber insulation significantly increased from birth to weaning. Pelage conductivity was low (0.12±0.01Wm(-1)°C(-1)) except in 9-day old pups (0.40±0.08Wm(-1)°C(-1)); the significantly higher conductivity may signal the beginning of the molt, and this age group may be the most vulnerable to early water entry. Citrate synthase activity significantly increased (49.68±3.26 to 75.08±3.52µmolmin(-1)gwetweight(-1)) in the muscle; however it is unlikely that increasing a single enzyme greatly impacts heat generation. BAT of younger pups contained UCP1, though expression and mitochondrial density quickly declined, and the ability of pups to produce heat via NST was lost by weaning. While total thermal resistance did not differ, neonatal and early nursing animals gained the majority of their thermal resistance from lanugo (82.5±0.03%); however, lanugo is not insulative when wet, and NST may be important to maintain euthermia and dry the coat if early immersion in water occurs. By late nursing, blubber seems sufficient as insulation (75.87±0.01% of resistance after 4 weeks), but high conductivity of fur may be responsible for retention of UCP1 expression. Weaned animals rely on blubber insulation, and no longer need NST, as wetted fur is no longer a threat to euthermia.

To each its own: Thermoregulatory strategy varies among neonatal polar phocids.

Cold environmental conditions and small body size promote heat loss and may create thermoregulatory challenges for marine mammals born in polar regions. However, among polar-born phocid seal species there are variations in physical attributes and environmental conditions at birth, allowing for an interesting contrast in thermoregulatory strategy. We compared thermoregulatory strategies through morphometrics, sculp attributes (conductivity and resistance), nonshivering thermogenesis (NST via uncoupling protein 1; UCP1), and muscle thermogenesis (via enzyme activity) in neonatal harp (Pagophilus groenlandicus), hooded (Cystophora cristata), and Weddell seals (Leptonychotes weddellii). Harp seals are the smallest at birth (9.8±0.7 kg), rely on lanugo (82.49±3.70% of thermal resistance), and are capable of NST through expression of UCP1 in brown adipose tissue (BAT). In contrast, hooded seal neonates (26.8±1.3 kg) have 2.06±0.23 cm of blubber, accounting for 38.19±6.07% of their thermal resistance. They are not capable of NST, as UCP1 is not expressed. The large Weddell seal neonates (31.5±4.9 kg) rely on lanugo (89.85±1.25% of thermal resistance) like harp seals, but no evidence of BAT was found. Muscle enzyme activity was highest in Weddell seal neonates, suggesting that they rely primarily on muscle thermogenesis. Similar total thermal resistance, combined with marked differences in thermogenic capacity of NST and ST among species, strongly supports that thermoregulatory strategy in neonatal phocids is more closely tied to pups' surface area to volume ratio (SA:V) and potential for early water immersion rather than mass and ambient environmental conditions.

Direct fitness correlates and thermal consequences of facultative aggregation in a desert lizard.

Social aggregation is a common behavioral phenomenon thought to evolve through adaptive benefits to group living. Comparing fitness differences between aggregated and solitary individuals in nature--necessary to infer an evolutionary benefit to living in groups--has proven difficult because communally-living species tend to be obligately social and behaviorally complex. However, these differences and the mechanisms driving them are critical to understanding how solitary individuals transition to group living, as well as how and why nascent social systems change over time. Here we demonstrate that facultative aggregation in a reptile (the Desert Night Lizard, Xantusia vigilis) confers direct reproductive success and survival advantages and that thermal benefits of winter huddling disproportionately benefit small juveniles, which can favor delayed dispersal of offspring and the formation of kin groups. Using climate projection models, however, we estimate that future aggregation in night lizards could decline more than 50% due to warmer temperatures. Our results support the theory that transitions to group living arise from direct benefits to social individuals and offer a clear mechanism for the origin of kin groups through juvenile philopatry. The temperature dependence of aggregation in this and other taxa suggests that environmental variation may be a powerful but underappreciated force in the rapid transition between social and solitary behavior.

Energetic costs and thermoregulation in northern fur seal (Callorhinus ursinus) pups: the importance of behavioral strategies for thermal balance in furred marine mammals.

Behavioral thermoregulation represents an important strategy for reducing energetic costs in thermally challenging environments, particularly among terrestrial vertebrates. Because of the cryptic lifestyle of aquatic species, the energetic benefits of such behaviors in marine endotherms have been much more difficult to demonstrate. In this study, I examined the importance of behavioral thermoregulation in the northern fur seal (Callorhinus ursinus) pup, a small-bodied endotherm that spends prolonged periods at sea. The thermal neutral zones of three weaned male northern fur seal pups (body mass range = 11.8-12.8 kg) were determined by measuring resting metabolic rate using open-flow respirometry at water temperatures ranging from 2.5° to 25.0°C. Metabolic rate averaged 10.03 ± 2.26 mL O2kg⁻¹ min⁻¹ for pups resting within their thermal neutral zone; lower critical temperature was 8.3° ± 2.5°C , approximately 8°C higher than the coldest sea surface temperatures encountered in northern Pacific waters. To determine whether behavioral strategies could mitigate this potential thermal limitation, I measured metabolic rate during grooming activities and the unique jughandling behavior of fur seals. Both sedentary grooming and active grooming resulted in significant increases in metabolic rate relative to rest (P = 0.001), and percent time spent grooming increased significantly at colder water temperatures (P < 0.001). Jughandling metabolic rate (12.71 ± 2.73 mL O2kg⁻¹ min ⁻¹) was significantly greater than resting rates at water temperatures within the thermal neutral zone (P < 0.05) but less than resting metabolism at colder water temperatures. These data indicate that behavioral strategies may help to mitigate thermal challenges faced by northern fur seal pups while resting at sea.