Spatial and cumulative organochlorine and mercury exposure assessments in Steller Sea lions of Alaska: Emphasizing pups.

Steller sea lions (SSL) are sentinels for monitoring environmental contaminants in remote areas of the Aleutian Islands, Alaska. Therefore, concentrations of several organochlorines (OCs) were measured in blood from 123 SSL pups sampled from 3 regions; the western Aleutian Islands (WAI), central Aleutian Islands (CAI), and the central Gulf of Alaska. Blood, blubber, and milk from 12 adult female SSL from WAI, CAI and southeast Alaska also were analyzed. Findings included the following. SSL pups had higher concentrations of some OCs and mercury (Hg) on rookeries in the WAI than those more easterly. Pups had significantly higher blood concentrations of many OC classes than adult females sampled within the same region; some pups had PCB concentrations exceeding thresholds of concern (∑PCBs >8600 ng/g lw). ∑PCB concentration in pup whole blood was positively correlated with the trophic marker, δ15N within the regions sampled, along with two PCB congeners (PCB138 and PCB153). This suggests that the dams of pups with higher ∑PCBs, PCB138, and PCB153 concentrations were feeding on more predatory prey. Adult female blubber ∑DDT and hexachlorocyclohexane concentrations were also positively correlated with δ15N values. Several pups (mostly from WAI) had blood Hg concentrations and/or blood PCB concentrations (surrogate for overall OC exposures) of concern. The finding that WAI SSL pups have been exposed to multiple contaminants calls for future investigation of their cumulative exposure to a mixture of contaminants especially their transplacental and then transmammary exposure routes.

Regional variations and drivers of mercury and selenium concentrations in Steller sea lions.

Mercury (Hg) can be neurotoxic to mammals and impact reproduction, whereas selenium (Se) is an important antioxidant known to ameliorate some adverse effects of Hg. Total Hg concentrations ([THg]) were measured in lanugo (pelage grown in utero) of 812 Steller sea lion (Eumetopias jubatus) pups across Alaska and Russia to assess fetal exposure during late gestation. The molar ratio of total Se to THg (TSe:THg) was determined in whole blood collected from 291 pups. Stable isotope ratios of carbon and nitrogen were measured in sections of vibrissae (whiskers, n = 498) and in lanugo (n = 480) of pups grown during late gestation to track diet variations among adult females that can drive Hg and Se exposure during this critical fetal development period. Lanugo [THg] ranged from 1.4 to 73.7 µg/g dry weight with the lowest median [THg] in Southeast Alaska. Pups from the Western Aleutian Islands had higher median lanugo [THg] than pups from other metapopulations in Alaska. Over 25% of pups in the Western Aleutian Islands had [THg] above published risk thresholds (20 µg/g) for other mammals. Whole blood molar TSe:THg was significantly lower in the Western Aleutian Islands and in some parts of the Central Aleutian Islands with higher molar ratios found in the Eastern Aleutian Islands and Central Gulf of Alaska. This suggests a limitation on potential protective functions of Se in the western regions with the highest relative [THg]. The Central Aleutian Island pups with [THg] over 20 µg/g had higher δ15N ratios than pups with lower [THg] suggesting dams consuming higher trophic level prey is a key driver for Hg exposure. However, regional differences likely reflect variability in diet of the dam during gestation and in Hg food web dynamics between oceanic regimes east and west of key passes in the Aleutian Islands.

Viral emergence in marine mammals in the North Pacific may be linked to Arctic sea ice reduction.

Climate change-driven alterations in Arctic environments can influence habitat availability, species distributions and interactions, and the breeding, foraging, and health of marine mammals. Phocine distemper virus (PDV), which has caused extensive mortality in Atlantic seals, was confirmed in sea otters in the North Pacific Ocean in 2004, raising the question of whether reductions in sea ice could increase contact between Arctic and sub-Arctic marine mammals and lead to viral transmission across the Arctic Ocean. Using data on PDV exposure and infection and animal movement in sympatric seal, sea lion, and sea otter species sampled in the North Pacific Ocean from 2001-2016, we investigated the timing of PDV introduction, risk factors associated with PDV emergence, and patterns of transmission following introduction. We identified widespread exposure to and infection with PDV across the North Pacific Ocean beginning in 2003 with a second peak of PDV exposure and infection in 2009; viral transmission across sympatric marine mammal species; and association of PDV exposure and infection with reductions in Arctic sea ice extent. Peaks of PDV exposure and infection following 2003 may reflect additional viral introductions among the diverse marine mammals in the North Pacific Ocean linked to change in Arctic sea ice extent.

Temporal records of diet diversity dynamics in individual adult female Steller sea lion (Eumetopias jubatus) vibrissae.

Detailed information on the nutrition of free-ranging mammals contributes to the understanding of life history requirements, yet is often quite limited temporally for most species. Reliable dietary inferences can be made by analyzing the stable carbon (C) and nitrogen (N) isotopic values (δ13C and δ15N) of some consumer tissues; exactly which tissue is utilized dictates the inferential scope. Steller sea lion (SSL) vibrissae are grown continuously without shedding and thus provide a continuous multi-year record of dietary consumption. We applied a novel kernel density approach to compare the δ13C and δ15N values along the length of SSL vibrissae with δ13C and δ15N distributions of potential prey species. This resulted in time-series of proportion estimates of dietary consumption for individual SSL. Substantial overlap in δ13C and δ15N distributions for prey species prevented a discrete species-scale assessment of SSL diets; however, a post hoc correlational analysis of diet proportion estimates revealed grouping by trophic level. Our findings suggest that adult female SSL diets in the western and central Aleutian Islands shift significantly according to season: diets contain a higher proportion of lower trophic level species (Pacific Ocean perch, northern rockfish, Atka mackerel and walleye pollock) in the summer, whereas in the winter SSL consume a much more diverse diet which includes a greater proportion of higher trophic level species (arrowtooth flounder, Kamchatka flounder, darkfin sculpin, Pacific cod, Pacific octopus, rock sole, snailfish, and yellow Irish lord).

Health status of young Alaska Steller sea lion pups (Eumetopias jubatus) as indicated by blood chemistry and hematology.

Blood chemistry and hematology were examined in 238 Steller sea lion pups (Eumetopias jubatus) to assess the health status of pups <1 month of age. Failure of juvenile recruitment (possibly due to nutritionally or physiologically compromised pups) into breeding populations has been proposed as a cause of recent declines of this endangered species in Alaska. To identify potential correlations with areas of high population decline, blood chemistry data were considered for three areas: eastern Aleutian Islands (low rates of population decline to stable populations), Gulf of Alaska (high rates of decline), and Southeast Alaska (stable to increasing population). Southeast Alaska pups showed elevated ketone body concentrations (beta-hydroxybutyrate,(beta-HBA)) and depressed glucose levels than pups in the Gulf of Alaska. Over 40% of the pups from Southeast Alaska had elevated beta-HBA concentrations suggesting they underwent longer periods of fasting than seen in pups from other areas. Hematocrit (Hct), hemoglobin concentration (Hb) and water content of the blood exhibited typical mammalian relationships. In summary, blood chemistry and hematology data showed no indication that Steller sea lion pups <1 month old from areas of population decline were nutritionally compromised.

Plasma haptoglobin levels in threatened Alaskan pinniped populations.

We evaluated the plasma concentration of the acute phase protein haptoglobin (Hp) from Steller sea lions (Eumetopias jubatus) and harbor seals (Phoca vitulina) in regions of Alaska (USA) where the populations of these pinnipeds were declining and compared the values with concentrations of Hp from the same species in areas where the populations were stable. Samples were collected from 1992 through 1994 at sites in Southeast Alaska, Prince William Sound, the Gulf of Alaska, and the Aleutian Islands. Significantly higher levels of Hp were found in the samples from the areas of decline compared to those from stable populations. Based on these findings, we propose that one may be able to distinguish these compromised pinniped populations using Hp as a biomedical indicator.

Developmental changes in cardiorespiratory patterns of sleep-associated apnea in northern elephant seals.

The development of heart rate and respiratory patterns related to sleep-associated apnea were studied in northern elephant seal (Mirounga angustirostris) pups and adult males. Heart rate patterns became more refined in conjunction with an age-related increase in apnea duration in pups. That is, older pups showed significant sinus arrhythmia, while breathing and apneic heart rate were both stable and similar in magnitude to the sinus arrhythmia minimum. By contrast, younger pups showed poor or nonexistent sinus arrhythmia and shorter apnea durations with a variable and/or high heart rate during apnea. Apnea duration was positively correlated with the development of sinus arrhythmia and negatively correlated with both eupneic and apneic heart rate. Adult males showed extremely well-developed patterns of sinus arrhythmia and, in all cases, the minimum heart rate during the sinus arrhythmia was lower than the average heart rate recorded during apnea. These results suggest that seal pups are not born with the cardiac control associated with voluntary long duration apnea, but that apnea tolerance increases with refined cardiorespiratory control.

Patterns of respiration and heart rate during wakefulness and sleep in elephant seal pups.

Although breath holding during diving has been studied extensively in seals, the recent observation that these mammals also exhibit long-duration apnea while apparently sleeping has not been systematically examined. This project examined sleep apnea in northern elephant seal pups (Mirounga angustirostris). The animals exhibited a sequential sleep pattern of wakefulness-slow-wave sleep (SWS)-rapid eye movement (REM) sleep that resembled the normal pattern of mammalian sleep. The typical respiratory pattern during sleep in 4-mo-old pups consisted of short periods of continuous breathing separated by periods of apnea of up to 12 min. Several cycles of apnea and eupnea could occur during a single sleep episode. Breathing during a sleep cycle occurred only in SWS, never during REM sleep. The eupneic heart rate was characterized by significant sinus arrhythmia, and the apneic heart rate was similar to the minimum value during normal sinus arrhythmia. Patterns of change in breathing and heart rate associated with wakefulness and sleep were similar in seals sleeping underwater and on land. When sleeping underwater, the seals raised their heads to the surface to breathe without awakening. The changes in heart rate associated with normal sinus arrhythmia, sleep apnea, and diving apnea appear to be similar, suggesting regulation by a common homeostatic control mechanism.

The biochemistry of natural fasting at its limits.

There are several groups of animals that are adapted for extremely long duration fasting as part of their reproductive cycle. Penguins, bears and seals routinely fast without food or water for months at time. However, they do not 'starve', as the biochemical implications of starving are very different from those of successful fasting. There are distinct biochemical adaptations in lipid, carbohydrate and especially protein metabolism that allow these animals to survive. It appears, at least for penguins and seals, that the duration of the fast may be limited by changes that occur in biochemical regulation near the ned of the fast. In all of these species, the biochemistry of fasting and the ecological and behavioral demands of their breeding cycles are closely interrelated.