Advances in thermal physiology of diving marine mammals: The dual role of peripheral perfusion.

The ability to maintain a high core body temperature is a defining characteristic of all mammals, yet their diverse habitats present disparate thermal challenges that have led to specialized adaptations. Marine mammals inhabit a highly conductive environment. Their thermoregulatory capabilities far exceed our own despite having limited avenues of heat transfer. Additionally, marine mammals must balance their thermoregulatory demands with those associated with diving (i.e. oxygen conservation), both of which rely on cardiovascular adjustments. This review presents the progress and novel efforts in investigating marine mammal thermoregulation, with a particular focus on the role of peripheral perfusion. Early studies in marine mammal thermal physiology were primarily performed in the laboratory and provided foundational knowledge through in vivo experiments and ex vivo measurements. However, the ecological relevance of these findings remains unknown because comparable efforts on free-ranging animals have been limited. We demonstrate the utility of biologgers for studying their thermal adaptations in the context in which they evolved. Our preliminary results from freely diving northern elephant seals (Mirounga angustirostris) reveal blubber's dynamic nature and the complex interaction between thermoregulation and the dive response due to the dual role of peripheral perfusion. Further exploring the potential use of biologgers for measuring physiological variables relevant to thermal physiology in other marine mammal species will enhance our understanding of the relative importance of morphology, physiology, and behavior for thermoregulation and overall homeostasis.

Space use of Pacific harbor seals (Phoca vitulina richardii) from two haulout locations along the Oregon coast.

BACKGROUND: There are approximately 10,000-12,000 Pacific harbor seals (Phoca vitulina richardii) inhabiting the Oregon coast, and unlike other species of pinnipeds in this region, are reliably present year-round. Despite this, and drastic rebounds in population since the enactment of the Marine Mammal Protection Act, limited data is available for the present period regarding their space use at sea, and within estuarine, riverine, or bay areas within the state. OBJECTIVE: To examine site-based differences in space use for 24 adult Pacific harbor seals captured and outfitted with satellite transmitters at two predominant haulout sites on the Oregon Coast, USA. DESIGN: We captured 24 adult harbor seals from two haulout sites on the Central Oregon coast between September 2014-16 and fitted them with external Wildlife Computers SPOT5 satellite transmitters to track movement. Using state-space modeled locations derived from satellite telemetry data, we evaluated spatial behavior of these animals using a correlated random walk model via R package crawl. Kernel density estimation was subsequently used to calculate home range and core area for each animal. Percent use of open ocean habitat versus use of estuaries, rivers and bays was quantified, as was an initial examination of presence within five newly-established marine reserves in Oregon. Examination of haulout site-related differences in spatial behavior were examined for seals captured in Netarts and Alsea Bays, Oregon and haul out behavior related to time of day, season, and tidal level was also investigated. RESULTS: The average individual home range for seals was 364.47 ± 382.87 km2 with seals captured in Alsea bay demonstrating a significantly higher home range area than those captured in Netarts Bay. Alsea bay seals also tended to range farther from shore than Netarts Bay animals. The average calculated core area for seals encompassed on average 29.41 ± 29.23 km2 per animal, however the home range of one animal was so small, core area could not be calculated. Use of marine reserves was limited for animals in this study, representing less than 2% of locations with a majority occurring in Cape Perpetua Marine Reserve and North Marine Protected Area. Seals were more likely to haul out during low tides and periods of low light (dusk, night and dawn), and hauling out behavior increased in winter months. SIGNIFICANCE: These findings demonstrate the first major documentation of space use of harbor seals in the state for nearly three decades, and lends itself to future comparison and formation of mechanistically-based hypotheses for behavior of a common marine mammal in the highly productive northern California Current System.

Muscular apoptosis but not oxidative stress increases with old age in a long-lived diver, the Weddell seal.

Seals experience repeated bouts of ischemia-reperfusion while diving, potentially exposing their tissues to increased oxidant generation and thus oxidative damage and accelerated aging. We contrasted markers of oxidative damage with antioxidant profiles across age and sex for propulsive (longissismus dorsi) and maneuvering (pectoralis) muscles of Weddell seals to determine whether previously observed morphological senescence is associated with oxidative stress. In longissismus dorsi, old (age 17-26 years) seals exhibited a nearly 2-fold increase in apoptosis over young (age 9-16 years) seals. There was no evidence of age-associated changes in lipid peroxidation or enzymatic antioxidant profiles. In pectoralis, 4-hydroxynonenal-Lys (4-HNE-Lys) levels increased 1.5-fold in old versus young seals, but lipid hydroperoxide levels and apoptotic index did not vary with age. Glutathione peroxidase activity was 1.5-fold higher in pectoralis of old versus young animals, but no other antioxidants changed with age in this muscle. With respect to sex, no differences in lipid hydroperoxides or apoptosis were observed in either muscle. Males had higher HSP70 expression (1.4-fold) and glutathione peroxidase activity (1.3-fold) than females in longissismus dorsi, although glutathione reductase activity was 1.4-fold higher in females. No antioxidants varied with sex in pectoralis. These results show that apoptosis is not associated with oxidative stress in aged Weddell seal muscles. Additionally, the data suggest that adult seals utilize sex-specific antioxidant strategies in longissismus dorsi but not pectoralis to protect skeletal muscles from oxidative damage.

Juvenile Steller sea lion (Eumetopias jubatus) utilization distributions in the Gulf of Alaska.

BACKGROUND: A utilization distribution quantifies the temporal and spatial probability of space use for individuals or populations. These patterns in movement arise from individuals' internal state and from their response to the external environment, and thus can provide insights for assessing factors associated with the management of threatened populations. The Western Distinct Population Segment of the Steller sea lion (Eumetopias jubatus) has declined to approximately 20% of levels encountered 40 years ago. At the height of the decline, juvenile survival appeared to be depressed and currently there is evidence that juvenile mortality due to predation may be constraining recovery in some regions. Therefore, our objectives were to identify what spaces are biologically important to juvenile Steller sea lions in the Kenai Fjords and Prince William Sound regions of the Gulf of Alaska. METHODS: We examined geospatial location data from juvenile sea lions tagged between 2000 and 2014 (n = 84) and derived individual and pooled-population utilization distributions (UDs) from their movements. Core areas were defined from the UDs using an individual-based approach; this quantitatively confirmed that all individuals in our sample exhibited concentrated use within their home range (95% UD). Finally, we explored if variation in UD characteristics were associated with sex, season, age, or region. RESULTS: We found evidence that individual juvenile home ranges were region and sex-specific, with males having larger home ranges on average. Core space characteristics were also sex-specific, and exhibited seasonal patterns of reduced size, increased proximity to haulouts, and increased intensity of use in the summer, but only in the Kenai Fjords-Gulf of Alaska region. CONCLUSIONS: This study highlights the areas of biological importance during this vulnerable life history stage, and the demographic, seasonal, and spatial factors associated with variation in movement patterns for a marine mesopredator. This can be useful information for promoting species recovery, and for future efforts to understand ecological patterns such as predator-prey interactions.

Intraperitoneal implantation of life-long telemetry transmitters in three rehabilitated harbor seal pups.

BACKGROUND: Pinnipeds, including many phocid species of concern, are inaccessible and difficult to monitor for extended periods using conventional, externally attached telemetry devices that are shed during the annual molt. Archival satellite transmitters were implanted intraperitoneally into three stranded Pacific harbor seal pups (Phoca vitulina richardii) that completed rehabilitation, to evaluate the viability of this surgical technique for the deployment of life long telemetry devices in phocids. The life history transmitters record information throughout the life of the host and transmit data to orbiting satellites after extrusion following death. RESULTS: Surgeries were performed under general anesthesia and a single transmitter was inserted into the ventrocaudal abdominal cavity via a 7-8 cm incision along the ventral midline between the umbilicus and pubic symphysis or preputial opening in each animal. Surgeries lasted from 45 to 51 min, and anesthesic times ranged from 55 to 79 min. All animals recovered well, were released into dry holding pens overnight, and were given access to water the following day. All three animals exhibited an expected inflammatory response, with acute phase responses lasting approximately three to four weeks. All three animals were tracked via externally attached satellite transmitters after release at 58 to 78 days following surgery, and minimum post-release survival was confirmed through continued movement data received over 278 to 289 days. CONCLUSION: The initial findings of low morbidity and zero mortality encountered during captive observation and post-release tracking periods support the viability of this surgical technique for the implantation of long-term telemetry devices in phocids.

Individual-based energetic model suggests bottom up mechanisms for the impact of coastal hypoxia on Pacific harbor seal (Phoca vitulina richardii) foraging behavior.

Wind-driven coastal hypoxia represents an environmental stressor that has the potential to drive redistribution of gilled marine organisms, and thereby indirectly affect the foraging characteristics of air-breathing upper trophic-level predators. We used a conceptual individual-based model to simulate effects of coastal hypoxia on the spatial foraging behavior and efficiency of a marine mammal, the Pacific harbor seal (Phoca vitulina richardii) on the Oregon coast. Habitat compression of fish was simulated at varying intensities of hypoxia. Modeled hypoxia affected up to 80% of the water column and half of prey species' horizontal habitat. Pacific sand lance (Ammodytes hexapterus), Pacific herring (Clupea pallasii), and English sole (Parophrys vetulus) were selected as representative harbor seal prey species. Model outputs most affected by coastal hypoxia were seal travel distance to foraging sites, time spent at depth during foraging dives, and daily energy balance. For larger seals, English sole was the most optimal prey during normoxia, however during moderate to severe hypoxia Pacific sand lance was the most beneficial prey. For smaller seals, Pacific herring was the most efficient prey species during normoxia, but sand lance became more efficient as hypoxia increased. Sand lance represented the highest increase in foraging efficiency during severe hypoxic events for all seals. Results suggest that during increasing hypoxia, smaller adult harbor seals could benefit by shifting from foraging on larger neritic schooling fishes to foraging closer inshore on less energetically-dense forage fish. Larger adult seals may benefit by shifting from foraging on groundfish to smaller, schooling neritic fishes as hypoxia increases. The model suggests a mechanism by which hypoxia may result in increased foraging efficiency of Pacific harbor seals, and therefore increased rates of predation on coastal fishes on the continental shelf during hypoxic events.

Key Questions in Marine Megafauna Movement Ecology.

It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.

The Effect of Novel Research Activities on Long-term Survival of Temporarily Captive Steller Sea Lions (Eumetopias jubatus).

Two novel research approaches were developed to facilitate controlled access to, and long-term monitoring of, juvenile Steller sea lions for periods longer than typically afforded by traditional fieldwork. The Transient Juvenile Steller sea lion Project at the Alaska SeaLife Center facilitated nutritional, physiological, and behavioral studies on the platform of temporary captivity. Temporarily captive sea lions (TJs, n = 35) were studied, and were intraperitoneally implanted with Life History Transmitters (LHX tags) to determine causes of mortality post-release. Our goal was to evaluate the potential for long-term impacts of temporary captivity and telemetry implants on the survival of study individuals. A simple open-population Cormack-Jolly-Seber mark-recapture model was built in program MARK, incorporating resightings of uniquely branded study individuals gathered by several contributing institutions. A priori models were developed to weigh the evidence of effects of experimental treatment on survival with covariates of sex, age, capture age, cohort, and age class. We compared survival of experimental treatment to a control group of n = 27 free-ranging animals (FRs) that were sampled during capture events and immediately released. Sex has previously been show to differentially affect juvenile survival in Steller sea lions. Therefore, sex was included in all models to account for unbalanced sex ratios within the experimental group. Considerable support was identified for the effects of sex, accounting for over 71% of total weight for all a priori models with delta AICc <5, and over 91% of model weight after removal of pretending variables. Overall, most support was found for the most parsimonious model based on sex and excluding experimental treatment. Models including experimental treatment were not supported after post-hoc considerations of model selection criteria. However, given the limited sample size, alternate models including effects of experimental treatments remain possible and effects may yet become apparent in larger sample sizes.

Heat loss in air of an Antarctic marine mammal, the Weddell seal.

The conflicting needs of homeostasis in air versus water complicate our understanding of thermoregulation in marine mammals. Large-scale modeling efforts directed at predicting the energetic impact of changing sea ice conditions on polar ecosystems require a better understanding of thermoregulation in air of free-ranging animals. We utilized infrared imaging as an indirect approach to determine surface temperatures of dry, hauled-out Weddell seals (Leptonychotes weddellii, n = 35) of varying age and body condition during the Antarctic summer. The study groups provided a fivefold range in body mass and a threefold range in blubber depth. Surface temperature (T s) did not vary by body region (head, shoulder, axilla, torso, hip, flippers). Average seal T s (mean 13.9 ± 11.2 °C) was best described through a combination of the physical traits of body mass and environmental variables of ambient temperature T air, and wind speed. Additional factors of ice temperature (T ice), relative humidity and cloud cover did not improve the model. Heat transfer model estimates suggested that radiation contributed 56.6 ± 7.7 % of total heat loss. Convection and conduction accounted for the remaining 15.7 ± 12.3 and 27.7 ± 9.3 %, respectively. Heat loss by radiation was primarily influenced by body mass and wind speed, whereas convective heat loss was influenced primarily by blubber depth and wind speed. Conductive heat loss was modeled largely as a function of physical traits of mass and blubber depth rather than any environmental covariates, and therefore was substantially higher in animals in leaner condition.

Constraint lines and performance envelopes in behavioral physiology: the case of the aerobic dive limit.

Constraint lines-the boundaries that delimit point clouds in bivariate scattergrams-have been applied in macro-ecology to quantify the effects of limiting factors on response variables, but have not been applied to the behavioral performance and physiological ecology of individual vertebrates. I propose that behavioral scattergrams of air-breathing, diving vertebrates contain informative edges that convey insights into physiological constraints that shape the performance envelopes of divers. In the classic example of repeated cycles of apnea and eupnea in diving, air-breathing vertebrates, the need to balance oxygen consumption, and intake should differentially constrain recovery for dives within or exceeding the aerobic dive limit (ADL). However, the bulk of variance observed in recovery versus dive duration scattergrams originates from undetermined behavioral variables, and deviations from overall stasis may become increasingly apparent at progressively smaller scales of observation. As shown on dive records from 79 Galápagos fur seals, the selection of appropriate time scales of integration yields two distinct recovery boundaries for dive series within and beyond the estimated ADL. An analysis of the corresponding constraint lines is independent of central tendencies in data and avoids violating parametric assumptions for large data sets where variables of interest account for only a small portion of observed variance. I hypothesize that the intercept between these constraint lines represents the effective ADL, and present physiological and ecological considerations to support this hypothesis.

Predation on an upper trophic marine predator, the Steller sea lion: evaluating high juvenile mortality in a density dependent conceptual framework.

The endangered western stock of the Steller sea lion (Eumetopias jubatus)--the largest of the eared seals--has declined by 80% from population levels encountered four decades ago. Current overall trends from the Gulf of Alaska to the Aleutian Islands appear neutral with strong regional heterogeneities. A published inferential model has been used to hypothesize a continuous decline in natality and depressed juvenile survival during the height of the decline in the mid-late 1980's, followed by the recent recovery of juvenile survival to pre-decline rates. However, these hypotheses have not been tested by direct means, and causes underlying past and present population trajectories remain unresolved and controversial. We determined post-weaning juvenile survival and causes of mortality using data received post-mortem via satellite from telemetry transmitters implanted into 36 juvenile Steller sea lions from 2005 through 2011. Data show high post-weaning mortality by predation in the eastern Gulf of Alaska region. To evaluate the impact of such high levels of predation, we developed a conceptual framework to integrate density dependent with density independent effects on vital rates and population trajectories. Our data and model do not support the hypothesized recent recovery of juvenile survival rates and reduced natality. Instead, our data demonstrate continued low juvenile survival in the Prince William Sound and Kenai Fjords region of the Gulf of Alaska. Our results on contemporary predation rates combined with the density dependent conceptual framework suggest predation on juvenile sea lions as the largest impediment to recovery of the species in the eastern Gulf of Alaska region. The framework also highlights the necessity for demographic models based on age-structured census data to incorporate the differential impact of predation on multiple vital rates.

Aerobic dive limit does not decline in an aging pinniped.

Apneustic hunters such as diving mammals exploit body oxygen stores while submerged; therefore, any decline in oxygen handling at advanced life stages could critically impair foraging ability. We calculated the aerobic dive limit (cADL = 17.9 ± 4.4 min SD) from blood and muscle oxygen stores and published metabolic rates of Weddell seals within (9-16 years, n = 24) and beyond peak-reproductive age (17-27 years, n = 26), to investigate (1) senescent constraints in apneustic hunting, and (2) whether mass or age primarily determines oxygen stores and ADL in older seals. We compared cADL with behavioral ADL from 5,275 free-ranging dives (bADL = 24.0 ± 5.3 min, n = 18 females). We observed no changes in Weddell seal oxygen stores, its determinants, or in ADLs late in life. Oxygen stores were better predicted by mass than age, consistent with published findings for young adults. Hematological panels (n = 6) were consistent across mass and age, though hematocrit (females > males, 6% elevation) and mean corpuscular hemoglobin content (females < males, 8% reduction) varied by sex. Whole blood viscosity was decreased with increasing mass in females and was higher than in males overall (+18%). This was largely due to elevated hematocrit in females, although plasma viscosity also varied under some conditions. Females had higher blood volume and elevated blood oxygen stores (vol% body mass), which did not translate into significantly higher cADL (18.1 vs. 17.1 min for males). Neither cADL nor bADL were mass- or age-dependent.

Health and condition in the adult Weddell seal of McMurdo Sound, Antarctica.

Weddell seals (Leptonychotes weddellii) are large-bodied, long-lived mammals that live only in the circumpolar Antarctic. As such, they represent an ideal sentinel species for the impacts of environmental change on polar species. However, longitudinal physiological studies of marine mammals are notoriously difficult due to their largely aquatic lifestyle, such that many baseline indicators of health and condition are not well defined. Fifty known-age, adult seals (9-27 years, 24 males, 26 females) in McMurdo Sound were sampled for mass, total body fat, blubber depth and a suite of blood parameters (21 variables) to assess hydration state, nutritional plane, reproductive hormones (females only), organ function and immune status. Total body mass increased with age, whereas variation in blubber depth was best described by mass and/or sex, with an overall greater blubber thickness in female seals (p<0.001). Ten blood parameters showed a significant effect of one or more model variables, most prominently between the sexes. Serum chemistry suggested that females were better nourished and displayed lower indicators of acute stress compared to males. We noted limited age-related declines that might indicate impaired organ function. Overall, seals demonstrated clinically normal values for large mammals, even at the upper end of the age continuum. Future physiological studies in this species are strongly encouraged to incorporate potential sex effects in experimental design and analysis.

The effects of two analgesic regimes on behavior after abdominal surgery in Steller sea lions.

This study examined the effects of two non-steroidal anti-inflammatory drug (NSAID) treatment protocols on the behavioral responses of juvenile Steller sea lions after abdominal surgery. Sea lions were randomly assigned to one of two treatments designed to control post-operative pain. The flunixin group (n=6) received flunixin meglumine (1mg/kg) administered as a single intramuscular (IM) injection before extubation from surgery. The carprofen group (n=5) received carprofen (4.4 mg/kg) as an IM injection before extubation, then orally at 24, 48 and 72 h after surgery. Seven behaviors related to post-operative pain were monitored by observers, blinded to treatment, for a total of 10 days (3 days pre-, day of surgery, and 6 days post-surgery). All seven behaviors changed after surgery regardless of NSAID treatment, two of which returned to baseline within 6 days of surgery. Only one behavior was mildly affected by analgesic treatment: sea lions in the carprofen group tended to spend less time lying down in Days 1-3 following surgery (i.e., the days which they received oral carprofen). These results suggested that neither treatment, at the dose administered, was effective in controlling pain in the days following this surgery.

Energetics of breath-hold hunting: modeling the effects of aging on foraging success in the Weddell seal.

A simulation model was developed to predict age-related changes in foraging energetics of individual Weddell seals, Leptonychotes weddellii. Aging in diving animals is interesting because their characteristic cyclic sequence of apneustic hunting and eupnea should elevate oxidative stress, possibly accelerating aging. Such a hypothesis can be evaluated by modeling energetics of constrained, time-partitioned activities with well-defined costs. Three possible consequences of physiological aging in divers were specified and appraised. The model examined the potential impacts of age-related decline in muscle contractile ability, increased buoyancy, and reduced aerobic dive limit, alone and in combination, on a daily energy budget. A uniform age effect evident in model outputs is reduced foraging efficiency. The components of this net effect are exacerbated for sub-optimal behavioral-response settings or environmental conditions. The model predicts that with advancing age, efficiency declines increase for aging scenarios in the following order: simulated 'young' adults; 'old' seals with increased buoyancy; 'old' seals with reduced aerobic dive limit; 'old' seals having reduced muscle contractile efficiency; and, 'old' seals with all three conditions. The model indicates narrowed behavioral options to maintain positive energy balance in older animals, suggesting that behavioral plasticity may not allow older animals to compensate for age-related performance constraints.

Chemical immobilization of Weddell seals (Leptonychotes weddellii) by ketamine/midazolam combination.

OBJECTIVE: To provide reliable, effective immobilization for Weddell seals under extreme field conditions using an injectable ketamine/midazolam combination. STUDY DESIGN: Observational study. ANIMALS: Thirty adult Weddell seals (12 male, 18 female) in Erebus Bay, Antarctica, body mass (mean +/- SD) 412 +/- 47 kg, aged 9-27 years. METHODS: Seals were immobilized with a target dose of 2 mg kg(-1) ketamine hydrochloride and 0.1 mg kg(-1) midazolam hydrochloride (IM), based on visually estimated body mass. When required, maintenance doses were administered at a target of 0.5 mg kg(-1) ketamine hydrochloride and 0.025 mg kg(-1) midazolam hydrochloride (IV). RESULTS: Complete immobilization was achieved in 33 of 40 injections (14 of which were repeat events on the same individual). Time to immobilization averaged 12 +/- 4 minutes, with a duration of initial immobility of 38 +/- 19 minutes. Total immobilization time varied by handling protocol, including condition assessment and muscle biopsy (Protocol 1, 60 +/- 13 minutes), condition assessment and instrument attachment (Protocol 2, 154 +/- 13 minutes), and condition assessment, muscle biopsy and instrument retrieval (Protocol 3, 48 +/- 8 minutes). Overall, a total immobilization time of 114 +/- 60 minutes was accomplished with 4 +/- 4 maintenance doses, and an average recovery time of 36 +/- 17 minutes. Most effects of the anesthetic combination were unrelated to mass, age, sex or total body fat. However, leaner seals had longer duration of initial immobility (% and kg total body fat) and recovery times (kg fat). Apnea events were uncommon and treated effectively with doxapram. No animals died. CONCLUSIONS AND CLINICAL RELEVANCE: Reliable and effective field immobilization of Weddell seals was accomplished with a low dose of ketamine hydrochloride and midazolam hydrochloride, utilizing IM injection initially and IV maintenance methods.

Muscle aging and oxidative stress in wild-caught shrews.

Red-toothed shrews (Soricidae, subfamily Soricinae) are an intriguing model system to examine the free-radical theory of aging in wild mammals, given their short (<18months) lifespan and high mass-specific metabolic rates. As muscle performance underlies both foraging ability and predator avoidance, any age-related decline should be detrimental to fitness and survival. Muscle samples of water shrews (Sorex palustris) and sympatrically distributed short-tailed shrews (Blarina brevicauda) were therefore assessed for oxidative stress markers, protective antioxidant enzymes and apoptosis. Activity levels of catalase and glutathione peroxidase increased with age in both species. Similarly, Cu,Zn-superoxide dismutase isoform content was elevated significantly in older animals of both species (increases of 60% in the water shrew, 25% in the short-tailed shrew). Only one oxidative stress marker (lipid peroxidation) was age-elevated; the others were stable or declined (4-hydroxynonenal adducts and dihydroethidium oxidation). Glutathione peroxidase activity was significantly higher in the short-tailed shrew, while catalase activity was 2x higher in water shrews. Oxidative stress indicators were on average higher in short-tailed shrews. Apoptosis occurred in <1% of myocytes examined, and did not increase with age. Within the constraints of the sample size we found evidence of protection against elevated oxidative stress in wild-caught shrews.

Muscle senescence in short-lived wild mammals, the soricine shrews Blarina brevicauda and Sorex palustris.

Red-toothed (soricine) shrews are consummate predators exhibiting the highest energy turnovers and shortest life spans (ca. 18 months) of any mammal, yet virtually nothing is known regarding their physiological aging. We assessed the emerging pattern of skeletal muscle senescence (contractile/connective tissue components) in sympatric species, the semi-aquatic water shrew (WS), Sorex palustris, and the terrestrial short-tailed shrew (STS), Blarina brevicauda, to determine if muscle aging occurs in wild, short-lived mammals (H(0): shrews do not survive to an age where senescence occurs), and if so, whether these alterations are species-specific. Gracilis muscles were collected from first-year (n=17) and second-year (n=17) field-caught shrews. Consistent with typical mammalian aging, collagen content (% area) increased with age in both species (S. palustris: approximately 50%; B. brevicauda: approximately 60%). Muscle was dominated by stiffer Type I collagen, and the ratio of collagen Type I:Type III more than doubled with age. The area ratio of muscle:collagen decreased with age in both species, but was considerably lower in adult STS, suggesting species-specificity of senescence. Extracellular space was age-elevated in B. brevicauda, but was preserved in S. palustris ( approximately 50 vs. 10% elevation). Though juvenile interspecific comparisons revealed no significance, adult WS myocytes had 68% larger cross-sectional area and occurred at 28% lower fibers/area than those of adult STS. We demonstrate that age-related muscle senescence does occur in wild-caught, short-lived mammals, and we therefore reject this classic aging theory tenet. Our findings moreover illustrate that differential age adjustments in contractile/connective tissue components of muscle occur in the two species of wild-caught shrews.

Diving into old age: muscular senescence in a large-bodied, long-lived mammal, the Weddell seal (Leptonychotes weddellii).

Classic aging theory postulates the absence of pronounced organismal senescence in wild animals since mortality probably occurs first. Large-bodied, long-lived mammals are a recognized exception to this tenet, yet organismal senescence has not been investigated to date in such mammals in the wild. Furthermore, oxidative stress theory of aging supports the suggestion that exercise hypoxia, as regularly incurred during apneustic foraging in diving mammals might lead to cellular dysfunction and accelerated aging. To determine if an aspect of organismal senescence occurs in wild marine mammals, we examined the pattern of skeletal muscle aging (contractile and connective tissue components of longissimus dorsi and pectoralis muscles) in free-ranging adult Weddell seals (9-26 years). The average myocyte cross-sectional area was 22% greater with age in the longissiums dorsi, but no significant increase occurred in the pectoralis. Cross-sectional area was not related to body mass. Changes in myocyte number per area were consistent with the 35-40% age-increase in extracellular space in both muscle groups. Also consistent with extracellular space remodeling, total and relative collagen contents were significantly elevated in older seals (115% in longissimus dorsi; 65% in pectoralis). The ratio of muscle myocyte to collagen declined with age (50-63%) at both sites. Additionally, a shift towards a higher ratio of type I to type III collagen occurred with advancing age in both muscle groups (79% increase in pectoralis; 49% in longissimus dorsi). We reject the classic tenet and null-hypothesis that Weddell seals do not survive to an age where muscular senescence becomes detectable.

Intraperitoneal implantation of life-long telemetry transmitters in otariids.

BACKGROUND: Pinnipeds, including many endangered and declining species, are inaccessible and difficult to monitor for extended periods using externally attached telemetry devices that are shed during the annual molt. Archival satellite transmitters were implanted intraperitoneally into four rehabilitated California sea lions (Zalophus californianus) and 15 wild juvenile Steller sea lions (Eumetopias jubatus) to determine the viability of this surgical technique for the deployment of long-term telemetry devices in otariids. The life history transmitters record information throughout the life of the host and transmit data to orbiting satellites after extrusion following death of the host. RESULTS: Surgeries were performed under isoflurane anesthesia and single (n = 4) or dual (n = 15) transmitters were inserted into the ventrocaudal abdominal cavity via an 8.5 to 12 cm incision along the ventral midline between the umbilicus and pubic symphysis or preputial opening. Surgeries lasted 90 minutes (SD = 8) for the 19 sea lions. All animals recovered well and were released into the wild after extended monitoring periods from 27 to 69 days at two captive animal facilities. Minimum post-implant survival was determined via post-release tracking using externally attached satellite transmitters or via opportunistic re-sighting for mean durations of 73.7 days (SE = 9.0, Z. californianus) and 223.6 days (SE = 71.5, E. jubatus). CONCLUSION: The low morbidity and zero mortality encountered during captive observation and post-release tracking periods confirm the viability of this surgical technique for the implantation of long-term telemetry devices in otariids.