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

In cold blood: evidence of Pacific sleeper shark (Somniosus pacificus) predation on Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska

Temperature data received post mortem in 2008–13 from 15 of 36 juvenile Steller sea lions (Eumetopias jubatus) that had been surgically implanted in 2005–11 with dual life history transmitters (LHX tags) indicated that all 15 animals died by predation. In 3 of those 15 cases, at least 1 of the 2 LHX tags was ingested by a cold-blooded predator, and those tags recorded, immediately after the sea lion’s death, temperatures that corresponded to deepwater values. These tags were regurgitated or passed 5–11 days later by predators. Once they sensed light and air, the tags commenced transmissions as they floated at the ocean surface, reporting temperatures that corresponded to regional sea-surface estimates. The circumstances related to the tag in a fourth case were ambiguous. In the remaining 11 cases, tags sensed light and air immediately after the sea lion’s death and reported temperatures that corresponded to estimates of regional sea-surface temperatures. In these 11 cases, circumstances did not allow for inferences on the species of predator. Among reported poikilotherm predators of Steller sea lions, only the Pacific sleeper shark (Somniosus pacificus) is known to have body core temperatures that are near ambient. The data from this study indicate that Pacific sleeper sharks need to be considered as a possible source of mortality of juvenile Steller sea lions in the region of the Gulf of Alaska

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

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

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

Spatially explicit detection of predation on individual pinnipeds from implanted post-mortem satellite data transmitters

To directly determine mortality and predation in the endangered western Steller sea lion Eumetopias jubatus, we deployed implanted, satellite-linked post-mortem data transmitters in 21 juveniles. Data recovered from 4 of 5 detected mortalities exhibited precipitous drops in ambient temperatures followed by immediate onset of transmissions (N = 3), or gradual cooling and delayed transmissions (N = 1). Precipitous drop data sets were classified as acute death at sea by trauma. A model to estimate algor mortis (body cooling) as a function of mass and ambient conditions was validated through simulations on 4 carcasses. Model outputs suggest that cooling rate masses can be qualitatively distinguished if well outside the prediction uncertainties. The observed gradual cooling rate was best described by a modeled mass one-sixth the animal’s mass at release, supporting the classification of the fourth event as acute death at sea by trauma. This suggests that at least 4 in 5 detected mortalities likely represent acute deaths at sea, probably due to predation. We conclude that precipitous drop events with immediate transmissions can be classified as acute death likely by predation, but gradual cooling events with delayed transmission should be reviewed on a case-by-case basis. In 3 cases that provided both ante-mortem and post-mortem locations from external and implanted transmitters, respectively, these differed by less than 17 km, illustrating that this technique provides spatially explicit data of predation on individual sea lions.Keywords: Algor mortis, Telemetry, Eumetopias jubatus, Predation, Mortality, Steller sea lio

Cumulative survival for juvenile Steller sea lions for ages 13 through 60 months estimated by different methods.

<p>Model LHX-eGOA is based on LHX transmitter data returns. Models HFYS are from a published inferential model <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0030173#pone.0030173-Holmes1" target="_blank">[21]</a> for three distinct time periods. Numbers in parentheses are 95% confidence intervals where available.</p

Juvenile survival and the juvenile fraction modeled as a function of Steller sea lion abundance.

<p>Juvenile survivorship is shown as the percentage of all juveniles ages 2–4 years that survive to the end of a year. The J/T metric is the count of all juveniles ages 2–4 years divided by the count of all ages 2–31 years (excluding only pups). (A) The <i>Flat</i> numerical response. (B) The <i>Linear</i> numerical response. (C) The <i>Sigmoid</i> numerical response.</p

Locations of juvenile Steller sea lion mortalities detected in the Gulf of Alaska.

<p>Eleven predation events indicated by open circles occurred in the eastern and central Gulf of Alaska (GOA). One mortality of undetermined cause indicated by the solid hexagon occurred in Prince William Sound. The endangered Western Distinct Population Segment is located to the west of 144° longitude.</p