James L. Bodkin

Microsatellite DNA and mitochondrial DNA variation in remnant and translocated sea otter(Enhydra lutris) populations

Abstract All existing sea otter (Enhydra lutris) populations have suffered at least 1, and in some cases 2, population bottlenecks. The 1st occurred during the 18th and 19th centuries as a result of commercial hunting that eliminated sea otters from much their native range and reduced surviving populations to small remnants. The 2nd bottleneck occurred when small numbers of otters were reintroduced, via translocation, to areas where the species had been eliminated. We examined genetic variation at 7 microsatellite loci and the mitochondrial DNA (mtDNA) control region in 3 remnant populations, Amchitka Island (Aleutian Islands, Alaska), central coastal California, and Prince William Sound (Alaska), and in 2 reintroduced populations, southeast Alaska and Washington, that were founded with transplants from Amchitka, and in the case of southeast Alaska, individuals from Prince William Sound as well. We found no evidence of reduced genetic diversity in translocated populations. Average expected microsatellite heterozygosities (HE) were similar in all populations (range, 0.40–0.47), and mtDNA haplotype diversities were higher in reintroduced populations (0.51 for both Washington and southeast Alaska) than in remnant populations (X̄ = 0.35; range, 0.18–0.45). The levels of genetic diversity we observed within sea otter populations were relatively low when compared with other mammals and are thought to be the result of fur trade exploitation.

INCORPORATING DIVERSE DATA AND REALISTIC COMPLEXITY INTO DEMOGRAPHIC ESTIMATION PROCEDURES FOR SEA OTTERS

Reliable information on historical and current population dynamics is central to understanding patterns of growth and decline in animal populations. We developed a maximum likelihood-based analysis to estimate spatial and temporal trends in age/sex-specific survival rates for the threatened southern sea otter (Enhydra lutris nereis), using annual population censuses and the age structure of salvaged carcass collections. We evaluated a wide range of possible spatial and temporal effects and used model averaging to incorporate model uncertainty into the resulting estimates of key vital rates and their variances. We compared these results to current demographic parameters estimated in a telemetry-based study conducted between 2001 and 2004. These results show that survival has decreased substantially from the early 1990s to the present and is generally lowest in the north-central portion of the populations range. The greatest temporal decrease in survival was for adult females, and variation in the survival of this age/sex class is primarily responsible for regulating population growth and driving population trends. Our results can be used to focus future research on southern sea otters by highlighting the life history stages and mortality factors most relevant to conservation. More broadly, we have illustrated how the powerful and relatively straightforward tools of information-theoretic-based model fitting can be used to sort through and parameterize quite complex demographic modeling frameworks.

Using Ecological Function to Develop Recovery Criteria for Depleted Species: Sea Otters and Kelp Forests in the Aleutian Archipelago

Recovery criteria for depleted species or populations normally are based on demographic measures, the goal being to maintain enough individuals over a sufficiently large area to assure a socially tolerable risk of future extinction. Such demographically based recovery criteria may be insufficient to restore the functional roles of strongly interacting species. We explored the idea of developing a recovery criterion for sea otters (Enhydra lutris) in the Aleutian archipelago on the basis of their keystone role in kelp forest ecosystems. We surveyed sea otters and rocky reef habitats at 34 island-time combinations. The system nearly always existed in either a kelp-dominated or deforested phase state, which was predictable from sea otter density. We used a resampling analysis of these data to show that the phase state at any particular island can be determined at 95% probability of correct classification with information from as few as six sites. When sea otter population status (and thus the phase state of the kelp forest) was allowed to vary randomly among islands, just 15 islands had to be sampled to estimate the true proportion that were kelp dominated (within 10%) with 90% confidence. We conclude that kelp forest phase state is a more appropriate, sensitive, and cost-effective measure of sea otter recovery than the more traditional demographically based metrics, and we suggest that similar approaches have broad potential utility in establishing recovery criteria for depleted populations of other functionally important species.

Estimating age of sea otters with cementum layers in the first premolar

We assessed sources of variation in the use of tooth cementum layers to determine age by comparing counts in premolar tooth sections to known ages of 20 sea otters (Enhydra lutris). Three readers examined each sample 3 times, and the 3 readings of each sample were averaged by reader to provide the mean estimated age. The mean (SE) of the known age sample was 5.2 years (1.0) and the 3 mean estimated ages were 7.0 (1.0), 5.9 (1.1) and, 4.4 (0.8). The proportions of estimates accurate to within ±1 year were 0.25, 0.55, and 0.65 and to within ±2 years 0.65, 0.80, and 0.70, by reader. The proportions of samples estimated with >3 years error were 0.20, 0.10, and 0.05. Errors as large as 7, 6, and 5 years were made among readers. In few instances did all readers uniformly provide either accurate (error 1 yr) counts. In most cases (0.85), 1 or 2 of the readers provided accurate counts. Coefficients of determination (R 2 ) between known ages and mean estimated ages were 0.81, 0.87, and 0.87, by reader. The results of this study suggest that cementum layers within sea otter premolar teeth likely are deposited annually and can be used for age estimation. However. criteria used in interpreting layers apparently varied by reader, occasionally resulting in large errors, which were not consistent among readers. While large errors were evident for some individual otters, there were no differences between the known and estimated age-class distributions generated by each reader. Until accuracy can be improved, application of this ageing technique should be limited to sample sizes of at least 6-7 individuals within age classes of ≥ 1 year.

Mitochondrial-DNA variation among subspecies and populations of sea otters (Enhydra lutris)

We used restriction-enzyme analysis of polymerase-chain reaction-amplified, mitochondrial DNA (mtDNA) to assess genetic differentiation of subspecies and populations of sea otters, Enhydra lutris , throughout the range of the species. There were several haplotypes of mtDNA in each subspecies and geographically separate populations. MtDNA sequence divergence of haplotypes of sea otters was 0.0004–0.0041 base substitutions per nucleotide. E. L nereis appears to have monophyletic mitochondrial DNA, while E. I. lutris and E. I. kenyoni do not. Different frequencies of haplotypes of mtDNA among populations reflect current restriction of gene flow and the unique histories of different populations. There are two or three haplotypes of mtDNA and diversity of haplotypes is 0.1376–0.5854 in each population of otters. This is consistent with theoretical work, which suggests that population bottlenecks of sea otters probably did not result in major losses of genetic variation for individual populations, or the species as a whole.

Could residual oil from the Exxon Valdez spill create a long-term population ''sink'' for sea otters in Alaska?

Over 20 years ago, the Exxon Valdez oil tanker spilled 42 million L of crude oil into the waters of Prince William Sound, Alaska, USA. At the time of the spill, the sea otter (Enhydra lutris) population inhabiting the spill area suffered substantial acute injuries and loss. Subsequent research has resulted in one of the best-studied species responses to an oil spill in history. However, the question remains: Is the spill still influencing the Prince William Sound sea otter population? Here we fit time-varying population models to data for the sea otter population of western Prince William Sound to quantify the duration and extent of mortality effects from the spill. We hypothesize that the patchy nature of residual oil left in the environment has created a source-sink population dynamic. We fit models using the age distributions of both living and dying animals and estimates of sea otter population size to predict the number of sea otters in the hypothesized sink population and the number lost to this sink due to chronic exposure to residual oil. Our results suggest that the sink population has remained at just over 900 individuals (95% CI: 606-960) between 1990 and 2009, during which time prime-age survival remained 2-6% below pre-spill levels. This reduced survival led to chronic losses of ;900 animals over the past two decades, which is similar in magnitude to the number of sea otter deaths documented in western Prince William Sound during the acute phase of the spill. However, the unaffected source population appears to be counterbalancing these losses, with the model indicating that the sea otter population increased from ;2150 individuals in 1990 to nearly 3000 in 2009. The most optimistic interpretation of our results suggests that mortality effects dissipated between 2005 and 2007. Our results suggest that residual oil can affect wildlife populations on time scales much longer than previously believed and that cumulative chronic effects can be as significant as acute effects. Further, source-sink population dynamics can explain the slow recovery observed in the spill-affected western Prince William Sound sea otter population and are consistent with available data.

Activity Budgets Derived From Time–Depth Recorders in a Diving Mammal

Abstract We describe a method to convert continuously collected time–depth data from archival time–depth recorders (TDRs) into activity budgets for a benthic-foraging marine mammal. We used data from 14 TDRs to estimate activity-specific time budgets in sea otters (Enhydra lutris) residing near Cross Sound, southeast Alaska, USA. From the TDRs we constructed a continuous record of behavior for each individual over 39–46 days during summer of 1999. Behaviors were classified as foraging (diving to the bottom), other diving (traveling, grooming, interacting), and nondiving (assumed resting). The overall average activity budget (proportion of 24-hr/d) was 0.37 foraging (8.9 hr/d), 0.11 in other diving (2.6 hr/d), and 0.52 nondiving time (12.5 hr/d). We detected significant differences in activity budgets among individuals and between groups within our sample. Historically, the sea otter population in our study area had been expanding and sequentially reoccupying vacant habitat since their reintroduction to the area in the 1960s, and our study animals resided in 2 adjacent yet distinct locations. Males (n = 5) and individuals residing in recently occupied habitat (n = 4) spent 0.28–0.30 of their time foraging (6.7–7.2 hr/d), 0.17–0.18 of their time in other diving behaviors (4.1–4.3 hr/d), and 0.53–0.54 of their time resting (12.7–13.0 hr/d). In contrast, females (n = 9) and individuals residing in longer occupied habitat (n = 10) spent 0.40 of their time foraging (9.6 hr/d), 0.08–0.09 of their time in other diving behaviors (1.9–2.2 hr/d), and 0.51–0.52 of their time resting (12.2–12.5 hr/d). Consistent with these differences, sea otters residing in more recently occupied habitat captured more and larger clams (Saxidomus spp., Protothaca spp., Macoma spp., Mya spp., Clinocardium spp.) and other prey, and intertidal clams were more abundant and larger in this area. We found that TDRs provided data useful for measuring activity time budgets and behavior patterns in a diving mammal over long and continuous time periods. Fortuitous contrasts in time budgets between areas where our study animals resided suggest that activity time budgets estimated from TDRs may be a sensitive indicator of population status, particularly in relation to prey availability.

Gene transcription in sea otters (Enhydra lutris); development of a diagnostic tool for sea otter and ecosystem health

Gene transcription analysis for diagnosing or monitoring wildlife health requires the ability to distinguish pathophysiological change from natural variation. Herein, we describe methodology for the development of quantitative real‐time polymerase chain reaction (qPCR) assays to measure differential transcript levels of multiple immune function genes in the sea otter (Enhydra lutris); sea otter‐specific qPCR primer sequences for the genes of interest are defined. We establish a ‘reference’ range of transcripts for each gene in a group of clinically healthy captive and free‐ranging sea otters. The 10 genes of interest represent multiple physiological systems that play a role in immuno‐modulation, inflammation, cell protection, tumour suppression, cellular stress response, xenobiotic metabolizing enzymes, antioxidant enzymes and cell–cell adhesion. The cycle threshold (CT) measures for most genes were normally distributed; the complement cytolysis inhibitor was the exception. The relative enumeration of multiple gene transcripts in simple peripheral blood samples expands the diagnostic capability currently available to assess the health of sea otters in situ and provides a better understanding of the state of their environment.

Assessment of clinical pathology and pathogen exposure in sea otters (Enhydra lutris) bordering the threatened population in Alaska.

Northern sea otter (Enhydra lutris kenyoni) abundance has decreased dramatically over portions of southwest Alaska, USA, since the mid-1980s, and this stock is currently listed as threatened under the Endangered Species Act. In contrast, adjacent populations in south central Alaska, USA, and Russia have been stable to increasing during the same period. Sea otters bordering the area classified in the recent decline were live-captured during 2004–2006 at Bering Island, Russia, and the Kodiak Archipelago, Alaska, USA, to evaluate differences in general health and current exposure status to marine and terrestrial pathogens. Although body condition was lower in animals captured at Bering Island, Russia, than it was at Kodiak, USA, clinical pathology values did not reveal differences in general health between the two regions. Low prevalences of antibodies (>5%) were found in Kodiak, USA, and on Bering Island, Russia, to Toxoplasma gondii, Sarcocystis neurona, and Leptospira interrogans. Exposure to phocine herpesvirus-1 was found in both Kodiak, USA (15.2%), and Bering Island, Russia (2.3%). Antibodies to Brucella spp. were found in 28% of the otters tested on Bering Island, Russia, compared with only 2.7% of the samples from Kodiak, USA. Prevalence of exposure to Phocine distemper virus (PDV) was 41% in Kodiak, USA, but 0% on Bering Island, Russia. Archived sera from southwest and south-central Alaska dating back to 1989 were negative for PDV, indicating exposure occurred in sea otters in Kodiak, USA, in recent years. Because PDV can be highly pathogenic in naïve and susceptible marine mammal populations, tissues should be examined to explore the contribution of this virus to otter deaths. Our results reveal an increase in exposure to pathogens in sea otters in Kodiak, Alaska, USA, since the 1990s.

The Nearshore Benthic Community of Kasatochi Island, One Year after the 2008 Volcanic Eruption

Abstract A description is presented of the nearshore benthic community of Kasatochi Island 10–12 months after a catastrophic volcanic eruption in 2008. The eruption extended the coastline of the island approximately 400 m offshore, mainly along the south, southeast, and southwest shores, to roughly the 20 m isobath. Existing canopy kelp of Eualaria (Alaria) fistulosa, as well as limited understory algal species and associated fauna (e.g., urchin barrens) on the hard substratum were apparently buried following the eruption. Samples and observations revealed the substrate around the island in 2009 was comprised almost entirely of medium and coarse sands with a depauperate benthic community, dominated by opportunistic pontogeneiid amphipods. Comparisons of habitat and biological communities with other nearby Aleutian Islands, as well as with the Icelandic volcanic island of Surtsey, confirm dramatic reductions in flora and fauna consistent with an early stage of recovery from a large-scale disturbance event.