Verena A. Gill

Phocine Distemper Virus in Northern Sea Otters in the Pacific Ocean, Alaska, USA

Phocine distemper virus (PDV) has caused 2 epidemics in harbor seals in the Atlantic Ocean but had never been identified in any Pacific Ocean species. We found that northern sea otters in Alaska are infected with PDV, which has created a disease threat to several sympatric and decreasing Pacific marine mammals.

CONSERVATION STATUS OF THE BUFF-BREASTED SANDPIPER: HISTORIC AND CONTEMPORARY DISTRIBUTION AND ABUNDANCE IN SOUTH AMERICA

Abstract We present historic and contemporary information on the distribution and abundance of Buff-breasted Sandpipers (Tryngites subruficollis) in South America. Historic information was collated from the literature, area ornithologists, and museums, whereas contemporary data were derived from surveys conducted throughout the main wintering range in Argentina, Uruguay, and Brazil during the austral summers of 1999 and 2001. Variable circular plot sampling was used to estimate population densities. During 1999, the highest concentration of Buff-breasted Sandpipers in Argentina was in southern Bahía Samborombón (General Lavalle District) and areas north of Mar Chiquita coastal lagoon. During 2001, the highest concentrations in Brazil were at Ilha da Torotama and Lagoa do Peixe National Park. During 1999 and 2001, the highest concentrations of Buff-breasted Sandpipers in Uruguay were found along three lagoons (Laguna de Rocha, Laguna de Castillos, and Laguna Garzón) bordering the Atlantic Ocean. Population densities (birds/ha) of Buff-breasted Sandpipers were 0.11 (95% C.I. = 0.04–0.31) in Argentina, 1.62 (0.67–3.93) in Brazil, and 1.08 (0.37–3.18) in Uruguay. High turnover rates at survey sites, due to the formation of large, mobile flocks, contributed to moderately large confidence intervals around our population density estimates. Nevertheless, compared with historic accounts of Buff-breasted Sandpipers, our survey data indicate the population size of this species has declined substantially since the late 1800s and contemporary information suggests the species has continued to decline during the past three decades. Buff-breasted Sandpipers were found almost exclusively in pasturelands and appear to depend heavily upon intensive grazing by livestock, which maintain suitable short grass conditions. We discuss the need for protection of critical areas and proper range management to ensure appropriate habitat remains available for the species, and provide suggestions for future research needs.

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.

Prevalence of algal toxins in Alaskan marine mammals foraging in a changing arctic and subarctic environment

Current climate trends resulting in rapid declines in sea ice and increasing water temperatures are likely to expand the northern geographic range and duration of favorable conditions for harmful algal blooms (HABs), making algal toxins a growing concern in Alaskan marine food webs. Two of the most common HAB toxins along the west coast of North America are the neurotoxins domoic acid (DA) and saxitoxin (STX). Over the last 20 years, DA toxicosis has caused significant illness and mortality in marine mammals along the west coast of the USA, but has not been reported to impact marine mammals foraging in Alaskan waters. Saxitoxin, the most potent of the paralytic shellfish poisoning toxins, has been well-documented in shellfish in the Aleutians and Gulf of Alaska for decades and associated with human illnesses and deaths due to consumption of toxic clams. There is little information regarding exposure of Alaskan marine mammals. Here, the spatial patterns and prevalence of DA and STX exposure in Alaskan marine mammals are documented in order to assess health risks to northern populations including those species that are important to the nutritional, cultural, and economic well-being of Alaskan coastal communities. In this study, 905 marine mammals from 13 species were sampled including; humpback whales, bowhead whales, beluga whales, harbor porpoises, northern fur seals, Steller sea lions, harbor seals, ringed seals, bearded seals, spotted seals, ribbon seals, Pacific walruses, and northern sea otters. Domoic acid was detected in all 13 species examined and had the greatest prevalence in bowhead whales (68%) and harbor seals (67%). Saxitoxin was detected in 10 of the 13 species, with the highest prevalence in humpback whales (50%) and bowhead whales (32%). Pacific walruses contained the highest concentrations of both STX and DA, with DA concentrations similar to those detected in California sea lions exhibiting clinical signs of DA toxicosis (seizures) off the coast of Central California, USA. Forty-six individual marine mammals contained detectable concentrations of both toxins emphasizing the potential for combined exposure risks. Additionally, fetuses from a beluga whale, a harbor porpoise and a Steller sea lion contained detectable concentrations of DA documenting maternal toxin transfer in these species. These results provide evidence that HAB toxins are present throughout Alaska waters at levels high enough to be detected in marine mammals and have the potential to impact marine mammal health in the Arctic marine environment.

Individual and colony-specific wintering areas of Pacific northern fulmars (Fulmarus glacialis)

Seabird mortality associated with longline fishing in the eastern Bering Sea occurs mainly from September to May, with northern fulmars (Fulmarus glacialis) comprising the majority (60%) of the bycatch. Along the west coast of North America, winter dieoffs of fulmars may be increasing in frequency and magnitude, the most severe on record being a wreck that peaked in October–November 2003. We deployed satellite transmitters on fulmars from the four main Alaska colonies and tracked individuals for up to 2 years. Fulmars from Hall Island (northern Bering Sea) moved to Russian coastal waters after breeding, while Pribilof Island fulmars (southeastern Bering Sea) remained relatively sedentary year-round. Birds from Chagulak Island (eastern Aleutians) preferred passes between the Aleutian Islands in winter or foraged widely over deep waters of the central Bering Sea and North Pacific. Fulmars from the Semidi Islands (western Gulf of Alaska) migrated directly to waters of the California Current. Individuals from...

PHENOTYPIC PLASTICITY IN AGE AT FIRST REPRODUCTION OF FEMALE NORTHERN SEA OTTERS (ENHYDRA LUTRIS KENYONI)

Abstract Life-history theory predicts that within a species, reproduction and survival rates will differ among populations that differ in resource availability or predation rates through phenotypic plasticity. When populations are near carrying capacity (K) or when they are declining due to reduced prey resources, the average age at 1st reproduction (average AFR) is predicted to be older than in populations below K. Differences between the trajectories of northern sea otter (Enhydra lutris kenyoni) populations in Alaska provides an opportunity to examine phenotypic plasticity. Using premolar teeth or reproductive tracts, we estimated average AFR from demographically distinct populations of sea otters in Alaska. We obtained samples from 2 populations near K, Prince William Sound (PWS) and the Aleutian Archipelago (archived samples), and from 2 populations below K, the Kodiak Archipelago and Sitka. The average AFR was lower in populations below K (3.60 years ± 0.16 SD) compared to those near K (4.21 ± 0.13 years, P < 0.001), and differed among all populations, with the Aleutian population possessing the oldest average AFR (4.29 ± 0.09 years) followed by PWS (4.05 ± 0.24 years), Sitka (3.80 ± 0.21 years), and Kodiak (3.19 ± 0.37 years). The difference in average AFR among populations supports life-history theory and provides evidence of phenotypic plasticity in sea otters. Our findings highlight the value of using average AFR as a tool for monitoring mammalian populations.

Mustelid Herpesvirus-2, a Novel Herpes Infection in Northern Sea Otters (Enhydra Lutris Kenyoni)

Oral ulcerations and plaques with epithelial eosinophilic intranuclear inclusions were observed in northern sea otters (Enhydra lutris kenyoni) that died or were admitted for rehabilitation after the 1989 Exxon Valdez oil spill (EVOS) in Alaska, USA. Transmission electron microscopy demonstrated the presence of herpesviral virions. Additionally, a serologic study from 2004 to 2005 found a high prevalence of exposure to a herpesvirus in live-captured otters. Tissues from 29 otters after the EVOS and nasal swabs from 83 live-captured otters in the Kodiak Archipelago were tested for herpesviral DNA. Analysis identified a novel herpesvirus in the gamma subfamily, most closely related to Mustelid herpesvirus-1 from badgers. Results indicated that this herpesvirus is associated with ulcerative lesions but is also commonly found in secretions of healthy northern sea otters.

Evaluating Cementum to Determine Past Reproduction in Northern Sea Otters

Abstract Age at first reproduction (AFR) has been difficult to quantify in mammals, as the most commonly used methods require reproductive tracts or direct observations. However, work in several large mammal species suggests that the width of cementum light bands in teeth decline once females begin to reproduce, suggesting that teeth structures might provide a new tool to examine AFR. To determine if changes in cementum light band width could be used to calculate AFR for the northern sea otter (Enhydra lutris kenyoni), we measured cementum light band widths on sectioned premolar teeth and compared them to reproductive tracts. We classified otters as parous if any single light band was narrower than a threshold value, selected as the value that minimized error rates. At a threshold value of 0.32, we correctly identified otters as parous or nulliparous in 83% of cases (n = 92) as compared to reproductive tracts, and the AFR estimated from teeth samples (3.52 ± 0.032 yr) was not different from that determined by reproductive tract analysis (3.45 ± 0.031 yr; t-test, P > 0.05). These data support the use of cementum as an indicator of past reproduction in individual female otters, which can then be used to estimate average AFR. Given that declines in cementum width have been described for other mammal species, the same quantitative approach used here could be applied to other species.

Novel Bartonella infection in northern and southern sea otters (Enhydra lutris kenyoni and Enhydra lutris nereis)

Since 2002, vegetative valvular endocarditis (VVE), septicemia and meningoencephalitis have contributed to an Unusual Mortality Event (UME) of northern sea otters in southcentral Alaska. Streptococcal organisms were commonly isolated from vegetative lesions and organs from these sea otters. Bartonella infection has also been associated with bacteremia and VVE in terrestrial mammals, but little is known regarding its pathogenic significance in marine mammals. Our study evaluated whether Streptococcus bovis/equinus (SB/E) and Bartonella infections were associated with UME-related disease characterized by VVE and septicemia in Alaskan sea otter carcasses recovered 2004-2008. These bacteria were also evaluated in southern sea otters in California. Streptococcus bovis/equinus were cultured from 45% (23/51) of northern sea otter heart valves, and biochemical testing and sequencing identified these isolates as Streptococcus infantarius subsp. coli. One-third of sea otter hearts were co-infected with Bartonella spp. Our analysis demonstrated that SB/E was strongly associated with UME-related disease in northern sea otters (P<0.001). While Bartonella infection was also detected in 45% (23/51) and 10% (3/30) of heart valves of northern and southern sea otters examined, respectively, it was not associated with disease. Phylogenetic analysis of the Bartonella ITS region allowed detection of two Bartonella species, one novel species closely related to Bartonella spp. JM-1, B. washoensis and Candidatus B. volans and another molecularly identical to B. henselae. Our findings help to elucidate the role of pathogens in northern sea otter mortalities during this UME and suggested that Bartonella spp. is common in sea otters from Alaska and California.

ANTIMICROBIAL SUSCEPTIBILITY OF BACTERIAL ISOLATES FROM SEA OTTERS (ENHYDRA LUTRIS)

Bacterial infections are an important cause of sea otter (Enhydra lutris) mortality, and some of these infections may originate from terrestrial and anthropogenic sources. Antimicrobials are an important therapeutic tool for management of bacterial infections in stranded sea otters and for prevention of infection following invasive procedures in free-ranging otters. In this study, susceptibility to commonly used antimicrobials was determined for 126 isolates of 15 bacterial species or groups from necropsied, live-stranded injured or sick, and apparently healthy wild sea otters examined between 1998 and 2005. These isolates included both gram-positive and gram-negative strains of primary pathogens, opportunistic pathogens, and environmental flora, including bacterial species with proven zoonotic potential. Minimal evidence of antimicrobial resistance and no strains with unusual or clinically significant multiple-drug resistance patterns were identified. Collectively, these findings will help optimize selection of appropriate antimicrobials for treatment of bacterial diseases in sea otters and other marine species.