Revealing the extent of sea otter impacts on bivalve prey through multi-trophic monitoring and mechanistic models.

Sea otters are apex predators that can exert considerable influence over the nearshore communities they occupy. Since facing near extinction in the early 1900s, sea otters are making a remarkable recovery in Southeast Alaska, particularly in Glacier Bay, the largest protected tidewater glacier fjord in the world. The expansion of sea otters across Glacier Bay offers both a challenge to monitoring and stewardship and an unprecedented opportunity to study the top-down effect of a novel apex predator across a diverse and productive ecosystem. Our goal was to integrate monitoring data across trophic levels, space, and time to quantify and map the predator-prey interaction between sea otters and butter clams Saxidomus gigantea, one of the dominant large bivalves in Glacier Bay and a favoured prey of sea otters. We developed a spatially-referenced mechanistic differential equation model of butter clam dynamics that combined both environmental drivers of local population growth and estimates of otter abundance from aerial survey data. We embedded this model in a Bayesian statistical framework and fit it to clam survey data from 43 intertidal and subtidal sites across Glacier Bay. Prior to substantial sea otter expansion, we found that butter clam density was structured by an environmental gradient driven by distance from glacier (represented by latitude) and a quadratic effect of current speed. Estimates of sea otter attack rate revealed spatial heterogeneity in sea otter impacts and a negative relationship with local shoreline complexity. Sea otter exploitation of productive butter clam habitat substantially reduced the abundance and altered the distribution of butter clams across Glacier Bay, with potential cascading consequences for nearshore community structure and function. Spatial variation in estimated sea otter predation processes further suggests that community context and local environmental conditions mediate the top-down influence of sea otters on a given prey. Overall, our framework provides high-resolution insights about the interaction among components of this food web and could be applied to a variety of other systems involving invasive species, epidemiology or migration.

Ecosystem response persists after a prolonged marine heatwave.

Some of the longest and most comprehensive marine ecosystem monitoring programs were established in the Gulf of Alaska following the environmental disaster of the Exxon Valdez oil spill over 30 years ago. These monitoring programs have been successful in assessing recovery from oil spill impacts, and their continuation decades later has now provided an unparalleled assessment of ecosystem responses to another newly emerging global threat, marine heatwaves. The 2014-2016 northeast Pacific marine heatwave (PMH) in the Gulf of Alaska was the longest lasting heatwave globally over the past decade, with some cooling, but also continued warm conditions through 2019. Our analysis of 187 time series from primary production to commercial fisheries and nearshore intertidal to offshore oceanic domains demonstrate abrupt changes across trophic levels, with many responses persisting up to at least 5 years after the onset of the heatwave. Furthermore, our suite of metrics showed novel community-level groupings relative to at least a decade prior to the heatwave. Given anticipated increases in marine heatwaves under current climate projections, it remains uncertain when or if the Gulf of Alaska ecosystem will return to a pre-PMH state.

Spatial variation in polycyclic aromatic hydrocarbon exposure in Barrow's goldeneye (Bucephala islandica) in coastal British Columbia.

Barrow's goldeneyes are sea ducks that winter throughout coastal British Columbia (BC). Their diet consists primarily of intertidal blue mussels, which can accumulate PAHs; accordingly, goldeneyes may be susceptible to exposure through contaminated prey. In 2014/15, we examined total PAH concentrations in mussels from undeveloped and developed coastal areas of BC. At those same sites, we used EROD to measure hepatic CYP1A induction in goldeneyes. We found higher mussel PAH concentrations at developed coastal sites. Regionally, goldeneyes from southern BC, which has relatively higher coastal development, had higher EROD activity compared to birds from northern BC. Our results suggest goldeneyes wintering in coastal BC were exposed to PAHs through diet, with higher exposure among birds wintering in coastal areas with greater anthropogenic influence. These results suggest the mussel-goldeneye system is suitable as a natural, multi-trophic-level indicator of contemporary hydrocarbon contamination occurrence and exposure useful for establishing oil spill recovery endpoints.

Cessation of oil exposure in harlequin ducks after the Exxon Valdez oil spill: Cytochrome P4501A biomarker evidence.

The authors quantified hepatic hydrocarbon-inducible cytochrome P4501A (CYP1A) expression, as ethoxyresorufin-O-deethylase (EROD) activity, in wintering harlequin ducks (Histrionicus histrionicus) captured in Prince William Sound, Alaska (USA), during 2011, 2013, and 2014 (22-25 yr following the 1989 Exxon Valdez oil spill). Average EROD activity was compared between birds from areas oiled by the spill and those from nearby unoiled areas. The present study replicated studies conducted from 1998 to 2009 demonstrating that harlequin ducks using areas oiled in 1989 had elevated EROD activity, indicative of oil exposure, up to 2 decades post spill. In the present study, it was found that average EROD activity during March 2011 was significantly higher in wintering harlequin ducks captured in oiled areas relative to unoiled areas, which the authors interpret to indicate that harlequin ducks continued to be exposed to residual Exxon Valdez oil up to 22 yr after the original spill. However, the 2011 results also indicated reductions in exposure relative to previous years. Average EROD activity in birds from oiled areas was approximately 2 times that in birds from unoiled areas in 2011, compared with observations from 2005 to 2009, in which EROD activity was 3 to 5 times higher in oiled areas. It was also found that average EROD activity during March 2013 and March 2014 was not elevated in wintering harlequin ducks from oiled areas. The authors interpret these findings to indicate that exposure of harlequin ducks to residual Exxon Valdez oil abated within 24 yr after the original spill. The present study finalizes a timeline of exposure, extending over 2 decades, for a bird species thought to be particularly vulnerable to oil contamination in marine environments. Environ Toxicol Chem 2017;36:1294-1300. Published 2016 Wiley Periodicals Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.

Sampling of Sea Ducks for Influenza A Viruses in Alaska during Winter Provides Lack of Evidence for Epidemiologic Peak of Infection.

Sampling of sea ducks for influenza A viruses in Alaska during winter provided no evidence for an epidemiologic peak of infection. Isolates were recovered, however, that provide information on viral diversity and dispersal that may not be realized through sampling efforts focused on other avian taxa.

A method for quantifying consistency in animal distributions using survey data.

The degree of consistency with which groups of animals use the landscape is determined by a variety of ecological processes that influence their movements and patterns of habitat use. We developed a technique termed Distributional Consistency that uses survey data of unmarked individuals to quantify temporal consistency in their spatial distribution, while accounting for changes in population size. Distributional consistency is quantified by comparing the observed distribution patterns to all theoretically possible distribution patterns of observed individuals, leading to a proportional score between 0 and 1, reflecting increasingly consistent use of sites within a region. The technique can be applied to survey data for any taxa across a range of spatial and temporal scales. We suggest ways in which distributional consistency could provide inferences about the dispersal and habitat decisions of individuals, and the scales at which these decisions operate. Distributional consistency integrates spatial and temporal processes to quantify an important characteristic of different habitats and their use by populations, which in turn will be particularly useful in complimenting and interpreting other ecological measures such as population density and stability. The technique can be applied to many existing data sets to investigate and evaluate a range of important ecological questions using simple survey data.

Cytochrome P4501A biomarker indication of the timeline of chronic exposure of Barrow's goldeneyes to residual Exxon Valdez oil.

We examined hepatic EROD activity, as an indicator of CYP1A induction, in Barrow's goldeneyes captured in areas oiled during the 1989 Exxon Valdez spill and those from nearby unoiled areas. We found that average EROD activity differed between areas during 2005, although the magnitude of the difference was reduced relative to a previous study from 1996/1997, and we found that areas did not differ by 2009. Similarly, we found that the proportion of individuals captured from oiled areas with elevated EROD activity (≥ 2 times unoiled average) declined from 41% in winter 1996/1997 to 10% in 2005 and 15% in 2009. This work adds to a body of literature describing the timelines over which vertebrates were exposed to residual Exxon Valdez oil and indicates that, for Barrow's goldeneyes in Prince William Sound, exposure persisted for many years with evidence of substantially reduced exposure by 2 decades after the spill.

Harlequin Duck population injury and recovery dynamics following the 1989 Exxon Valdez oil spill.

The 1989 Exxon Valdez oil spill caused significant injury to wildlife populations in Prince William Sound, Alaska, USA. Harlequin Ducks (Histrionicus histrionicus) were particularly vulnerable to the spill and have been studied extensively since, leading to one of the most thorough considerations of the consequences of a major oil spill ever undertaken. We compiled demographic and survey data collected since the spill to evaluate the timing and extent of mortality using a population model. During the immediate aftermath of the spill, we estimated a 25% decrease in Harlequin Duck numbers in oiled areas. Survival rates remained depressed in oiled areas 6-9 years after the spill and did not equal those from unoiled areas until at least 11-14 years later. Despite a high degree of site fidelity to wintering sites, immigration was important for recovery dynamics, as the relatively large number of birds from habitats outside the spill zone provided a pool of individuals to facilitate numerical increases. On the basis of these model inputs and assumptions about fecundity rates for the species, we projected a timeline to recovery of 24 years under the most-likely combination of variables, with a range of 16 to 32 years for the best-case and worst-case scenarios, respectively. Our results corroborate assertions from other studies that the effects of spilled oil on wildlife can be expressed over much longer time frames than previously assumed and that the cumulative mortality associated with chronic exposure to residual oil may actually exceed acute mortality, which has been the primary concern following most oil spills.

Survival of captive and free-ranging Harlequin Ducks (Histrionicus histrionicus) following surgical liver biopsy.

We measured intra- and postoperative mortality rates of captive and free-ranging Harlequin Ducks (Histrionicus histrionicus) undergoing surgical liver biopsy sampling for determination of the induction of cytochrome P4501A, a biomarker of oil exposure. Liver biopsies were taken from and radio transmitters were implanted into 157 free-ranging Harlequin Ducks over three winters (55 in 2000, 55 in 2001, and 47 in 2002). No birds died during surgery, but seven (4.5%) died during recovery from anesthesia (three in 2001 and four in 2002). None of the deaths could be attributed directly to the liver biopsy. Four of the 150 (2.7%) birds that were released died in the 2 wk period after surgery. All post-release deaths occurred in 2001; no birds died after release in 2000 or 2002. No mortalities of 36 captive birds occurred during surgery or recovery or in the 2 wk period following surgery. Hemorrhage was a minor problem with one captive bird. Surgical liver biopsies appear to be a safe procedure, but anesthetic complications may occur with overwintering ducks.

Cytochrome P4501A biomarker indication of oil exposure in harlequin ducks up to 20 years after the Exxon Valdez oil spill.

Hydrocarbon-inducible cytochrome P4501A (CYP1A) expression was measured, as ethoxyresorufin-O-deethylase (EROD) activity, in livers of wintering harlequin ducks (Histrionicus histrionicus) captured in areas of Prince William Sound, Alaska, USA, oiled by the 1989 Exxon Valdez spill and in birds from nearby unoiled areas, during 2005 to 2009 (up to 20 years following the spill). The present work repeated studies conducted in 1998 that demonstrated that in harlequin ducks using areas that received Exxon Valdez oil, EROD activity was elevated nearly a decade after the spill. The present findings strongly supported the conclusion that average levels of hepatic EROD activity were higher in ducks from oiled areas than those from unoiled areas during 2005 to 2009. This result was consistent across four sampling periods; furthermore, results generated from two independent laboratories using paired liver samples from one of the sampling periods were similar. The EROD activity did not vary in relation to age, sex, or body mass of individuals, nor did it vary strongly by season in birds collected early and late in the winter of 2006 to 2007, indicating that these factors did not confound inferences about observed differences between oiled and unoiled areas. We interpret these results to indicate that harlequin ducks continued to be exposed to residual Exxon Valdez oil up to 20 years after the original spill. This adds to a growing body of literature suggesting that oil spills have the potential to affect wildlife for much longer time frames than previously assumed.

Evaluation of a Portable Automated Serum Chemistry Analyzer for Field Assessment of Harlequin Ducks, Histrionicus histrionicus.

A portable analytical chemistry analyzer was used to make field assessments of wild harlequin ducks (Histrionicus histrionicus) in association with telemetry studies of winter survival in Prince William Sound, Alaska. We compared serum chemistry results obtained on-site with results from a traditional laboratory. Particular attention was paid to serum glucose and potassium concentrations as potential indicators of high-risk surgical candidates based on evaluation of the field data. The median differential for glucose values (N = 82) between methods was 0.6 mmol/L (quartiles 0.3 and 0.9 mmol/L) with the median value higher when assayed on site. Analysis of potassium on site returned a median of 2.7 mmol/L (N = 88; quartiles 2.4 and 3.0 mmol/L). Serum potassium values were too low for quantitation by the traditional laboratory. Changes in several serum chemistry values following a three-day storm during the study support the value of on site evaluation of serum potassium to identify presurgical patients with increased anesthetic risk.

PCB exposure in sea otters and harlequin ducks in relation to history of contamination by the Exxon Valdez oil spill.

Exposure to contaminants other than petroleum hydrocarbons could confound interpretation of Exxon Valdez oil spill effects on biota at Prince William Sound, Alaska. Hence, we investigated polychlorinated biphenyls (PCBs) in blood of sea otters and harlequin ducks sampled during 1998. PCB concentrations characterized by lower chlorinated congeners were highest in sea otters from the unoiled area, whereas concentrations were similar among harlequin ducks from the oiled and unoiled area. Blood enzymes often elevated by xenobiotics were not related to PCB concentrations in sea otters. Only sea otters from the unoiled area had estimated risk from PCBs, and PCB composition or concentrations did not correspond to reported lower measures of population performance in sea otters or harlequin ducks from the oiled area. PCBs probably did not influence limited sea otter or harlequin duck recovery in the oiled area a decade after the spill.

Plasma yolk precursor dynamics during egg production by female greater scaup (Aythya marila): Characterization and indices of reproductive state.

We characterized dynamics of the plasma yolk precursors vitellogenin (VTG), very-low-density lipoprotein (total VLDL-TG), and VLDL particle size distribution during egg production by female greater scaup (order: Anseriformes, Aythya marila). We also evaluated VTG and total VLDL-TG as physiological indices of reproductive state. Mean (+/-1 SE) plasma concentrations of VTG and total VLDL-TG for females with nondeveloped ovaries were 0.58 +/- 0.05 microg Zn mL(-1) and 3.75 +/- 0.29 mmol TG L(-1), respectively. Yolk precursor concentrations increased rapidly to maximum levels in association with small increases in ovary mass during rapid follicle growth. Mean concentrations of VTG and total VLDL-TG for females with a full ovarian follicle hierarchy were 3.38 +/- 0.40 microg Zn mL(-1) and 7.31 +/- 2.56 mmol TG L(-1), respectively. Concentrations of VTG and total VLDL remained elevated throughout the laying cycle and decreased markedly by 3 d into incubation. Individual reproductive state (non-egg producing vs. egg producing) was more accurately identified by plasma profiles of VTG (90%) than by those of total VLDL-TG (74%). Greater scaup VLDL particle sizes during egg production were within the range for predicted yolk-targeted VLDL size (25-44 nm). We conclude that plasma profiles of VTG and total VLDL-TG can be used as nonlethal, physiological indices of reproductive state in greater scaup and should be of great utility to a variety of evolutionary, ecological, and applied conservation studies of reproduction in waterfowl.

A blood survey of elements, viral antibodies, and hemoparasites in wintering Harlequin Ducks (Histrionicus histrionicus) and Barrow's Goldeneyes (Bucephala islandica).

Twenty-eight Harlequin Ducks (Histrionicus histrionicus) and 26 Barrow's Goldeneyes (Bucephala islandica) were captured in Prince William Sound, Alaska, between 1 and 15 March 2005. Blood was collected for quantification of element concentrations, prevalence of antibodies to several viruses, and hemoparasite prevalence and identification. Although we found selenium concentrations that have been associated with selenosis in some birds (>or=2.0 ppm ww), our findings contribute to a growing literature describing relatively high selenium in apparently healthy birds in marine environments. Avian influenza virus antibodies were detected in the plasma of 28% of the ducks. No antibodies against adenovirus, reovirus, or paramyxovirus 1 were detected. Several hemo-parasite species were identified in 7% of ducks. Our findings are similar to those in other free-living marine waterfowl and do not indicate unusual concerns for the health of these species in this area in late winter.

Effects of ACTH, capture, and short term confinement on glucocorticoid concentrations in harlequin ducks (Histrionicus histrionicus).

Little is known about baseline concentrations of adrenal hormones and hormonal responses to stress in sea ducks, although significant population declines documented in several species suggest that sea ducks are exposed to increased levels of environmental stress. Such declines have been observed in geographically distinct harlequin duck populations. We performed an adrenocorticotropic hormone (ACTH) challenge to evaluate adrenal function and characterize corticosterone concentrations in captive harlequin ducks and investigated the effects of capture, surgery, and short term confinement on corticosterone concentrations in wild harlequin ducks. Harlequin ducks responded to the ACTH challenge with an average three-fold increase in serum corticosterone concentration approximately 90 min post injection, and a four- to five-fold increase in fecal glucocorticoid concentration 2 to 4 h post injection. Serum corticosterone concentrations in wild harlequin ducks increased within min of capture and elevated levels were found for several hours post capture, indicating that surgery and confinement maintain elevated corticosterone concentrations in this species. Mean corticosterone concentrations in wild harlequin ducks held in temporary captivity were similar to the maximum response levels during the ACTH challenge in captive birds. However, large variation among individuals was observed in responses of wild birds, and we found additional evidence suggesting that corticosterone responses varied between hatch year and after hatch year birds.

Movements of wintering surf scoters: predator responses to different prey landscapes.

The distribution of predators is widely recognized to be intimately linked to the distribution of their prey. Foraging theory suggests that predators will modify their behaviors, including movements, to optimize net energy intake when faced with variation in prey attributes or abundance. While many studies have documented changes in movement patterns of animals in response to temporal changes in food, very few have contrasted movements of a single predator species naturally occurring in dramatically different prey landscapes. We documented variation in the winter movements, foraging range size, site fidelity, and distribution patterns of a molluscivorous sea duck, the surf scoter (Melanitta perspicillata), in two areas of coastal British Columbia with very different shellfish prey features. Baynes Sound has extensive tidal flats with abundant clams, which are high-quality and temporally stable prey for scoters. Malaspina Inlet is a rocky fjord-like inlet where scoters consume mussels that are superabundant and easily accessible in some patches but are heavily depleted over the course of winter. We used radio telemetry to track surf scoter movements in both areas and found that in the clam habitats of Baynes Sound, surf scoters exhibited limited movement, small winter ranges, strong foraging site fidelity, and very consistent distribution patterns. By contrast, in mussel habitats in the Malaspina Inlet, surf scoters displayed more movement, larger ranges, little fidelity to specific foraging sites, and more variable distribution patterns. We conclude that features associated with the different prey types, particularly the higher depletion rates of mussels, strongly influenced seasonal space use patterns. These findings are consistent with foraging theory and confirm that predator behavior, specifically movements, is environmentally mediated.

Inflammatory reaction to fabric collars from percutaneous antennas attached to intracoelomic radio transmitters implanted in harlequin ducks (Histrionicus histrionicus).

In wild birds implanted intracoelomically with radio transmitters, a synthetic fabric collar placed around the base of a percutaneous antenna is believed to function as a barrier to contamination of the coelom. We examined 13 fabric collars recovered from percutaneous antennas of radio transmitters implanted intracoelomically in harlequin ducks (Histrionicus histrionicus) 12 months earlier. Both the transmitters and antenna collars were encapsulated in fibrous connective tissue, with adhesions to internal organs. Histologically, bacteria were evident at the fabric-plastic interface in 8 of 10 collars examined in cross section and along the length of the collar in 3 collars examined longitudinally. Bacteria were confined within the fibrotic sheath surrounding the transmitter and the antenna collar in all birds. No evidence of chronic systemic effects secondary to implantation was present on hematologic or serum biochemical testing. These findings indicate that antenna collars do not prevent the entry of bacteria along the percutaneous antenna but may help stabilize the antenna and minimize coelomic contamination. We conclude that radio transmitters implanted into the coelom of harlequin ducks do not appear to cause significant health problems for at least 1 year after implantation.

Long-term ecosystem response to the Exxon Valdez oil spill.

The ecosystem response to the 1989 spill of oil from the Exxon Valdez into Prince William Sound, Alaska, shows that current practices for assessing ecological risks of oil in the oceans and, by extension, other toxic sources should be changed. Previously, it was assumed that impacts to populations derive almost exclusively from acute mortality. However, in the Alaskan coastal ecosystem, unexpected persistence of toxic subsurface oil and chronic exposures, even at sublethal levels, have continued to affect wildlife. Delayed population reductions and cascades of indirect effects postponed recovery. Development of ecosystem-based toxicology is required to understand and ultimately predict chronic, delayed, and indirect long-term risks and impacts.