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Brenda E. Ballachey

Publications and source records attributed to Brenda E. Ballachey.

At least 37 records · Page 2Linked to original sources

Lessons from the 1989 Exxon Valdez oil spill: A biological perspective

On March 24, 1989, the tanker vessel Exxon Valdez altered its course to avoid floating ice, and ran aground on Bligh Reef in northeastern Prince William Sound (PWS), Alaska (Figure 1). The tanker was carrying about 53 million gallons of Prudhoe Bay crude, a heavy oil, and an estimated 11 million gallons spilled (264,000 barrels or about 42 million liters) in what was, prior to the Deepwater Horizon (DWH) spill of 2010, the largest accidental release of oil into U.S. waters (Morris and Loughlin 1994; Spies et al. 1996; Shigenaka 2014). Following the Exxon Valdez oil spill (EVOS), a broad range of studies was implemented and 25 years later, monitoring and research efforts to understand the long-term impacts of the spill continue, although now at a lesser intensity. The Exxon Valdez and DWH spills differed in many ways (Plater 2010; Atlas and Hazen 2011; Sylves and Comfort 2012), but there are also similarities, and lessons from the EVOS experience may offer valuable insights as research efforts proceed in the wake of the DWH spill. Here we provide an overview of the EVOS, summarize key findings from several long-term biological research programs, and conclude with some considerations of lessons learned after two and a half decades of study.

Alaska

Quantifying long-term risks to sea otters from the 1989 'Exxon Valdez' oil spill: reply to Harwell & Gentile (2013)

Recovery of sea otter populations in Prince William Sound (PWS), Alaska, has been delayed for more than 2 decades following the 1989 ‘Exxon Valdez’ oil spill. Harwell & Gentile (2013; Mar Ecol Prog Ser 488:291–296) question our conclusions in Bodkin et al. (2012; Mar Ecol Prog Ser 447:273-287) regarding adverse effects that oil lingering in the environment may have on sea otters. They agree that exposure may continue, but disagree that it constitutes a significant risk to sea otters. In Bodkin et al. (2012), we suggested that subtle effects of chronic exposure were the most reasonable explanation for delayed recovery of the sea otter population in areas of western PWS, where shorelines were most heavily oiled. Here, we provide additional information on the ecology of sea otters that clarifies why the toxicological effects of oral ingestion of oil do not reflect all effects of chronic exposure. The full range of energetic, behavioral, and toxicological concerns must be considered to appraise how chronic exposure to residual oil may constrain recovery of sea otter populations.

Alaska

Long-term effects of the 'Exxon Valdez' oil spill: Sea otter foraging in the intertidal as a pathway of exposure to lingering oil

The protracted recovery of some bird and mammal populations in western Prince William Sound (WPWS), Alaska, and the persistence of spilled 'Exxon Valdez' oil in intertidal sediments, suggests a pathway of exposure to consumers that occupy nearshore habitats. To evaluate the hypothesis that sea otter ( Enhydra lutris ) foraging allows access to lingering oil, we contrast spatial relations between foraging behavior and documented oil distribution. We recovered archival time-depth recorders implanted in 19 sea otters in WPWS, where lingering oil and delayed ecosystem recovery are well documented. Sea otter foraging dives ranged from +2.7 to -92 m below sea level (MLLW), with intertidal accounting for 5 to 38% of all foraging. On average, female sea otters made 16050 intertidal dives per year and 18% of these dives were at depths above the +0.80 m tidal elevation. Males made 4100 intertidal dives per year and 26% of intertidal foraging took place at depths above the +0.80 m tidal elevation. Estimated annual oil encounter rates ranged from 2 to 24 times yr -1 for females, and 2 to 4 times yr -1 for males. Exposure rates increased in spring when intertidal foraging doubled and females were with small pups. In summer 2008, we found sea otter foraging pits on 13.5 of 24.8 km of intertidal shoreline surveyed. Most pits (82%) were within 0.5 m of the zero tidal elevation and 15% were above 0.5 m, the level above which most (65%) lingering oil remains. In August 2008, we detected oil above background concentrations in 18 of 41 (44%) pits excavated by sea otters on beaches with prior evidence of oiling, with total PAH concentrations up to 56000 ng g−1 dry weight. Our estimates of intertidal foraging, the widespread presence of foraging pits in the intertidal, and the presence of oil in and near sea otter foraging pits documents a pathway of exposure from lingering intertidal oil to sea otters foraging in WPWS.

Alaska

Variations of transcript profiles between sea otters Enhydra lutris from Prince William Sound, Alaska, and clinically normal reference otters

Development of blood leukocyte gene transcript profiles has the potential to expand condition assessments beyond those currently available to evaluate wildlife health, including sea otters Enhydra lutris , both individually and as populations. The 10 genes targeted in our study represent multiple physiological systems that play a role in immuno-modulation, inflammation, cell protection, tumor suppression, cellular stress-response, xenobiotic metabolizing enzymes, and antioxidant enzymes. These genes can be modified by biological, physical, or anthropogenic impacts and consequently provide information on the general type of stressors present in a given environment. We compared gene transcript profiles of sea otters sampled in 2008 among areas within Prince William Sound impacted to varying degrees by the 1989 ‘Exxon Valdez’ oil spill with those of captive and wild reference sea otters. Profiles of sea otters from Prince William Sound showed elevated transcription in genes associated with tumor formation, cell death, organic exposure, inflammation, and viral exposure when compared to the reference sea otter group, indicating possible recent and chronic exposure to organic contaminants. Sea otters from historically designated oiled areas within Prince William Sound 19 yr after the oil spill had higher transcription of genes associated with tumor formation, cell death, heat shock, and inflammation than those from areas designated as less impacted by the spill.

Alaska

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 (C T ) 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.

Molecular Ecology Resources

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.

Alaska

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. ??2011 by the Ecological Society of America.

Ecological Applications

Trends in sea otter population abundance in western Prince William Sound, Alaska: Progress toward recovery following the 1989 Exxon Valdez oil spill

Sea otters in western Prince William Sound (WPWS) and elsewhere in the Gulf of Alaska suffered widespread mortality as a result of oiling following the 1989 T/V Exxon Valdez oil spill. Following the spill, extensive efforts have been directed toward identifying and understanding long-term consequences of the spill and the process of recovery. We conducted annual aerial surveys of sea otter abundance from 1993 to 2009 (except for 2001 and 2006) in WPWS. We observed an increasing trend in population abundance at the scale of WPWS through 2000 at an average annual rate of 4 percent: however, at northern Knight Island where oiling was heaviest and sea otter mortality highest, no increase in abundance was evident by 2000. We continued to see significant increase in abundance at the scale of WPWS between 2001 and 2009, with an average annual rate of increase from 1993 to 2009 of 2.6 percent. We estimated the 2009 population size of WPWS to be 3,958 animals (standard error=653), nearly 2,000 animals more than the first post-spill estimate in 1993. Surveys since 2003 also have identified a significant increasing trend at the heavily oiled site in northern Knight Island, averaging about 25 percent annually and resulting in a 2009 estimated population size of 116 animals (standard error=19). Although the 2009 estimate for northern Knight Island remains about 30 percent less than the pre-spill estimate of 165 animals, we interpret this trend as strong evidence of a trajectory toward recovery of spill-affected sea otter populations in WPWS.

Alaska

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.

Alaska

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.

Marine Pollution Bulletin

Modeling the Effects of Mortality on Sea Otter Populations

Conservation and management of sea otters can benefit from managing the magnitude and sex composition of human related mortality, including harvesting within sustainable levels. Using age and sex-specific reproduction and survival rates from field studies, we created matrix population models representing sea otter populations with growth rates of 1.005, 1.072, and 1.145, corresponding to stable, moderate, and rapid rates of change. In each modeled population, we incrementally imposed additional annual mortality over a 20-year period and calculated average annual rates of change (lambda). Additional mortality was applied to (1) males only, (2) at a 1:1 ratio of male to female, and (3) at a 3:1 ratio of male to female. Dependent pups (age 0-0.5) were excluded from the mortality. Maintaining a stable or slightly increasing population was largely dependent on (1) the magnitude of additional mortality, (2) the underlying rate of change in the population during the period of additional mortality, and (3) the extent that females were included in the additional mortality (due to a polygnous reproductive system where one male may breed with more than one female). In stable populations, additional mortality as high as 2.4 percent was sustainable if limited to males only, but was reduced to 1.2 percent when males and females were removed at ratios of 3:1 or 0.5 percent at ratios of 1:1. In moderate growth populations, additional mortality of 9.8 percent (male-only) and 15.0 percent (3:1 male to female) maximized the sustainable mortality about 3-10 ten-fold over the stable population levels. However, if additional mortality consists of males and females at equal proportions, the sustainable rate is 7.7 percent. In rapid growth populations, maximum sustainable levels of mortality as high as 27.3 percent were achieved when the ratio of additional mortality was 3:1 male to female. Although male-only mortality maximized annual harvest in stable populations, high male biased mortality in all simulations eventually led to low proportions of males, leading to instability in projected populations over time. Our findings identify the critical need to understand underlying rates of change that can be acquired only through frequent monitoring of managed populations. Models could be improved through better understanding of the effects of density and demographic and environmental stochasticity on sea otter vital rates. Although our primary objective was to provide information useful in managing harvests of sea otters, our findings have implications for the conservation and management of sea otter populations subjected to other sources of mortality that can be quantified, such as incidental, accidental, or illegal.

Scientific Investigations Report

Stress-related hormones and genetic diversity in sea otters (Enhydra lutris)

Sea otters ( Enhydra lutris ) once ranged throughout the coastal regions of the north Pacific, but were extirpated throughout their range during the fur trade of the 18th and 19th centuries, leaving only small, widely scattered, remnant populations. All extant sea otter populations are believed to have experienced a population bottleneck and thus have lost genetic variation. Populations that undergo severe population reduction and associated inbreeding may suffer from a general reduction in fitness termed inbreeding depression. Inbreeding depression may result in decreased testosterone levels in males, and reduced ability to respond to stressful stimuli associated with an increase in the stress-related adrenal glucocorticoid hormones, cortisol and corticosterone. We investigated correlations of testosterone, cortisol, and corticosterone with genetic diversity in sea otters from five populations. We found a significant negative correlation between genetic diversity and both mean population-level ( r 2 = 0.27, P < 0.001) and individual-level ( r 2 = 0.54, P < 0.001) corticosterone values, as well as a negative correlation between genetic diversity and cortisol at the individual level ( r 2 = 0.17, P = 0.04). No relationship was found between genetic diversity and testosterone ( P = 0.57). The strength of the correlations, especially with corticosterone, suggests potential negative consequences for overall population health, particularly for populations with the lowest genetic diversity.

Marine Mammal Science

Response of Pacific walruses to disturbances from capture and handling activities at a haul-out in Bristol Bay, Alaska

Observations were made on hems of the Pacific walrus (Odobenus rosmarus divergens) to study their response during the capturing and handling of adult males in summer 1995 at a haul-out at Cape Peirce in southwestern Alaska. Three behaviors (alertness, displacement, and dispersal) were quantified from 16 capture sessions. Herd sizes ranged from 622 to 5,289 walruses. Handling of an immobilized walrus consisted of attempts to attach telemetry devices to the tusks and collect various biological samples. Handling activities resulted in an average of about 10-fold or greater levels of behavior in alertness, displacement, and dispersal than during precapture and darting periods. High levels of behavior usually occurred within the first 45 min of handling. In 8 of 10 capture sessions, walruses returned to predisturbance levels of behavior within 40 min of cessation of the handling disturbance. Alertness and displacement were moderately and negatively correlated with herd size during the handling period, which may reflect an effect of a threshold distance from the point of disturbance to responding individuals. Observations of walruses tagged with VHF radio transmitters indicated that the activities from a given capture session did not preclude tagged walruses from using the haul-out over a subsequent 11-wk monitoring period. Moreover, non-tagged walruses continued to extensively use the haul-out during and after the period in which capture sessions were conducted.

Marine Mammal Science

Comparison of cytochrome P450 1A induction in blood and liver cells of sea otters

Sea otters in oiled areas of western PWS had elevated levels of cytochrome P450 1A (CYP1A), a biomarker of hydrocarbon exposure, measured in blood samples collected from otters in 1996- 98. In summer 2001, as part of project 01423, we have proposed to resample CYP1A in blood from sea otters in oiled and unoiled areas of PWS. Herein we describe a complementary effort to project 01423. We propose also to sample liver from the captured sea otters, for assays of CYP1A, and for examination of histopathological changes. Liver CYP1A levels will be compared to those measured in blood from the same individuals. We will also assay for CYP1A in archived frozen liver samples from sea otters that were oiled and died in 1989, to enable comparison of current levels of CYP1A induction with levels in sea otters that had a known high degree of oil exposure. The results of this study will provide a basis for comparison of cytochrome P4501A induction in sea otters in 1989, in 1996-98, and in 2001, and will help determine if there is a decline in CYP1A levels over time.

Alaska

Long-term ecosystem repsonse 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.

Alaska

Correlates to survival of juvenile sea otters in Prince William Sound, Alaska, 1992-1993

We estimated survival of sea otters (Enhydra lutris) for 1 year post weaning during 1992 - 1993 in Prince William Sound (PWS), location of the 1989 Exxon Valdez oil spill. We sampled 38 pups in eastern PWS (EPWS), an unoiled area occupied by sea otters for <15 years, and 33 pups from oiled western PWS (WPWS), occupied for >25 years. We compared survival between areas, sexes, and condition groups. We also examined the relation of blood parameters to survival . Survival was estimated at 0.74 in EPWS and 0.52 in WPWS. Female survival was 0.86 in EPWS and 0.64 in WPWS, whereas male survival was lower, 0.61 in EPWS and 0.44 in WPWS. Sea otters from EPWS were in better condition (mass/length) than WPWS sea otters . Pups in better condition had higher survival in EPWS but not in WPWS. Foraging success was greater in EPWS than in WPWS, consistent with either an effect of length of occupation or the effects of oil on the prey base or a combination of these effects. Area differences in blood parameters suggested liver damage in WPWS sea otters , perhaps resulting from continued exposure to oil. Thus, both length of occupation and oiling history likely influenced juvenile survival in PWS.

Alaska

Patterns and processes of population change in selected nearshore vertebrate predators

Sea otters and harlequin ducks have not fully recovered from the oil spill. This project will explore links between oil exposure and the lack of population recovery, with the intent of understanding constraints to recovery of these species and the nearshore environment. In FY 02, sea otter work will include aerial surveys of distribution and abundance and estimates of age-specific survival rates. Harlequin duck field studies will examine the relationship between survival and CYP1A. Captive experiments on harlequin ducks will examine the relationships between oil exposure and CYP1A induction, and metabolic and behavioral consequences of exposure.

Report

Harlequin duck population recovery following the 'Exxon Valdez' oil spill: Progress, process and constraints

Following the 1989 'Exxon Valdez' oil spill in Prince William Sound, Alaska, we studied the status of recovery of harlequin duck Histrionicus histrionicus populations during 1995 to 1998. We evaluated potential constraints on full recovery, including (1) exposure to residual oil; (2) food limitation; and (3) intrinsic demographic limitations on population growth rates. In this paper, we synthesize the findings from our work and incorporate information from other harlequin duck research and monitoring programs to provide a comprehensive evaluation of the response of this species to the 'Exxon Valdez' spill. We conclude that harlequin duck populations had not fully recovered by 1998. Furthermore, adverse effects continued as many as 9 yr after the oil spill, in contrast to the conventional paradigm that oil spill effects on bird populations are short-lived. These conclusions are based on the findings that (1) elevated cytochrome P450 (CYP1A) induction on oiled areas indicated continued exposure to oil in 1998; (2) adult female winter survival was lower on oiled than unoiled areas during 1995 to 1998; (3) fall population surveys by the Alaska Department of Fish and Game indicated numerical declines in oiled areas during 1995 to 1997; and (4) densities on oiled areas in 1996 and 1997 were lower than expected using models that accounted for effects of habitat attributes. Based on hypothesized links between oil contamination and demography, we suggest that harlequin duck population recovery was constrained primarily by continued oil exposure. Full population recovery will also be delayed by the time necessary for intrinsic population growth to allow return to pre-spill numbers following cessation of residual oil spill effects. Although not all wildlife species were affected by the 'Exxon Valdez' oil spill, and some others may have recovered quickly from any effects, harlequin duck life history characteristics and benthic, nearshore feeding habits make them susceptible to both initial and long-term oil spill effects.

Alaska